(2023) Nature Communications. 14, 269. Abstract
It has long been debated how humans resolve fine details and perceive a stable visual world despite the incessant fixational motion of their eyes. Current theories assume these processes to rely solely on the visual input to the retina, without contributions from motor and/or proprioceptive sources. Here we show that contrary to this widespread assumption, the visual system has access to high-resolution extra-retinal knowledge of fixational eye motion and uses it to deduce spatial relations. Building on recent advances in gaze-contingent display control, we created a spatial discrimination task in which the stimulus configuration was entirely determined by oculomotor activity. Our results show that humans correctly infer geometrical relations in the absence of spatial information on the retina and accurately combine high-resolution extraretinal monitoring of gaze displacement with retinal signals. These findings reveal a sensory-motor strategy for encoding space, in which fine oculomotor knowledge is used to interpret the fixational input to the retina.
(2022) AbstractVisual hyperacuity with moving sensor and recurrent neural computations
Dynamical phenomena, such as recurrent neuronal activity and perpetual motion of the eye, are typically overlooked in models of bottom-up visual perception. Recent experiments suggest that tiny inter-saccadic eye motion ("fixational drift") enhances visual acuity beyond the limit imposed by the density of retinal photoreceptors. Here we hypothesize that such an enhancement is enabled by recurrent neuronal computations in early visual areas. Specifically, we explore a setting involving a low-resolution dynamical sensor that moves with respect to a static scene, with drift-like tiny steps. This setting mimics a dynamical eye viewing objects in perceptually-challenging conditions. The dynamical sensory input is classified by a convolutional neural network with recurrent connectivity added to its lower layers, in analogy to recurrent connectivity in early visual areas. Applying our system to CIFAR-10 and CIFAR-100 datasets down-sampled via 8x8 sensor, we found that (i) classification accuracy, which is drastically reduced by this down-sampling, is mostly restored to its 32x32 baseline level when using a moving sensor and recurrent connectivity, (ii) in this setting, neurons in the early layers exhibit a wide repertoire of selectivity patterns, spanning the spatiotemporal selectivity space, with neurons preferring different combinations of spatial and temporal patterning, and (iii) curved sensor's trajectories improve visual acuity compared to straight trajectories, echoing recent experimental findings involving eye-tracking in challenging conditions. Our work sheds light on the possible role of recurrent connectivity in early vision as well as the roles of fixational drift and temporal-frequency selective cells in the visual system. It also proposes a solution for artificial image recognition in settings with limited resolution and multiple time samples, such as in edge AI applications.
(2022) Scientific Reports. 12, 1, p. 2922-2922 Abstract
Hand movements are essential for tactile perception of objects. However, the specific functions served by active touch strategies, and their dependence on physiological parameters, are unclear and understudied. Focusing on planar shape perception, we tracked at high resolution the hands of 11 participants during shape recognition task. Two dominant hand movement strategies were identified: contour following and scanning. Contour following movements were either tangential to the contour or oscillating perpendicular to it. Scanning movements crossed between distant parts of the shapes' contour. Both strategies exhibited non-uniform coverage of the shapes' contours. Idiosyncratic movement patterns were specific to the sensed object. In a second experiment, we have measured the participants' spatial and temporal tactile thresholds. Significant portions of the variations in hand speed and in oscillation patterns could be explained by the idiosyncratic thresholds. Using data-driven simulations, we show how specific strategy choices may affect receptors activation. These results suggest that motion strategies of active touch adapt to both the sensed object and to the perceiver's physiological parameters.
(2021) Neuron (Cambridge, Mass.). 109, 22, p. 3542-3544 Abstract
The neural basis of time perception remains an enigma. In rats performing interval judgment tasks, striatal time coding has drawn attention as one potential substrate. Toso et al. (2021b) find that such time coding does not account for stimulus duration perception.
(2021) Proceedings of the National Academy of Sciences - PNAS. 118, 34, e202279211. Abstract
Natural vision is a dynamic and continuous process. Under natural conditions, visual object recognition typically involves continuous interactions between ocular motion and visual contrasts, resulting in dynamic retinal activations. In order to identify the dynamic variables that participate in this process and are relevant for image recognition, we used a set of images that are just above and below the human recognition threshold and whose recognition typically requires >2 s of viewing. We recorded eye movements of participants while attempting to recognize these images within trials lasting 3 s. We then assessed the activation dynamics of retinal ganglion cells resulting from ocular dynamics using a computational model. We found that while the saccadic rate was similar between recognized and unrecognized trials, the fixational ocular speed was significantly larger for unrecognized trials. Interestingly, however, retinal activation level was significantly lower during these unrecognized trials. We used retinal activation patterns and oculomotor parameters of each fixation to train a binary classifier, classifying recognized from unrecognized trials. Only retinal activation patterns could predict recognition, reaching 80% correct classifications on the fourth fixation (on average, ∼2.5 s from trial onset). We thus conclude that the information that is relevant for visual perception is embedded in the dynamic interactions between the oculomotor sequence and the image. Hence, our results suggest that ocular dynamics play an important role in recognition and that understanding the dynamics of retinal activation is crucial for understanding natural vision.
(2021) The Journal of Neuroscience. 41, 22, p. 4826-4839 Abstract
Perception is an active process, requiring the integration of both proprioceptive and exteroceptive information. In the rat's vibrissal system, a classical model for active sensing, the relative contribution of the two information streams was previously studied at the peripheral, thalamic and cortical levels. Contributions of brainstem neurons were only indirectly inferred for some trigeminal nuclei according to their thalamic projections. The current work addressed this knowledge gap by performing the first comparative study of the encoding of proprioceptive whisking and exteroceptive touch signals in the oralis (SpVo), interpolaris (SpVi) and paratrigeminal (Pa5) brainstem nuclei. We used artificial whisking in anesthetized male rats, which allows a systematic analysis of the relative contribution of the proprioceptive and exteroceptive information streams along the ascending pathways in the absence of motor or cognitive top-down modulations. We found that (i) neurons in the rostral and caudal parts of the SpVi convey whisking and touch information, respectively, as predicted by their thalamic projections; (ii) neurons in the SpVo encode both whisking and touch information and (iii) neurons of the Pa5 encode a complex combination of whisking and touch information. In particular, the Pa5 contains a relatively large fraction of neurons that are inhibited by active touch, a response observed so far only in the thalamus. Overall, our systematic characterization of afferent responses to active touch in the trigeminal brainstem approves the hypothesized functions of SpVi neurons and present evidence that SpVo and Pa5 neurons are involved in the processing of active vibrissal touch.
The present work constitutes the first comparative study of the encoding of proprioceptive (whisking) and exteroceptive (touch) information in the rat's brainstem trigeminal nuclei, the first stage of vibrissal processing in the central nervous system. It shows that (i) as expected, the rostral and caudal interpolaris neurons convey primarily whisking and touch information, respectively, (ii) the oralis nucleus, whose function was previously unknown, encodes primarily touch information, (iii) a subtractive computation, reported at the thalamic level, already occurs at the brainstem level and (iv) a novel afferent pathway probably ascends via the paratrigeminal nucleus, encoding both proprioceptive and exteroceptive information.
(2021) Anatomical Record. 304, 2, p. 400-412 Abstract
In whisking rodents, mystacial pad is supplied with vibrissae and contains a collagenous skeleton that is a part of the snout fascia. Collagenous skeleton is built of fibrillary, spongy and tough connective tissue that splits into three interconnected layers: superficial, deep spongy mesh and subcapsular fibrous mat. The integrity of the collagenous skeleton is maintained by tough follicular capsules of which ends are embedded into superficial layer and subcapsular fibrous mat. To move vibrissae, the forces of intrinsic muscles are applied directly to the capsules of the vibrissa follicles, whereas the forces of extrinsic muscles, to other parts of the collagenous skeleton which transmit the forces to the capsules. According to the spatial distribution and anchoring sites of the muscles and fascia, extrinsic muscles provide vibrissa protraction or retraction by pulling superficial layer of the collagenous skeleton rostral or caudal, respectively. Vibrissae can be also retracted when the efforts of extrinsic muscles are applied to the subcapsular fibrous mat that has a matrix composed of oriented rostro‐caudal wavy fibrils. When the muscles relax, vibrissae return to their resting position. Deep spongy layer encompasses vibrissal follicles providing a uniform distribution of stresses and strains during whisking. In the mystacial pad, fascia is a dominant type of tissue that maintains integrity of the vibrissa motor plant, translates muscular momentum to the vibrissae and plays a role in vibrissae movements.
(2021) iScience. 24, 1, 101918. Abstract
We examined the development of new sensing abilities in adults by training participants to perceive remote objects through their fingers. Using an Active-Sensing based sensory Substitution device (ASenSub), participants quickly learned to perceive fast via the new modality and preserved their high performance for more than 20 months. Both sighted and blind participants exhibited almost complete transfer of performance from 2D images to novel 3D physical objects. Perceptual accuracy and speed using the ASenSub were, on average, 300% and 600% better than previous reports for 2D images and 3D objects. This improvement is attributed to the ability of the participants to employ their own motor-sensory strategies. Sighted participants dominant strategy was based on motor-sensory convergence on the most informative regions of objects, similarly to fixation patterns in vision. Congenitally, blind participants did not show such a tendency, and many of their exploratory procedures resembled those observed with natural touch.
(2020) PLoS ONE. 15, 10 , 0240660. Abstract
Vision is obtained with a continuous motion of the eyes. The kinematic analysis of eye motion, during any visual or ocular task, typically reveals two (kinematic) components: saccades, which quickly replace the visual content in the retinal fovea, and drifts, which slowly scan the image after each saccade. While the saccadic exchange of regions of interest (ROIs) is commonly considered to be included in motor-sensory closed-loops, it is commonly assumed that drifts function in an open-loop manner, that is, independent of the concurrent visual input. Accordingly, visual perception is assumed to be based on a sequence of open-loop processes, each initiated by a saccade-triggered retinal snapshot. Here we directly challenged this assumption by testing the dependency of drift kinematics on concurrent visual inputs using real-time gaze-contingent-display. Our results demonstrate a dependency of the trajectory on the concurrent visual input, convergence of speed to condition-specific values and maintenance of selected drift-related motor-sensory controlled variables, all strongly indicative of drifts being included in a closed-loop brain-world process, and thus suggesting that vision is inherently a closed-loop process.
(2020) PLoS Biology. 18, 5, 3000571. Abstract
Animals actively move their sensory organs in order to acquire sensory information. Some rodents, such as mice and rats, employ cyclic scanning motions of their facial whiskers to explore their proximal surrounding, a behavior known as whisking. Here, we investigated the contingency of whisking kinematics on the animal's behavioral context that arises from both internal processes (attention and expectations) and external constraints (available sensory and motor degrees of freedom). We recorded rat whisking at high temporal resolution in 2 experimental contexts-freely moving or head-fixed-and 2 spatial sensory configurations-a single row or 3 caudal whiskers on each side of the snout. We found that rapid sensorimotor twitches, called pumps, occurring during free-air whisking carry information about the rat's upcoming exploratory direction, as demonstrated by the ability of these pumps to predict consequent head and body locomotion. Specifically, pump behavior during both voluntary motionlessness and imposed head fixation exposed a backward redistribution of sensorimotor exploratory resources. Further, head-fixed rats employed a wide range of whisking profiles to compensate for the loss of head- and body-motor degrees of freedom. Finally, changing the number of intact vibrissae available to a rat resulted in an alteration of whisking strategy consistent with the rat actively reallocating its remaining resources. In sum, this work shows that rats adapt their active exploratory behavior in a "homeostatic" attempt to preserve sensorimotor coverage under changing environmental conditions and changing sensory capacities, including those imposed by various laboratory conditions.
An Observer-inclusive Hypothesis Suggesting a Reduction of the Perceived Universe to String Interactions
Physics and neuroscience share overlapping objectives, the major of which is probably the attempt to reduce the observed universe to a set of rules. The approaches are complementary, attempting to find a reduced description of the universe or of the observer, respectively. We propose here that combining the two approaches within an observer-inclusive physical scheme, bears significant advantages. In such a scheme, the same set of rules applies to the universe and its observers, and the two descriptions are entangled. We show here that analyzing special relativity in an observer-inclusive framework can resolve its contradiction with the observed non-locality of physical interactions. The contradiction is resolved by reducing the universe (including the observer) to a dynamic distribution of closed strings (“ceons”) whose vibration waves travel at c. This ceons model is consistent with special and general relativity, non-locality and the holographic principle; it also eliminates Zeno’s motion paradoxes. Yet, the model entails several new empirical predictions. Finally, the ceons model suggests a fundamental physical implementation of active biological perception. Paraphrasing Torricelli, this paper suggests that we live submerged in a c of light.
(2019) Frontiers in Integrative Neuroscience. 13, 64. Abstract
Rats can be trained to associate relative spatial locations of objects with the spatial location of rewards. Here we ask whether rats can localize static silent objects with other body parts in the dark, and if so with what resolution. We addressed these questions in trained rats, whose interactions with the objects were tracked at high-resolution before and after whisker trimming. We found that rats can use other body parts, such as trunk and ears, to localize objects. Localization resolution with non-whisking body parts (henceforth, ‘body’) was poorer than that obtained with whiskers, even when left with a single whisker at each side. Part of the superiority of whiskers was obtained via the use of multiple contacts. Transfer from whisker to body localization occurred within one session, provided that body contacts with the objects occurred before whisker trimming, or in the next session otherwise. This transfer occurred whether temporal cues were used for discrimination or when discrimination was based on spatial cues alone. Rats’ decision in each trial was based on the sensory cues acquired in that trial and on decisions and reward locations in previous trials. When sensory cues were acquired by body contacts, rat decisions relied more on the reward location in previous trials. Overall, the results suggest that rats can generalize the idea of relative object location across different body parts, while preferring to rely on whiskers-based localization, which occurs earlier and conveys higher resolution.
(2019) Scholarpedia journal. 14, 3, 52463. Abstract
How do we perceive our environment? Despite decades of intensive research the scientific community does not seem to converge on an agreed direction. To begin with, there is no agreement about the general scheme of perception: is perception ‘direct’ or ‘indirect’? Does it depend on active sensor movements? Is it based on the construction of internal representations? Moreover, the neurobiology of perception seems to progress for the most part independently of its theory; partially, arguably, due to the lack of a structured theoretical landscape. This article proposes a structured theoretical landscape, which, despite its simplicity (or in fact thanks to its simplicity), can form an initial step towards productive theory-experiment dialogue.
(2018) Journal of Physiological Sciences. 68, 6, p. 875-880 Abstract
A self-adjusting head holder is designed to allow stable fixation and precise positioning (anterior-posterior, pitch, and roll) of guinea pig head in stereotaxic devices. These are achieved with no use of ear-bars. It is thus easy to use, preferable for studies of the auditory system, and for avoiding tissue damage of the ear in general. This head holder can accommodate various head sizes and is thus adapted for males and females of a large range of body weights, as confirmed for guinea pigs of 360-940g. Moreover, this head holder is easy and cost-effective to manufacture, making it accessible for any lab. Here, we present background and mechanical rationale, the technical specifications, and step-by-step manufacturing instructions for the stainless-steel and the plastic MRI-compatible versions of our self-adjusting head holder.
(2018) Trends in Cognitive Sciences. 22, 10, p. 883-895 Abstract
Establishing a representation of space is a major goal of sensory systems. Spatial information, however, is not always explicit in the incoming sensory signals. In most modalities it needs to be actively extracted from cues embedded in the temporal flow of receptor activation. Vision, on the other hand, starts with a sophisticated optical imaging system that explicitly preserves spatial information on the retina. This may lead to the assumption that vision is predominantly a spatial process: all that is needed is to transmit the retinal image to the cortex, like uploading a digital photograph, to establish a spatial map of the world. However, this deceptively simple analogy is inconsistent with theoretical models and experiments that study visual processing in the context of normal motor behavior. We argue here that, as with other senses, vision relies heavily on temporal strategies and temporal neural codes to extract and represent spatial information.
(2017) Neuron. 96, 4, p. 730-735 Abstract
Science is ideally suited to connect people from different cultures and thereby foster mutual understanding. To promote international life science collaboration, we have launched "The Science Bridge'' initiative. Our current project focuses on partnership between Western and Middle Eastern neuroscience communities.[All authors]
(2017) Anatomical Record. 300, 9, p. 1643-1653 Abstract
Whisking mammals move their whiskers in the rostrocaudal and dorsoventral directions with simultaneous rolling about their long axes (torsion). Whereas muscular control of the first two types of whisker movement was already established, the anatomic muscular substrate of the whisker torsion remains unclear. Specifically, it was not clear whether torsion is induced by asymmetrical operation of known muscles or by other largely unknown muscles. Here, we report that mystacial pads of newborn and adult rats and mice contain oblique intrinsic muscles (OMs) that connect diagonally adjacent vibrissa follicles. Each of the OMs is supplied by a cluster of motor end plates. In rows A and B, OMs connect the ventral part of the rostral follicle with the dorsal part of the caudal follicle. In rows C-E, in contrast, OMs connect the dorsal part of the rostral follicle to the ventral part of the caudal follicle. This inverse architecture is consistent with previous behavioral observations [Knutsen et al.: Neuron 59 (2008) 35-42]. In newborn mice, torsion occurred in irregular single twitches. In adult anesthetized rats, microelectrode mediated electrical stimulation of an individual OM that is coupled with two adjacent whiskers was sufficient to induce a unidirectional torsion of both whiskers. Torsional movement was associated with protracting movement, indicating that in the vibrissal system, like in the ocular system, torsional movement is mechanically coupled to horizontal and vertical movements. This study shows that torsional whisker rotation is mediated by specific OMs whose morphology and attachment sites determine rotation direction and mechanical coupling, and motor innervation determines rotation dynamics.
(2017) Current Biology. 27, 12, p. 1836-1843 Abstract
Rats' large whiskers (macrovibrissae) are used to explore their nearby environment, typically using repetitive protraction-retraction "whisking'' motions that are coordinated with head and body movements [1-8]. Once objects are detected, the rat can further explore the object tactually by using both the macrovibrissae and an array of shorter, stationary microvibrissae on the chin, as well as by using the lips [9-11]. When touch occurs during whisking, a fast reflexive response, termeda touch-inducedpump(TIP), may be triggered. During a TIP, the whisker slightly retracts and protracts again, doubling the number of pressure onsets per contact. In head-fixed rats, TIPs occur in similar to 25% of the contacts . Here we report that the occurrence of TIPs depends strongly on attention, indicated by head-turning toward an object: when rats intended to explore an object, either after encountering it during free exploration or when expecting its existence, the probability of a TIP increased from 65% without an increase in TIP latency. TIP regulation was unilateral and specific to the attended object; when two objects were palpated bilaterally simultaneously, TIP probability increased to >65% and decreased to
(2017) Neuron. 94, 3, p. 423-425 Abstract
Understanding how perception emerges depends on the understanding of sensory acquisition by sensory organs. In this issue of Neuron, Severson et al. (2017) present a brilliant leap towards understanding active sensory coding by mechanoreceptors.
(2016) eLife. 5, 12830. Abstract
Perception of external objects involves sensory acquisition via the relevant sensory organs. A widely-accepted assumption is that the sensory organ is the first station in a serial chain of processing circuits leading to an internal circuit in which a percept emerges. This open-loop scheme, in which the interaction between the sensory organ and the environment is not affected by its concurrent downstream neuronal processing, is strongly challenged by behavioral and anatomical data. We present here a hypothesis in which the perception of external objects is a closed-loop dynamical process encompassing loops that integrate the organism and its environment and converging towards organism-environment steady-states. We discuss the consistency of closed-loop perception (CLP) with empirical data and show that it can be synthesized in a robotic setup. Testable predictions are proposed for empirical distinction between open and closed loop schemes of perception.
(2016) Nature Neuroscience. 19, 3, p. 487-+ Abstract
To attribute spatial meaning to sensory information, the state of the sensory organ must be represented in the nervous system. In the rodent's vibrissal system, the whisking-cycle phase has been identified as a key coordinate, and phase-based representation of touch has been reported in the somatosensory cortex. Where and how phase is extracted in the ascending afferent pathways remains unknown. Using a closed-loop interface in anesthetized rats, we found that whisking phase is already encoded in a frequency-and amplitude-invariant manner by primary vibrissal afferents. We found that, for naturally constrained whisking dynamics, such invariant phase coding could be obtained by tuning each receptor to a restricted kinematic subspace. Invariant phase coding was preserved in the brainstem, where paralemniscal neurons filtered out the slowly evolving offset, whereas lemniscal neurons preserved it. These results demonstrate accurate, perceptually relevant, mechanically based processing at the sensor level.
Errata to "Structure-function correlations of rat trigeminal primary neurons: Emphasis on club-like endings, a vibrissal mechanoreceptor" (vol 91, pg 560)
In this paper, the phrases should be corrected as follows:(page 575, ref. 20)For “parent”Read “trunk”(page 576, ref. 39)For “peroxidise”Read “peroxidase”[All authors]
(2016) Vision Research. 118, p. 25-30 Abstract
During natural viewing large saccades shift the visual gaze from one target to another every few hundreds of milliseconds. The role of microsaccades (MSs), small saccades that show up during long fixations, is still debated. A major debate is whether MSs are used to redirect the visual gaze to a new location or to encode visual information through their movement. We argue that these two functions cannot be optimized simultaneously and present several pieces of evidence suggesting that MSs redirect the visual gaze and that the visual details are sampled and encoded by ocular drifts. We show that drift movements are indeed suitable for visual encoding. Yet, it is not clear to what extent drift movements are controlled by the visual system, and to what extent they interact with saccadic movements. We analyze several possible control schemes for saccadic and drift movements and propose experiments that can discriminate between them. We present the results of preliminary analyses of existing data as a sanity check to the testability of our predictions. (C) 2014 Elsevier Ltd. All rights reserved.
(2016) Closed Loop Neuroscience. El Hady A.(eds.). London, UK: . p. 93-100 Abstract
One hundred and twenty years ago, the American philosopher and psychologist John Dewey published his seminal paper The Reflex Arc Concept in Psychology in the Psychological Review. In this essay Dewey claims that the model of a reflex arc is a misguided and partial concept; “what we have is a circuit, not an arc or broken segment of a circle,” says Dewey, who termed this complete circuit coordination—a dynamic sensory-motor process that underlies perception. Despite extensive evidence demonstrating the necessary connection between action and sensation, the arc paradigm Dewey opposed remains to this day the guiding framework to which almost all neuroscientific endeavors adhere to. This bias stems from the prevailing experimental methodology and in particular, from the definitions of stimulus and response. Here we propose closed-loop methodology, complemented by Dewey's functional definitions of stimulus and response, as a possible framework for the advancement of the dynamical circuit interpretation.
Scholarpedia’s Encyclopedia of Touch provides a comprehensive collection of peer-reviewed articles written by leading researchers, detailing our current scientific understanding of tactile sensing and its neural substrates in animals including humans. The encyclopedia allows ideas and insights to be shared between researchers working on different aspects of touch and in different species, including research in synthetic touch systems. In addition, this encyclopedia raises awareness of research in tactile sensing and increases scientific and public interest in the field.The articles address subjects including tactile control, whiskered robots, vibrissal coding, the molecular basis of touch, invertebrate mechanoreception, fingertip transducers and tactile sensing.All the articles in this encyclopedia provide in-depth and state-of-the-art scholarly treatment of the academic topics concerned, making it an excellent reference work for academics, professionals and students.
Structure-function correlations of rat trigeminal primary neurons: Emphasis on club-like endings, a vibrissal mechanoreceptor
This study focuses on the structure and function of the primary sensory neurons that innervate vibrissal follicles in the rat. Both the peripheral and central terminations, as well as their firing properties were identified using intracellular labelling and recording in trigeminal ganglia in vivo. Fifty-one labelled neurons terminating peripherally, as club-like, Merkel, lanceolate, reticular or spiny endings were identified by their morphology. All neurons responded robustly to air puff stimulation applied to the vibrissal skin. Neurons with club-like endings responded with the highest firing rates; their peripheral processes rarely branched between the cell body and their terminal tips. The central branches of these neurons displayed abundant collaterals terminating within all trigeminal nuclei. Analyses of three-dimensional reconstructions reveal a palisade arrangement of club-like endings bound to the ringwulst by collagen fibers. Our morphological findings suggest that neurons with club-like endings sense mechanical aspects related to the movement of the ringwulst and convey this information to all trigeminal nuclei in the brainstem.[All authors]
(2015) Frontiers in Systems Neuroscience. 9, 160. Abstract
When you don't have a clue where to look for something you are interested in, such as cookies hidden in the kitchen, the best strategy may be a random search. If that something can be remotely sensed by you, e.g., smelled, then your search would be facilitated by adding gradient-sensing—if the gradient over two or more samples taken along a path is positive don't change the path, if not—select another path (randomly). This algorithm has been adapted by microbes while searching for food (known as chemotaxis)—it ensures that the microbes, as a community, would find any reachable food located in their vicinity. The same algorithm appears to have subserved scientific search for several centuries with a great success.
(2015) Scholarpedia of Touch. Ahissar E., Izhikevich E. & Prescott T.(eds.). p. 161-176 Abstract
It is commonly assumed that object perception is the combination of sensory features into unified perceptual entities. Tactile object perception may therefore be defined as the perception of objects whose feature information is acquired via touch. Consequently, research relevant to the topic of tactile objects has focused on exploring the primitives of the tactile system, their interrelation, and how they may be bound together. The current discussion does not explicitly rule out, nor does it address, kinesthetic sensation. As such, tactile perception is used here interchangeably with haptic perception (Lederman and Klatzky 2009).
Correction: Saraf-Sinik et al., Motion Makes Sense: An Adaptive Motor-Sensory Strategy Underlies the Perception of Object Location in Rats (vol 35, pg 8777, 2015)
In the article “Motion Makes Sense: An Adaptive Motor-Sensory Strategy Underlies the Perception of Object Location in Rats” by Inbar Saraf-Sinik, Eldad Assa, and Ehud Ahissar, which appeared on pages 8777–8789 of the June 10, 2015 issue, several errors were discovered and are corrected.
(2015) Perception. 44, 8-9, p. 986-994 Abstract
Eye movements (eyeM) are an essential component of visual perception. They allow the sampling and scanning of stationary scenes at various spatial scales, primarily at the scene level, via saccades, and at the local level, via fixational eyeM. Given the constant motion of visual images on the retina, a crucial factor in resolving spatial ambiguities related to the external scene is the exact trajectory of eyeM. We show here that the trajectory of eyeM can be encoded at high resolution by simple retinal receptive fields of the symmetrical type. We also show that such encoding can account for motion illusions such as the Ouchi illusion. In addition, encoding of motion projections along horizontal and vertical symmetrical simple retinal receptive fields entails a kind of Cartesian decomposition of the 2-D image into two 1-D projections.
(2015) Anatomical Record. 298, 7, p. 1347-58 25408106. Abstract
Coordinated action of facial muscles during whisking, sniffing, and touching objects is an important component of active sensing in rodents. Accumulating evidence suggests that the anatomical schemes that underlie active sensing are similar across the majority of whisking rodents. Intriguingly, however, muscle architecture in the mystacial pad of the mouse was reported to be different, possessing only one extrinsic vibrissa protracting muscle (M. nasalis) in the rostral part of the snout. In this study, the organization of the muscles that move the nose and the mystacial vibrissae in mice was re-examined and compared with that reported previously in other rodents. We found that muscle distribution within the mystacial pad and around the tip of the nose in mice is isomorphic with that found in other whisking rodents. In particular, in the rostral part of the mouse snout, we describe both protractors and retractors of the vibrissae. Nose movements are controlled by the M. dilator nasi and five subunits of the M. nasolabialis profundus, with involvement of the nasal cartilaginous skeleton as a mediator in the muscular effort translation.
Motion Makes Sense: An Adaptive Motor-Sensory Strategy Underlies the Perception of Object Location in Rats
Tactile perception is obtained by coordinated motor-sensory processes. We studied the processes underlying the perception of object location in freely moving rats. We trained rats to identify the relative location of two vertical poles placed in front of them and measured at high resolution the motor and sensory variables (19 and 2 variables, respectively) associated with this whiskers-based perceptual process. We found that the rats developed stereotypic head and whisker movements to solve this task, in a manner that can be described by several distinct behavioral phases. During two of these phases, the rats' whiskers coded object position by first temporal and then angular coding schemes. We then introduced wind (in two opposite directions) and remeasured their perceptual performance and motor-sensory variables. Our rats continued to perceive object location in a consistent manner under wind perturbations while maintaining all behavioral phases and relatively constant sensory coding. Constant sensory coding was achieved by keeping one group of motor variables (the "controlled variables") constant, despite the perturbing wind, at the cost of strongly modulating another group of motor variables (the "modulated variables"). The controlled variables included coding-relevant variables, such as head azimuth and whisker velocity. These results indicate that consistent perception of location in the rat is obtained actively, via a selective control of perception-relevant motor variables.
(2015) Cerebral Cortex. 25, 4, p. 845-848 Abstract
What are the functions implemented by neurons in the sensory nuclei of the thalamus? It seems that this question has accompanied cortical and thalamic studies since their onset some 6 decades ago. Over the years, the simplistic, traditional view of thalamic neurons as mere relays of sensory information has given way to more sophisticated views, of which several alternative hypotheses have been proposed. This commentary briefly reviews the 2 current major hypotheses and shows how a new, pioneering experiment, published in Cerebral Cortex by Groh, Acsady and colleagues, discriminates between them. The commentary further elaborates on the thalamo-cortical processing suggested by the new findings, the general sensory-motor scheme to which these findings may be relevant, and the possible roles such thalamo-cortical processing may have in sensory-motor control.
(2015) Israel Journal of Ecology & Evolution. 61, 2, p. 95–105 Abstract
Smell and touch convey most of the information that nocturnal rodents collect in their natural environments, each via its own complex network of muscles, receptors and neurons. Being active senses, a critical factor determining the integration of their sensations relates to the degree of their coordination. While it has been known for nearly 50years that sniffing and whisking can be coordinated, the dynamics of such coordination and its dependency on behavioral and environmental conditions are not yet understood. Here we introduce a novel non-invasive method to track sniffing along with whisking and locomotion using high-resolution video recordings of mice, during free exploration of an open arena. Active sensing parameters in each modality showed significant dependency on exploratory modes ("Outbound", "Exploration" and "Inbound") and locomotion speed. Surprisingly, the correlation between sniffing and whisking was often as high as the bilateral inter-whisker correlation. Both inter-whisker and inter-modal coordination switched between distinct high-correlation and low-correlation states. The fraction of time with high-correlation states was higher in the Outbound and Exploration modes compared with the Inbound mode. Overall, these data indicate that sniffing-whisking coordination is a complex dynamic process, likely to be controlled by multiple-level inter-modal coordinated loops of motor-sensory networks.
(2015) Scholarpedia: the peer reviewed open access encyclopedia. 10, 4, 32785. Abstract
Systems neuroscience attempts to understand the realization of brain-related functions at the level of organization that can be captured by logico-mathematical models (Von Bertalanffy, 1950), such as those describing man-made systems. In the case of perceptual systems, like that of touch, this level of organization is captured by schemes such as the one in Figure 1. Research groups addressing vibrissal touch are trying to map the vibrissal system anatomically, reveal the physiological properties of its components and the interactions between the components, and understand the function of each component and sub-system. As a result, an understanding of the emergence of tactile perception in this system is expected to arise. Importantly, systems neuroscience is not a reductionist method and its application does not preclude the value of explanations at other levels of research.
(2015) Cerebral Cortex. 25, 3, p. 563-577 Abstract
In whisking rodents, object location is encoded at the receptor level by a combination of motor and sensory related signals. Recoding of the encoded signals can result in various forms of internal representations. Here, we examined the coding schemes occurring at the first forebrain level that receives inputs necessary for generating such internal representations-the thalamocortical network. Single units were recorded in 8 thalamic and cortical stations in artificially whisking anesthetized rats. Neuronal representations of object location generated across these stations and expressed in response latency and magnitude were classified based on graded and binary coding schemes. Both graded and binary coding schemes occurred across the entire thalamocortical network, with a general tendency of graded-to-binary transformation from thalamus to cortex. Overall, 63% of the neurons of the thalamocortical network coded object position in their firing. Thalamocortical responses exhibited a slow dynamics during which the amount of coded information increased across 4-5 whisking cycles and then stabilized. Taken together, the results indicate that the thalamocortical network contains dynamic mechanisms that can converge over time on multiple coding schemes of object location, schemes which essentially transform temporal coding to rate coding and gradual to labeled-line coding.
(2015) Anatomical Record. 298, 3, p. 546-553 Abstract
In a number of mammals muscle dilator nasi (naris) has been described as a muscle that reduces nasal airflow resistance by dilating the nostrils. Here we show that in rats the tendon of this muscle inserts into the aponeurosis above the nasal cartilage. Electrical stimulation of this muscle raises the nose and deflects it laterally towards the side of stimulation, but does not change the size of the nares. In alert head-restrained rats, electromyographic recordings of muscle dilator nasi reveal that it is active during nose motion rather than nares dilation. Together these results suggest an alternative role for the muscle dilator nasi in directing the nares for active odor sampling rather than dilating the nares. We suggest that dilation of the nares results from contraction of muscles of the maxillary division of muscle nasolabialis profundus. This muscle group attaches to the outer wall of the nasal cartilage and to the plate of the mystacial pad. Contraction of these muscles exerts a dual action: it pulls the lateral nasal cartilage outward, thus dilating the naris, and drags the plate of the mystacial pad rostrally to produce a slight retraction of the vibrissae. On the basis of these results, we propose that muscle dilator nasi of the rat should be re-named muscle deflector nasi, and that the maxillary parts of muscle nasolabialis profundus should be referred to as muscle dilator nasi.
(2014) Journal of Computational Neuroscience. 37, 2, p. 259-280 Abstract
Animals explore novel environments in a cautious manner, exhibiting alternation between curiosity-driven behavior and retreats. We present a detailed formal framework for exploration behavior, which generates behavior that maintains a constant level of novelty. Similar to other types of complex behaviors, the resulting exploratory behavior is composed of exploration motor primitives. These primitives can be learned during a developmental period, wherein the agent experiences repeated interactions with environments that share common traits, thus allowing transference of motor learning to novel environments. The emergence of exploration motor primitives is the result of reinforcement learning in which information gain serves as intrinsic reward. Furthermore, actors and critics are local and ego-centric, thus enabling transference to other environments. Novelty control, i.e. the principle which governs the maintenance of constant novelty, is implemented by a central action-selection mechanism, which switches between the emergent exploration primitives and a retreat policy, based on the currently-experienced novelty. The framework has only a few parameters, wherein time-scales, learning rates and thresholds are adaptive, and can thus be easily applied to many scenarios. We implement it by modeling the rodent's whisking system and show that it can explain characteristic observed behaviors. A detailed discussion of the framework's merits and flaws, as compared to other related models, concludes the paper.
(2014) Journal of Neuroscience. 34, 38, p. 12646-12661 Abstract
When encountering novel environments, animals perform complex yet structured exploratory behaviors. Despite their typical structuring, the principles underlying exploratory patterns are still not sufficiently understood. Here we analyzed exploratory behavioral data from two modalities: whisking and locomotion in rats and mice. We found that these rodents maximized novelty signal-to-noise ratio during each exploration episode, where novelty is defined as the accumulated information gain. We further found that these rodents maximized novelty during outbound exploration, used novelty-triggered withdrawal-like retreat behavior, and explored the environment in a novelty-descending sequence. We applied a hierarchical curiosity model, which incorporates these principles, to both modalities. We show that the model captures the major components of exploratory behavior in multiple timescales: single excursions, exploratory episodes, and developmental timeline. The model predicted that novelty is managed across exploratory modalities. Using a novel experimental setup in which mice encountered a novel object for the first time in their life, we tested and validated this prediction. Further predictions, related to the development of brain circuitry, are described. This study demonstrates that rodents select exploratory actions according to a novelty management framework and suggests a plausible mechanism by which mammalian exploration primitives can be learned during development and integrated in adult exploration of complex environments.
(2013) Anatomical Record. 296, 12, p. 1821-1832 Abstract
The rhinarium is the rostral-most area of the snout that surrounds the nostrils, and is hairless in most mammals. In rodents, it participates in coordinated behaviors, active tactile sensing, and active olfactory sensing. In rats, the rhinarium is firmly connected to the nasal cartilages, and its motility is determined by movements of the rostral end of the nasal cartilaginous skeleton (NCS). Here, we demonstrate the nature of different cartilaginous regions that form the rhinarium and the nasofacial muscles that deform these regions during movements of the NCS. These muscles, together with the dorsal nasal cartilage that is described here, function as a rhinarial motor plant.
Tactile Modulation of Whisking via the Brainstem Loop: Statechart Modeling and Experimental Validation
Rats repeatedly sweep their facial whiskers back and forth in order to explore their environment. Such explorative whisking appears to be driven by central pattern generators (CPGs) that operate independently of direct sensory feedback. Nevertheless, whisking can be modulated by sensory feedback, and it has been hypothesized that some of this modulation already occurs within the brainstem. However, the interaction between sensory feedback and CPG activity is poorly understood. Using the visual language of statecharts, a dynamic, bottom-up computerized model of the brainstem loop of the whisking system was built in order to investigate the interaction between sensory feedback and CPG activity during whisking behavior. As a benchmark, we used a previously quantified closed-loop phenomenon of the whisking system, touched-induced pump (TIP), which is thought to be mediated by the brainstem loop. First, we showed that TIPs depend on sensory feedback, by comparing TIP occurrence in intact rats with that in rats whose sensory nerve was experimentally cut. We then inspected several possible feedback mechanisms of TIPs using our model. The model ruled out all hypothesized mechanisms but one, which adequately simulated the corresponding motion observed in the rat. Results of the simulations suggest that TIPs are generated via sensory feedback that activates extrinsic retractor muscles in the mystacial pad. The model further predicted that in addition to the touching whisker, all whiskers found on the same side of the snout should exhibit a TIP. We present experimental results that confirm the predicted movements in behaving rats, establishing the validity of the hypothesized interaction between sensory feedback and CPG activity we suggest here for the generation of TIPs in the whisking system.
(2013) IEEE Engineering in Medicine and Biology Society Conference Proceedings. p. 3206-3209 Abstract
This paper presents a tactile vision substitution system (TVSS) for the study of active sensing. Two algorithms, namely image processing and trajectory tracking, were developed to enhance the capability of conventional TVSS. Image processing techniques were applied to reduce the artifacts and extract important features from the active camera and effectively converted the information into tactile stimuli with much lower resolution. A fixed camera was used to record the movement of the active camera. A trajectory tracking algorithm was developed to analyze the active sensing strategy of the TVSS users to explore the environment. The image processing subsystem showed advantageous improvement in extracting object's features for superior recognition. The trajectory tracking subsystem, on the other hand, enabled accurately locating the portion of the scene pointed by the active camera and providing profound information for the study of active sensing strategy applied by TVSS users.
(2013) Nature Neuroscience. 16, 5, p. 622-634 Abstract
In the vibrissal system, touch information is conveyed by a receptorless whisker hair to follicle mechanoreceptors, which then provide input to the brain. We examined whether any processing, that is, meaningful transformation, occurs in the whisker itself. Using high-speed videography and tracking the movements of whiskers in anesthetized and behaving rats, we found that whisker-related morphological phase planes, based on angular and curvature variables, can represent the coordinates of object position after contact in a reliable manner, consistent with theoretical predictions. By tracking exposed follicles, we found that the follicle-whisker junction is rigid, which enables direct readout of whisker morphological coding by mechanoreceptors. Finally, we found that our behaving rats pushed their whiskers against objects during localization in a way that induced meaningful morphological coding and, in parallel, improved their localization performance, which suggests a role for pre-neuronal morphological computation in active vibrissal touch.
(2013) Journal of Physiology Paris. 107, 2-Jan, p. 107-115 Abstract
Rats move their whiskers to acquire information about their environment. It has been observed that they palpate novel objects and objects they are required to localize in space. We analyze whisker-based object localization using two complementary paradigms, namely, active learning and intrinsic-reward reinforcement learning. Active learning algorithms select the next training samples according to the hypothesized solution in order to better discriminate between correct and incorrect labels. Intrinsic-reward reinforcement learning uses prediction errors as the reward to an actor-critic design, such that behavior converges to the one that optimizes the learning process. We show that in the context of object localization, the two paradigms result in palpation whisking as their respective optimal solution. These results suggest that rats may employ principles of active learning and/or intrinsic reward in tactile exploration and can guide future research to seek the underlying neuronal mechanisms that implement them. Furthermore, these paradigms are easily transferable to biomimetic whisker-based artificial sensors and can improve the active exploration of their environment. (C) 2012 Elsevier Ltd. All rights reserved.
(2012) Frontiers in Computational Neuroscience. 6, 89. Abstract
During natural viewing, the eyes are never still. Even during fixation, miniature movements of the eyes move the retinal image across tens of foveal photoreceptors. Most theories of vision implicitly assume that the visual system ignores these movements and somehow overcomes the resulting smearing. However, evidence has accumulated to indicate that fixational eye movements cannot be ignored by the visual system if fine spatial details are to be resolved. We argue that the only way the visual system can achieve its high resolution given its fixational movements is by seeing via these movements. Seeing via eye movements also eliminates the instability of the image, which would be induced by them otherwise. Here we present a hypothesis for vision, in which coarse details are spatially encoded in gaze-related coordinates, and fine spatial details are temporally encoded in relative retinal coordinates. The temporal encoding presented here achieves its highest resolution by encoding along the elongated axes of simple-cell receptive fields and not across these axes as suggested by spatial models of vision. According to our hypothesis, fine details of shape are encoded by interreceptor temporal phases, texture by instantaneous intra-burst rates of individual receptors, and motion by inter-burst temporal frequencies. We further describe the ability of the visual system to readout the encoded information and recode it internally. We show how readingout of retinal signals can be facilitated by neuronalp haselocked loops( NPLLs), which lock to the retinal jitter; this locking enables recoding of motion information and temporal framing of shape and texture processing. A possible implementation of this locking-and-recoding process by specific thalamocortical loops is suggested. Overall it is suggested that high-acuity vision is based primarily on temporal mechanisms of the sort presented here and low-acuity vision is based primarily on spatial mechanisms.
(2012) Journal of Neuroscience. 32, 40, p. 14022-14032 Abstract
Perception involves motor control of sensory organs. However, the dynamics underlying emergence of perception from motor-sensory interactions are not yet known. Two extreme possibilities are as follows: (1) motor and sensory signals interact within an open-loop scheme in which motor signals determine sensory sampling but are not affected by sensory processing and (2) motor and sensory signals are affected by each other within a closed-loop scheme. We studied the scheme of motor-sensory interactions in humans using a novel object localization task that enabled monitoring the relevant overt motor and sensory variables. We found that motor variables were dynamically controlled within each perceptual trial, such that they gradually converged to steady values. Training on this task resulted in improvement in perceptual acuity, which was achieved solely by changes in motor variables, without any change in the acuity of sensory readout. The within-trial dynamics is captured by a hierarchical closed-loop model in which lower loops actively maintain constant sensory coding, and higher loops maintain constant sensory update flow. These findings demonstrate interchangeability of motor and sensory variables in perception, motor convergence during perception, and a consistent hierarchical closed-loop perceptual model.
(2012) PLoS ONE. 7, 9, 44272. Abstract
Whisking mediated touch is an active sense whereby whisker movements are modulated by sensory input and behavioral context. Here we studied the effects of touching an object on whisking in head-fixed rats. Simultaneous movements of whiskers C1, C2, and D1 were tracked bilaterally and their movements compared. During free-air whisking, whisker protractions were typically characterized by a single acceleration-deceleration event, whisking amplitude and velocity were correlated, and whisk duration correlated with neither amplitude nor velocity. Upon contact with an object, a second acceleration-deceleration event occurred in about 25% of whisk cycles, involving both contacting (C2) and non-contacting (C1, D1) whiskers ipsilateral to the object. In these cases, the rostral whisker (C2) remained in contact with the object throughout the double-peak phase, which effectively prolonged the duration of C2 contact. These "touch-induced pumps'' (TIPs) were detected, on average, 17.9 ms after contact. On a slower time scale, starting at the cycle following first touch, contralateral amplitude increased while ipsilateral amplitude decreased. Our results demonstrate that sensory-induced motor modulations occur at various timescales, and directly affect object palpation.
(2012) Neural Networks. 32, p. 119-129 Abstract
A curious agent acts so as to optimize its learning about itself and its environment, without external supervision. We present a model of hierarchical curiosity loops for such an autonomous active learning agent, whereby each loop selects the optimal action that maximizes the agent's learning of sensory-motor correlations. The model is based on rewarding the learner's prediction errors in an actor-critic reinforcement learning (RL) paradigm. Hierarchy is achieved by utilizing previously learned motor-sensory mapping, which enables the learning of other mappings, thus increasing the extent and diversity of knowledge and skills. We demonstrate the relevance of this architecture to active sensing using the well-studied vibrissae (whiskers) system, where rodents acquire sensory information by virtue of repeated whisker movements. We show that hierarchical curiosity loops starting from optimally learning the internal models of whisker motion and then extending to object localization result in free-air whisking and object palpation, respectively. (C) 2012 Elsevier Ltd. All rights reserved.
(2012) Anatomical Record. 295, 7, p. 1181-1191 Abstract
Histochemical examination of the dorsorostral quadrant of the rat snout revealed superficial and deep muscles that are involved in whisking, sniffing, and airflow control. The part of M. nasolabialis profundus that acts as an intrinsic (follicular) muscle to facilitate protraction and translation of the vibrissae is described. An intraturbinate and selected rostral-most nasal muscles that can influence major routs of inspiratory airflow and rhinarial touch through their control of nostril configuration, atrioturbinate and rhinarium position, were revealed.
(2011) Philosophical Transactions Of The Royal Society B-Biological Sciences. 366, 1581, p. 3070-3076 Abstract
In order to identify basic aspects in the process of tactile perception, we trained rats and humans in similar object localization tasks and compared the strategies used by the two species. We found that rats integrated temporally related sensory inputs ('temporal inputs') from early whisk cycles with spatially related inputs ('spatial inputs') to align their whiskers with the objects; their perceptual reports appeared to be based primarily on this spatial alignment. In a similar manner, human subjects also integrated temporal and spatial inputs, but relied mainly on temporal inputs for object localization. These results suggest that during tactile object localization, an iterative motor-sensory process gradually converges on a stable percept of object location in both species.
(2011) 2011 International Joint Conference On Neural Networks (Ijcnn). p. 3008-3015 Abstract
A curious agent, be it a robot, animal or human, acts so as to learn as much as possible about itself and its environment. Such an agent can also learn without external supervision, but rather actively probe its surrounding and autonomously induce the relations between its action's effects on the environment and the resulting sensory input. We present a model of hierarchical motor-sensory loops for such an autonomous active learning agent, meaning a model that selects the appropriate action in order to optimize the agent's learning. Furthermore, learning one motor-sensory mapping enables the learning of other mappings, thus increasing the extent and diversity of knowledge and skills, usually in hierarchical manner. Each such loop attempts to optimally learn a specific correlation between the agent's available internal information, e. g. sensory signals and motor efference copies, by finding the action that optimizes that learning. We demonstrate this architecture on the well-studied vibrissae system, and show how sensory-motor loops are actively learnt from the bottom-up, starting with the forward and inverse models of whisker motion and then extending them to object localization. The model predicts transition from free-air whisking that optimally learns the self-generated motor-sensory mapping to touch-induced palpation that optimizes object localization, both observed in naturally behaving rats.
(2011) Anatomical Record. 294, 5, p. 764-773 Abstract
Anatomical and functional integrity of the rat mystacial pad (MP) is dependent on the intrinsic organization of its extracellular matrix. By using collagen autofluorescence, in the rat MP, we revealed a collagenous skeleton that interconnects whisker follicles, corium, and deep collagen layers. We suggest that this skeleton supports MP tissues, mediates force transmission from muscles to whiskers, facilitates whisker retraction after protraction, and limits MP extensibility. Anat Rec, 294: 764-773, 2011. (C) 2011 Wiley-Liss, Inc.
(2010) Journal of Neurophysiology. 104, 5, p. 2532-2542 Abstract
Whisking is controlled by multiple, possibly functionally segregated, motor sensory-motor loops. While testing for effects of endocannabinoids on whisking, we uncovered the first known functional segregation of channels controlling whisking amplitude and timing. Channels controlling amplitude, but not timing, were modulated by cannabinoid receptor type 1 (CB1R). Systemic administration of CB1R agonist Delta(9)-tetrahydrocannabinol (Delta(9)-THC) reduced whisking spectral power across all tested doses (1.25-5 mg/kg), whereas whisking frequency was affected at only very high doses (5 mg/kg). Concomitantly, whisking amplitude and velocity were significantly reduced in a dose-dependent manner (25-43 and 26-50%, respectively), whereas cycle duration and bilateral synchrony were hardly affected (3-16 and 3-9%, respectively). Preadministration of CB1R antagonist SR141716A blocked Delta(9)-THC-induced kinematic alterations of whisking, and when administered alone, increased whisking amplitude and velocity but affected neither cycle duration nor synchrony. These findings indicate that whisking amplitude and timing are controlled by separate channels and that endocannabinoids modulate amplitude control channels.
(2010) Anatomical Record. 293, 7, p. 1192-1206 Abstract
The vibrissal system of the rat is an example of active tactile sensing, and has recently been used as a prototype in construction of touch-oriented robots. Active vibrissal exploration and touch are enabled and controlled by musculature of the mystacial pad. So far, knowledge about motor control of the rat vibrissal system has been extracted from what is known about the vibrissal systems of other species, mainly mice and hamsters, since a detailed description of the musculature of the rat mystacial pad was lacking. In the present work, the musculature of the rat mystacial pad was revealed by slicing the mystacial pad in four different planes, staining of mystacial pad slices for cytochrome oxidase, and tracking spatial organization of mystacial pad muscles in consecutive slices. We found that the rat mystacial pad contains four superficial extrinsic muscles and five parts of the M. nasolabialis profundus. The connection scheme of the three parts of the M. nasolabialis profundus is described here for the first time. These muscles are inserted into the plate of the mystacial pad, and thus, their contraction causes whisker retraction. All the muscles of the rat mystacial pad contained three types of skeletal striated fibers (red, white, and intermediate). Although the entire rat mystacial pad usually functions as unity, our data revealed its structural segmentation into nasal and maxillary subdivisions. The mechanisms of whisking in the rat, and hypotheses concerning biomechanical interactions during whisking, are discussed with respect to the muscle architecture of the rat mystacial pad. Anat Rec, 293:1192-1206, 2010. (C) 2010 Wiley-Liss, Inc.
(2010) Haptics. p. 298-305 Abstract
The present study examined the human ability to learn a new sensory modality, specifically "whisking". An experimental apparatus containing artificial whiskers, force sensors, position sensors and computer interface was developed. Twelve participants took part in an experiment containing three tasks: pole localization in the radial dimension, roughness estimation, and object recognition. All tasks were performed only through use of the artificial whiskers which were attached to participants' fingers. With little or no practice humans were able to localize objects, recognize shapes and assess roughness with accuracy equal to or greater than that of rats in equivalent tasks, though with longer times. While the number of available whiskers significantly affected shape recognition, it did not affect radial localization accuracy. Introspection by participants revealed a wide range of motor-sensory strategies developed in order to solve the tasks.
(2010) Journal of Neuroscience. 30, 26, p. 8935-8952 Abstract
A mechanistic description of the generation of whisker movements is essential for understanding the control of whisking and vibrissal active touch. We explore how facial-motoneuron spikes are translated, via an intrinsic muscle, to whisker movements. This is achieved by constructing, simulating, and analyzing a computational, biomechanical model of the motor plant, and by measuring spiking to movement transformations at small and large angles using high-precision whisker tracking in vivo. Our measurements revealed a supralinear summation of whisker protraction angles in response to consecutive motoneuron spikes with moderate interspike intervals (5 ms
(2009) Nature. 462, 7275, p. 859-861 Abstract
Imaging of brain structures in living mice reveals that learning new tasks leads to persistent remodelling of synaptic structures, with each new skill associated with a small and unique assembly of new synapses.
(2009) Trends in Neurosciences. 32, 2, p. 101-109 Abstract
It has been argued whether internal representations are encoded using a universal ('the neural code') or multiple codes. Here, we review a series of experiments that demonstrate that tactile encoding of object location via whisking employs an orthogonal, triple-code scheme. Rats, and other rodents, actively move the whiskers back and forth to localize and identify objects. Neural recordings from primary sensory afferents, along with behavioral observations, demonstrate that vertical coordinates of contacted objects are encoded by the identity of activated afferents, horizontal coordinates by the timing of activation and radial coordinates by the intensity of activation. Because these codes are mutually independent, the three-dimensional location of an object could, in principle, be encoded by individual afferents during single whisker-object contacts. One advantage of such a same-neuron-different-codes scheme over the traditionally assumed same-code-different-neurons scheme is a reduction of code ambiguity that, in turn, simplifies decoding circuits.
(2008) Nature Neuroscience. 11, 12, p. 1369-1370 Abstract
Demonstrating how specific motor signals modulate sensory processing in the rat vibrissal system, a new study in this issue shows that motor signals first attenuate and then amplify afferent sensory signals.
(2008) Frontiers in Neuroanatomy. 2, 4. Abstract
The ventral posteromedial thalamic nucleus (VPM) of the rat contains at least two major vibrissa-representing compartments: the dorsomedial (VPMdm), which belongs to the lemniscal afferent pathway, and the ventrolateral (VPMvl), which belongs to the extralemniscal afferent pathway. Although input-output projections and functional characteristics that distinguish these two compartments were recently clarified, a comprehensive structural analysis of these compartments and the border between them was lacking. This paper addresses structural and functional relationships between the VPMdm and VPMvl. We found that the size of the VPM is almost constant across individual rats. Next, we computed a canonical map of the VPM in the oblique plane, where structural borders are best visualized. Using the canonical map, and sequential slices cut in oblique and coronal planes, we determined the border between the VPMdm and VPMvl in the standard coronal plane, and verified it with in vivo extracellular recordings. The position of the border between these two vibrissal sub-nuclei changes along the rostrocaudal extent within the VPM due to the relative sizes of these sub-nuclei at any point. The border between the VPMdm and VPMvl, which was revealed by this technique, can now be included in atlases of the rat brain and should facilitate experimental correlation of tactile functions with thalamic regions.
(2008) Nature Reviews Neuroscience. 9, 9, p. I-I Abstract
Correction to the acknowledgements.
(2008) Nature Reviews Neuroscience. 9, 8, p. 601-612 Abstract
In the visual system of primates, different neuronal pathways are specialized for processing information about the spatial coordinates of objects and their identity - that is, 'where' and 'what'. By contrast, rats and other nocturnal animals build up a neuronal representation of 'where' and 'what' by seeking out and palpating objects with their whiskers. We present recent evidence about how the brain constructs a representation of the surrounding world through whisker-mediated sense of touch. While considerable knowledge exists about the representation of the physical properties of stimuli - like texture, shape and position - we know little about how the brain represents their meaning. Future research may elucidate this and show how the transformation of one representation to another is achieved.
(2008) Journal of Neurophysiology. 100, 2, p. 1152-1154 Abstract
to the editor: In a recent Epub issue of the Journal of Neurophysiology, a paper (Masri et al. 2008) appeared in which the authors claim to replicate experiments, but not results, previously obtained in our laboratory (Ahissar et al. 2000; Sosnik et al. 2001). We maintain that Masri et al. 1) did not replicate our experiments, 2) probed the vibrissal system in a different parametric regime, and 3) their results are not inconsistent with ours.
Vibrissal kinematics in 3D: Tight coupling of azimuth, elevation, and torsion across different whisking modes
Perception is usually an active process by which action selects and affects sensory information. During rodent active touch, whisker kinematics influences how objects activate sensory receptors. In order to fully characterize whisker motion, we reconstructed whisker position in 3D and decomposed whisker motion to all its degrees of freedom. We found that, across behavioral modes, in both head-fixed and freely moving rats, whisker motion is characterized by translational movements and three rotary components: azimuth, elevation, and torsion. Whisker torsion, which has not previously been described, was large (up to 1000), and torsional angles were highly correlated with whisker azimuths. The coupling of azimuth and torsion was consistent across whisking epochs and rats and was similar along rows but systematically varied across rows such that rows A and E counterrotated. Torsional rotation of the whiskers enables contact information to be mapped onto the circumference of the whisker follicles in a predictable manner across protraction-retraction cycles.
Sensation-targeted motor control: Every spike counts? Focus on: "Whisker movements evoked by stimulation of single motor neurons in the facial nucleus of the rat"
Traditionally, sensory processing and motor control have been studied separately, reflecting the belief that sensory and motor streams remain independent until linked via cortical “associative” areas. Although this belief no longer dominates neuroscience, the traditional tendency to continue to study sensory processing and motor control separately is not easily overcome. Only after closely examining operation of sensory organs does one realize how important motor control is for sensation. The recent elegant study of Herfst and Brecht reveals how accurate sensation-targeted motor control should be in one such system—the vibrissal system.
(2008) Biological Cybernetics. 98, 6, p. 449-458 Abstract
Rats use their large facial hairs (whiskers) to detect, localize and identify objects in their proximal three-dimensional (3D) space. Here, we focus on recent evidence of how object location is encoded in the neural sensory pathways of the rat whisker system. Behavioral and neuronal observations have recently converged to the point where object location in 3D appears to be encoded by an efficient orthogonal scheme supported by primary sensory-afferents: each primary-afferent can signal object location by a spatial (labeled-line) code for the vertical axis (along whisker arcs), a temporal code for the horizontal axis (along whisker rows), and an intensity code for the radial axis (from the face out). Neuronal evidence shows that (i) the identities of activated sensory neurons convey information about the vertical coordinate of an object, (ii) the timing of their firing, in relation to other reference signals, conveys information about the horizontal object coordinate, and (iii) the intensity of firing conveys information about the radial object coordinate. Such a triple-coding scheme allows for efficient multiplexing of 3D object location information in the activity of single neurons. Also, this scheme provides redundancy since the same information may be represented in the activity of many neurons. These features of orthogonal coding increase accuracy and reliability. We propose that the multiplexed information is conveyed in parallel to different readout circuits, each decoding a specific spatial variable. Such decoding reduces ambiguity, and simplifies the required decoding algorithms, since different readout circuits can be optimized for a particular variable.
(2007) Neuron. 56, 4, p. 578-579 Abstract
In the sense of touch, it is the motion of the sensory receptors themselves that leads to an afferent signal-whether these receptors are in our fingertips sliding along a surface or a rat's whiskers palpating an object. Afferent signals can be correctly interpreted only if the sensory system receives information about the brain's own motor output. In this issue of Neuron, Urbain and Deschenes provide new insights into the physiological and anatomical interplay between tactile and motor signals in rats.
Layer-specific touch-dependent facilitation and depression in the somatosensory cortex during active whisking
Brains adapt to new situations by retuning their neurons. The most common form of neuronal adaptation, typically observed with repetitive stimulations of passive sensory organs, is depression (responses gradually decrease until stabilized). We studied cortical adaptation when stimuli are acquired by active movements of the sensory organ. In anesthetized rats, artificial whisking was induced at 5 Hz, and activity of individual neurons in layers 2-5 was recorded during whisking in air (Whisking condition) and whisking against an object (Touch condition). Response strengths were assessed by spike counts. Input-layer responses (Layers 4 and 5a) usually facilitated during the whisking train, whereas superficial responses (layer 2/3) usually depressed. In layers 2/3 and 4, but not 5a, responses were usually stronger during touch trials than during whisking in air. Facilitations were specific to the protraction phase; during retraction, responses depressed in all layers and conditions. These dynamic processes were accompanied by a slow positive wave of activity progressing from superficial to deeper layers and lasting for similar to 1 s, during the transient phase of response. Our results indicate that, in the cortex, adaptation does not depend only on the level of activity or the frequency of its repetition but rather on the nature of the sensory information that is conveyed by that activity and on the processing layer. The input and laminar specificities observed here are consistent with the hypothesis that the paralemniscal layer 5a is involved in the processing of whisker motion, whereas the lemniscal barrels in layer 4 are involved in the processing of object identity.
(2006) Current Opinion in Neurobiology. 16, 4, p. 435-444 Abstract
Rats sweep their vibrissae through space to locate objects in their immediate environment. In essence, their view of the proximal world is generated through pliable hairs that tap and palpate objects. The texture and shape of those objects must be discerned for the rat to assess the value of the object. Furthermore, the location of those objects must be specified with reference to the position of the rat's head for the rat to plan its movements. Recent in vivo and in vitro electrophysiological measurements provide insight into the algorithms and mechanisms that underlie these behavioral-based computations.
(2006) Journal of Neuroscience. 26, 33, p. 8451-8464 Abstract
Using their large mystacial vibrissas, rats perform a variety of tasks, including localization and identification of objects. We report on the discriminatory thresholds and behavior of rats trained in a horizontal object localization task. Using an adaptive training procedure, rats learned to discriminate offsets in horizontal (anteroposterior) location with all, one row, or one arc of whiskers intact, but not when only a single whisker (C2) was intact on each cheek. However, rats initially trained with multiple whiskers typically improved when retested later with a single whisker intact. Individual rats reached localization thresholds as low as 0.24 mm (similar to 1). Among the tested groups, localization acuity was finest (
Temporal decoding by phase-locked loops: Unique features of circuit-level implementations and their significance for vibrissal information processing
Rhythmic active touch, such as whisking, evokes a periodic reference spike train along which the timing of a novel stimulus, induced, for example,when the whiskers hit an external object, can be interpreted. Previous work supports the hypothesis that the whisking-induced spike train entrains a neural implementation of a phase-locked loop (NPLL) in the vibrissal system. Here we extend this work and explore how the entrained NPLL decodes the delay of the novel, contact-induced stimulus and facilitates object localization. We consider two implementations of NPLLs, which are based on a single neuron or a neural circuit, respectively, and evaluate the resulting temporal decoding capabilities. Depending on the structure of the NPLL, it can lock in either a phase- or co-phase-sensitive mode, which is sensitive to the timing of the input with respect to the beginning of either the current or the next cycle, respectively. The co-phase-sensitive mode is shown to be unique to circuit-based NPLLs. Concentrating on temporal decoding in the vibrissal system of rats, we conclude that both the nature of the information processing task and the response characteristics suggest that the computation is sensitive to the co-phase. Consequently, we suggest that the underlying thalamocortical loop should implement a circuit-based NPLL.
Mapping the gates. Focus on "Relationship between physiological response type (RA and SA) and vibrissal receptive field of neurons within the rat trigeminal ganglion"
Four decades ago, Hubel and Wiesel demonstrated that cortical neurons show a response specificity that does not exist in the thalamus or retina and triggered a universal pursuit after cortical mechanisms of perception. Under this pursuit hid an implicit assumption that whatever is needed to be known about the input to the cortex is already known. Forty years later, we are realizing that actually we don’t know what the sensory organs are telling the brain, and yet, this knowledge is crucial to discriminate between alternative hypotheses of cortical function. Specifically, recent studies on sensor-level encoding of natural-like or complex stimuli in vision (e.g., Olveczky et al. 2003; Puchalla et al. 2005) and touch (e.g., Andermann et al. 2004; Arabzadeh et al. 2005; Jones et al. 2004; Szwed et al. 2003, 2006) have shown that information conveyed to the cortex differs from what was assumed previously. At the same time, important foundations needed to guide experiments on sensory encoding are still missing, and that is why the article published in this issue of Journal of Neurophysiology (p. 3129–3145) in which Leiser and Moxon (2006) provide the first functional map of the trigeminal ganglion (TG) of the rat, is a significant step toward systematic characterization of tactile encoding.
(2006) PLoS Biology. 4, 5, p. 819-825 Abstract
In active sensation, sensory information is acquired via movements of sensory organs; rats move their whiskers repetitively to scan the environment, thus detecting, localizing, and identifying objects. Sensory information, in turn, affects future motor movements. How this motor-sensory-motor functional loop is implemented across anatomical loops of the whisker system is not yet known. While inducing artificial whisking in anesthetized rats, we recorded the activity of individual neurons from three thalamic nuclei of the whisker system, each belonging to a different major afferent pathway: paralemniscal, extralemniscal (a recently discovered pathway), or lemniscal. We found that different sensory signals related to active touch are conveyed separately via the thalamus by these three parallel afferent pathways. The paralemniscal pathway conveys sensor motion (whisking) signals, the extralemniscal conveys contact (touch) signals, and the lemniscal pathway conveys combined whisking-touch signals. This functional segregation of anatomical pathways raises the possibility that different sensory-motor processes, such as those related to motion control, object localization, and object identification, are implemented along different motor-sensory-motor loops.
Coding of stimulus frequency by latency in thalamic networks through the interplay of GABA(B)-mediated feedback and stimulus shape
A temporal sensory code occurs in posterior medial (POm) thalamus of the rat vibrissa system, where the latency for the spike rate to peak is observed to increase with increasing frequency of stimulation between 2 and 11 Hz. In contrast, the latency of the spike rate in the ventroposterior medial (VPm) thalamus is constant in this frequency range. We consider the hypothesis that two factors are essential for latency coding in the POm. The first is GABA B-mediated feedback inhibition from the reticular thalamic (Rt) nucleus, which provides delayed and prolonged input to thalamic structures. The second is sensory input that leads to an accelerating spike rate in brain stem nuclei. Essential aspects of the experimental observations are replicated by the analytical solution of a rate-based model with a minimal architecture that includes only the POm and Rt nuclei, i.e., an increase in stimulus frequency will increase the level of inhibitory output from Rt thalamus and lead to a longer latency in the activation of POm thalamus. This architecture, however, admits period-doubling at high levels of GABA B-mediated conductance. A full architecture that incorporates the VPm nucleus suppresses period-doubling. A clear match between the experimentally measured spike rates and the numerically calculated rates for the full model occurs when VPm thalamus receives stronger brain stem input and weaker GABA B-mediated inhibition than POm thalamus. Our analysis leads to the prediction that the latency code will disappear if GABA B-mediated transmission is blocked in POm thalamus or if the onset of sensory input is too abrupt. We suggest that GABA B-mediated inhibition is a substrate of temporal coding in normal brain function.
Responses of trigeminal ganglion neurons to the radial distance of contact during active vibrissal touch
Rats explore their environment by actively moving their whiskers. Recently, we described how object location in the horizontal (front - back) axis is encoded by first-order neurons in the trigeminal ganglion (TG) by spike timing. Here we show how TG neurons encode object location along the radial coordinate, i.e., from the snout outward. Using extracellular recordings from urethane-anesthetized rats and electrically induced whisking, we found that TG neurons encode radial distance primarily by the number of spikes fired. When an object was positioned closer to the whisker root, all touch-selective neurons recorded fired more spikes. Some of these cells responded exclusively to objects located near the base of whiskers, signaling proximal touch by an identity (labeled-line) code. A number of tonic touch-selective neurons also decreased delays from touch to the first spike and decreased interspike intervals for closer object positions. Information theory analysis revealed that near-certainty discrimination between two objects separated by 30% of the length of whiskers was possible for some single cells. However, encoding reliability was usually lower as a result of large trial-by-trial response variability. Our current findings, together with the identity coding suggested by anatomy for the vertical dimension and the temporal coding of the horizontal dimension, suggest that object location is encoded by separate neuronal variables along the three spatial dimensions: temporal for the horizontal, spatial for the vertical, and spike rate for the radial dimension.
(2005) The Auditory Cortex. p. 295-314 Abstract
The temporal envelope of speech contains low-frequency information, which is crucial for speech comprehension. This information is essential for identification of phonemes, syllables, words, and sentences (Rosen, 1992). The temporal envelope of speech defines slow variations of the spectral energy of a spoken sentence, variations that are usually below 8 Hz (Houtgast & Steeneken, 1985). Comprehension of speech depends on the integrity of its temporal envelope between 4 and 16 Hz (Drullman et al., 1994; van der Horst et al., 1999). The mechanisms by which this information is extracted and processed are not yet known.
(2005) Journal of Neurophysiology. 93, 4, p. 2294-2301 Abstract
Due to recent advances that enable real-time electrophysiological recordings in brains of awake behaving rodents, effective methods for analyzing the large amount of behavioral data thus generated, at millisecond resolution, are required. We describe a semiautomated, efficient method for accurate tracking of head and mystacial vibrissae (whisker) movements in freely moving rodents using high-speed video. By tracking the entire length of individual whiskers, we show how both location and shape of whiskers are relevant when describing the kinematics of whisker movements and whisker interactions with objects during a whisker-dependent task and exploratory behavior.
(2004) Journal of Neurophysiology. 92, 6, p. 3298-3308 Abstract
Ample data indicate that the gustatory cortex (GC) subserves the processing, encoding, and storage of taste information. To further elucidate the neural processes involved, we recorded multi-unit activity in the GC of the freely behaving rat as it became familiar with a novel tastant. Exposure to the tastant was performed over three 40- to 50-min sessions, 24 h apart. In each session, the tastant was presented repeatedly, 1 s at a time, with 10- to 12-s inter-trial intervals. The neural response to the tastant typically lasted 7 s. Our results show that the average neuronal response to the tastant increased as this tastant became familiar, but this increase was detected only during the last 5 s of the response. The increased response was not generalized to another tastant. Furthermore, our analysis suggests that specific neuronal populations subserve the processing of familiarity of specific tastants. The signature of familiarity was not detected in the course of the familiarization session, but only on the subsequent day, suggesting that its development involves slow post-acquisition processes. Our data are in line with the notion that GC neurons process multiple taste attributes, familiarity included, during different temporal phases of their response. The data also suggest that by default the brain considers a taste stimulus as novel, unless proven otherwise.
(2004) Somatosensory and Motor Research. 21, 3/4, p. 183-187 Abstract
Understanding of the functional neurobiology of the rodent whisker system would be advanced by neurobehavioral studies in awake, behaving animals that combine unit recording from structures at various levels of the system with quantitative characterization of the kinematics and temporal organization of whisking. Such studies require the solution of a number of methodological problems. These include: chronic recording procedures ensuring unit isolation, stability and maximum yield, monitoring and display of unit activity and whisker movements within the same (ms) timeframe and behavioral paradigms which bring whisking movement parameters under the control of the experimenter rather than the rat. Here we describe a head-fixed rodent preparation which makes possible chronic recording of unit activity in the awake, whisking rat, combined with real-time, high resolution monitoring of whisker and pad movements in two dimensions and under behavioral control. While the head-fixed "whisking" preparation has some inherent limitations, it may be used to address a number of important neurobehavioral problems. We suggest that it should contribute significantly to understanding the functional neurobiology of the whisker system.
(2003) Neuron. 40, 3, p. 621-630 Abstract
Mammals acquire much of their sensory information by actively moving their sensory organs. Yet, the principles of encoding by active sensing are not known. Here we investigated the encoding principles of active touch by rat whiskers (vibrissae). We induced artificial whisking in anesthetized rats and recorded from first-order neurons in the trigeminal ganglion. During active touch, first-order trigeminal neurons presented a rich repertoire of responses, which could not be inferred from their responses to passive deflection stimuli. Individual neurons encoded four specific events: whisking, contact with object, pressure against object, and detachment from object. Whisking-responsive neurons fired at specific deflection angles, reporting the actual whiskers' position with high precision. Touch-responsive neurons encoded the horizontal coordinate of objects' position by spike timing. These findings suggest two specific encoding-decoding schemes.
Acetylcholine-dependent potentiation of temporal frequency representation in the barrel cortex does not depend on response magnitude during conditioning
The response properties of neurons of the postero-medial barrel sub-field of the somatosensory cortex (the cortical structure receiving information from the mystacial vibrissae can be modified as a consequence of peripheral manipulations of the afferent activity. This plasticity depends on the integrity of the cortical cholinergic innervation, which originates at the nucleus basalis magnocellularis (NBM). The activity of the NBM is related to the behavioral state of the animal and the putative cholinergic neurons are activated by specific events, such as reward-related signals, during behavioral learning. Experimental studies oil acetylcholine (ACh)-dependent cortical plasticity have shown that ACh is needed for both the induction and the expression of plastic modifications induced by sensory-cholinergic pairings. Here we review and discuss ACh-dependent plasticity and activity -dependent plasticity and ask whether these two mechanisms are linked. To address this question, we analyzed our data and tested whether changes mediated by ACh were activity-dependent. We show that ACh-dependent potentiation of response in the barrel cortex of rats observed after sensory-cholinergic pairing was not correlated to the changes in activity induced during pairing. Since these results suggest that the effect of ACh during pairing is not exerted through a direct control of the post-synaptic activity, we propose that ACh might induce its effect either pre- or post-synaptically through activation of second messenger cascades. (C) 2004 Elsevier Ltd. All rights reserved.
(2003) Journal of Neuroscience. 23, 8, p. 3100-3105 Abstract
Sensory processing and its perception require that local information would also be available globally. Indeed, in the mammalian neocortex, local excitation spreads over large distances via the long-range horizontal connections in layer 2/3 and may spread over an entire cortical area if excitatory polysynaptic pathways are also activated. Therefore, a balance between local excitation and surround inhibition is required. Here we explore the spatiotemporal aspects of cortical depolarization and hyperpolarization of rats anesthetized with urethane. New voltage-sensitive dyes (VSDs) were used for high-resolution real-time visualization of the cortical responses to whisker deflections and cutaneous stimulations of the whisker pad. These advances facilitated imaging of ongoing activity and evoked responses even without signal averaging. We found that the motion of a single whisker evoked a cortical response exhibiting either one or three phases. During a triphasic response, there was first a cortical depolarization in a small cortical region the size of a single cortical barrel. Subsequently, this depolarization increased and spread laterally in an oval manner, preferentially along rows of the barrel field. During the second phase, the amplitude of the evoked response declined rapidly, presumably because of recurrent inhibition. Subsequently, the third phase exhibiting a depolarization rebound was observed and clear, and similar to16 Hz oscillations were detected. Stimulus conditions revealing a net surround hyperpolarization during the second phase were also found. By using new, improved VSD, the present findings shed new light on the spatial parameters of the intricate spatiotemporal cortical interplay of inhibition and excitation.
(2003) Cerebral Cortex. 13, 1, p. 53-62 Abstract
Two classes of neuronal architectures dominate in the ongoing debate on the nature of computing by nervous systems. The first is a predominantly feedforward architecture, in which local interactions among neurons within each processing stage play a less influential role compared with the drive of the input to that stage. The second class is a recurrent network architecture, in which the local interactions among neighboring neurons dominate the dynamics of neuronal activity so that the input acts only to bias or seed the state of the network. The study of sensorimotor networks, however, serves to highlight a third class of architectures, which is neither feedforward nor locally recurrent and where computations depend on large-scale feedback loops. Findings that have emerged from our laboratories and those of our colleagues suggest that the vibrissa sensorimotor system is involved in such closed-loop computations. In particular, single unit responses from vibrissa sensory and motor areas show generic signatures of phase-sensitive detection and control at the level of thalamocortical and corticocortical loops. These loops are likely to be components within a greater closed-loop vibrissa sensorimotor system, which optimizes sensory processing.
(2001) Proceedings of the National Academy of Sciences of the United States of America. 98, 23, p. 13367-13372 Abstract
Speech comprehension depends on the integrity of both the spectral content and temporal envelope of the speech signal. Although neural processing underlying spectral analysis has been intensively studied, less is known about the processing of temporal information. Most of speech information conveyed by the temporal envelope is confined to frequencies below 16 Hz, frequencies that roughly match spontaneous and evoked modulation rates of primary auditory cortex neurons. To test the importance of cortical modulation rates for speech processing, we manipulated the frequency of the temporal envelope of speech sentences and tested the effect on both speech comprehension and cortical activity. Magnetoencephalographic signals from the auditory cortices of human subjects were recorded while they were performing a speech comprehension task. The test sentences used in this task were compressed in time. Speech comprehension was degraded when sentence stimuli were presented in more rapid (more compressed) forms. We found that the average comprehension level, at each compression, correlated with (i) the similarity between the frequencies of the temporal envelopes of the stimulus and the subject's cortical activity ("stimulus-cortex frequency-matching") and (it) the phase-locking (PL) between the two temporal envelopes ("stimulus-cortex PL"). Of these two correlates, PL was significantly more indicative for single-trial success. Our results suggest that the match between the speech rate and the a priori. modulation capacities of the auditory cortex is a prerequisite for comprehension. However, this is not sufficient: stimulus-cortex PL should be achieved during actual sentence presentation.
(2001) Journal of Neuroscience. 21, 20, p. 1A-1A Abstract
In the article “Importance of Temporal Cues for Tactile Spatial-Frequency Discrimination,” by Efrat Gamzu and Ehud Ahissar, which appeared on pages 7416–7427 of the September 15, 2001 issue, LT rather than HT should have appeared throughout the first column of Table 2.
(2001) Neuron. 32, 2, p. 185-201 Abstract
Sensory information is encoded both in space and in time. Spatial encoding is based on the identity of activated receptors, while temporal encoding is based on the timing of activation. In order to generate accurate internal representations of the external world, the brain must decode both types of encoded information, even when processing stationary stimuli. We review here evidence in support of a parallel processing scheme for spatially and temporally encoded information in the tactile system and discuss the advantages and limitations of sensory-derived temporal coding in both the tactile and visual systems. Based on a large body of data, we propose a dynamic theory for vision, which avoids the impediments of previous dynamic theories.
(2001) Journal of Neuroscience. 21, 18, p. 7416-7427 Abstract
While scanning a textured surface with fingers, tactile information is encoded both spatially, by differential activation of adjacent receptors, and temporally, by changes in receptor activation during movements of the fingers across the surface. We used a tactile discrimination task to examine the dependence of human tactile perception on the availability of spatial and temporal cues. Subjects discriminated between spatial frequencies of metal gratings presented simultaneously to both hands. Tactile temporal cues were eliminated by preventing lateral hand movements; tactile spatial cues were eliminated by using gloves with an attached rubber pin. Analysis revealed separation of the subjects into two groups: "spatiotemporal" (ST) and "latent-temporal" (LT). Under normal conditions, the performance of ST subjects was significantly better than that of the LT subjects. Prevention of lateral movements impaired performance of both ST and LT subjects. However, when only temporal cues were available, the performance of ST subjects was significantly impaired, whereas that of the LT subjects either improved or did not change. Under the latter condition, LT subjects changed strategy to scanning with alternating hands, at velocities similar to the velocities normally used by ST subjects. These velocities generated temporal frequencies between 15 and 30 Hz. The LT subjects were unaware of their improved performance. Nine of ten LT subjects significantly improved their performance under normal conditions when trained to scan gratings using alternating hands and velocities similar to those used by ST subjects. We conclude that (1) temporal cues are essential for spatial-frequency discrimination, (2) human subjects vary in the tactile strategies they use for texture exploration, and (3) poor tactile performers can significantly improve by using strategies that emphasize temporal cues.
Acetylcholine-dependent induction and expression of functional plasticity in the barrel cortex of the adult rat
The involvement of acetylcholine (ACh) in the induction of neuronal sensory plasticity is well documented. Recently we demonstrated in the somatosensory cortex of the anesthetized rat that ACh is also involved in the expression of neuronal plasticity. Pairing stimulation of the principal whisker at a fixed temporal frequency with ACh iontophoresis induced potentiations of response that required re-application of ACh to be expressed. Here we fully characterize this phenomenon and extend it to stimulation of adjacent whiskers. We show that these ACh-dependent potentiations are cumulative and reversible. When several sensori-cholinergic pairings were applied consecutively with stimulation of the principal whisker, the response at the paired frequency was further increased, demonstrating a cumulative process that could reach saturation levels. The potentiations were specific to the stimulus frequency: if the successive pairings were done at different frequencies, then the potentiation caused by the first pairing was depotentiated, whereas the response to the newly paired frequency was potentiated. During testing, the potentiation of response did not develop immediately on the presentation of the paired frequency during application of ACh: the analysis of the kinetics of the effect indicates that this process requires the sequential presentation of several trains of stimulation at the paired frequency to be expressed. We present evidence that a plasticity with similar characteristics can be induced for responses to stimulation of an adjacent whisker, suggesting that this potentiation could participate in receptive field spatial reorganizations. The spatial and temporal properties of the ACh-dependent plasticity presented here impose specific constraints on the underlying cellular and molecular mechanisms.
(2001) Journal of Neurophysiology. 86, 1, p. 354-367 Abstract
Part of the information obtained by rodent whiskers is carried by the frequency of their movement. In the thalamus of anesthetized rats, the whisker frequency is represented by two different coding schemes: by amplitude and spike count (i.e., response amplitudes and spike counts decrease as a function of frequency) in the lemniscal thalamus and by latency and spike count (latencies increase and spike counts decrease as a function of frequency) in the paralemniscal thalamus (see accompanying paper). Here we investigated neuronal representations of the whisker frequency in the primary somatosensory ("barrel") cortex of the anesthetized rat, which receives its input from both the lemniscal and paralemniscal thalamic nuclei. Single and multi-units were recorded from layers 2/3, 4 (barrels only), 5a, and 5b during vibrissal stimulation. Typically, the input frequency was represented by amplitude and spike count in the barrels of layer 4 and in layer 5b (the "lemniscal layers") and by latency and spike count in layer 5a (the "paralemniscal layer"). Neurons of layer 2/3 displayed a mixture of the two coding schemes. When the pulse width of the stimulus was reduced from 50 to 20 ms, the latency coding in layers 5a and 2/3 was dramatically reduced, while the spike-count coding was not affected; in contrast, in layers 4 and 5b, the latencies remained constant, but the spike counts were reduced with 20-ms stimuli. The same effects were found in the paralemniscal and lemniscal thalamic nuclei, respectively (see accompanying paper). These results are consistent with the idea that thalamocortical loops of different pathways, although terminating within the same cortical columns, perform different computations in parallel. Furthermore, the mixture of coding schemes in layer 2/3 might reflect an integration of lemniscal and paralemniscal outputs.
(2001) Journal of Neurophysiology. 86, 1, p. 339-353 Abstract
How does processing of information change the internal representations used in subsequent stages of sensory pathways? To approach this question, we studied the representations of whisker movements in the lemniscal and paralemniscal pathways of the rat vibrissal system. We recently suggested that these two pathways encode movement frequency in different ways. We proposed that paralemniscal thalamocortical circuits, functioning as phase-locked loops (PLLs), translate temporally coded information into a rate code. Here we focus on the two major trigeminal nuclei of the brain stem, nucleus principalis and subnucleus interpolaris, and on their thalamic targets, the ventral posteromedial nucleus (VPM) and the medial division of the posterior nucleus (POm). This is the first study in which these brain stem and thalamic nuclei were explored together in the same animals and using the same stimuli. We studied both single- and multi-unit activity. We moved the whiskers both mechanically and by air puffs; here we present air-puff-induced movements because they are more similar to natural movements than movements induced by mechanical stimulations. We describe the basic properties of the responses in these brain stem and thalamic nuclei. The responses in both brain stem nuclei were similar; responses to air puffs were mostly tonic and followed the trajectory of whisker movement. The responses in the two thalamic nuclei were similar during low-frequency stimulations or during the first pulses of high-frequency stimulations, exhibiting more phasic responses than those of brain stem neurons. However, with frequencies >2 Hz, VPM and POm responses differed, generating different representations of the stimulus frequency. In the VPM, response amplitudes (instantaneous firing rates) and spike counts (total number of spikes per stimulus cycle) decreased as a function of the frequency. In the POm, latencies increased and spike count decreased as a function of the frequency. Having desc
(2001) Journal of Comparative Neurology. 431, 1, p. 127-128 Abstract
Figures 8 and 11 were incorrectly printed in the original version of this article.The corrected figures appear here. Additionally, two spelling errors occurred in the caption of Figure 1. The words “microvibrasse” on line 6 and “vibrasse” on line7 should read “microvibrissae” and “vibrissae,” respectively.
(2001) Journal of Comparative Neurology. 429, 3, p. 372-387 Abstract
The spatial organization of the anatomical structures along the trigeminal afferent pathway of the rat conserves the topographical order of the receptor sheath: The brainstem barrelettes, thalamic barreloids, and cortical barrels all reflect the arrangement of whiskers across the mystacial pad. Although both the amount of innervation in the mystacial pad and the size of cortical barrels were shown previously to exhibit increasing gradients toward the ventral and caudal whiskers, whether similar gradients existed in the brainstem and thalamus was not known. Here, the authors investigated the size gradients of the barreloids in the ventral posteromedial nucleus of the rat thalamus. Because the angles used to cut the brain were crucial to this study, the optimal cutting angles were determined first for visualization of individual barreloids and of the entire barreloid field. Individual barreloids, arcs, and rows as well as entire barreloid fields were clearly visualized using cytochrome oxidase staining of brain slices that were cut with the optimal cutting angles. For the first five arcs (including straddlers), the length of barreloids increased in the direction of dorsal-to-ventral whiskers and of caudal-to-rostral whiskers. These gradients reveal an inverse relationship between the size of barreloids and whiskers (length and follicle diameter) along arcs and rows. The largest barreloids in the ventral posteromedial nucleus were those that represent whiskers C2-C4, D2-D4, and E2-E4, which are neither the largest nor the most innervated whiskers in the mystacial pad. This implies that the extended representation is not merely a reflection of peripheral innervation biases and probably serves an as yet unknown processing function. J. Comp. Neurol. 429:372-387, 2001. (C) zool. Wiley-Liss, Inc.
(2001) Advances in Neural Population Coding. Nicolelis M. A. L.(eds.). p. 75-87 Abstract
This chapter discusses the temporal and spatial coding in the rat vibrissal system. Spatial encoding of the world is accomplished by arrays of receptors, which are spatially organized across the sensory organs. Each receptor is sensitive to a specific and limited range within the sensation spectrum. Temporal encoding is attained by the temporal pattern of receptor firing, which is not limited to the dynamic aspects of the stimulus, and can also be used for encoding stationary aspects. Primates explore the texture of objects by moving their fingers across it, and rodents scan their environment by moving their whiskers. Tactile acquisition by the whiskers is a motor sensory active process. Whiskers are moved by the motor system to acquire information, which is then analyzed by the sensory system. Changes in pressure, caused by the presence of an object, or by the ridges and grooves across its surface, are detected by the mechanoreceptors. The rat vibrissal system provides a clear example of dissociated coding schemes.
(2000) Nature. 406, 6793, p. 302-306 Abstract
The anatomical connections from the whiskers to the rodent somatosensory (barrel) cortex form two parallel (lemniscal and paralemniscal) pathways(1,2). It is unclear whether the paralemniscal pathway is directly involved in tactile processing, because paralemniscal neuronal responses show poor spatial resolution, labile latencies and strong dependence on cortical feedback(3-5). Here we show that the paralemniscal system can transform temporally encoded vibrissal information into a rate code. We recorded the representations of the frequency of whisker movement along the two pathways in anaesthetized rats. In response to varying stimulus frequencies, the lemniscal neurons exhibited amplitude modulations and constant latencies. In contrast, paralemniscal neurons in both thalamus and cortex coded the input frequency as changes in latency. Because the onset latencies increased and the offset latencies remained constant, the latency increments were translated into a rate code: increasing onset latencies led to lower spike counts. A thalamocortical loop that includes cortical oscillations and thalamic gating can account for these results. Thus, variable latencies and effective cortical feedback in the paralemniscal system can serve the processing of temporal sensory cues, such as those that encode object location during whisking. In contrast, fixed time locking in the lemniscal system is crucial for reliable spatial processing.
(2000) Nature. 403, 6769, p. 549-553 Abstract
State-dependent learning is a phenomenon in which the retrieval of newly acquired information is possible only if the subject is in the same sensory context and physiological state as during the encoding phase(1). In spite of extensive behavioural and pharmacological characterization(2), no cellular counterpart of this phenomenon has been reported, Here we describe a neuronal analogue of state-dependent learning in which cortical neurons show an acetylcholine-dependent expression of an acetylcholine-induced functional plasticity. This was demonstrated on neurons of rat somatosensory 'barrel' cortex, whose tunings to the temporal frequency of whisker deflections were modified by cellular conditioning. Pairing whisker stimulation with acetylcholine applied iontophoretically yielded selective lasting modification of responses, the expression of which depended on the presence of exogenous acetylcholine. Administration of acetylcholine during testing revealed frequency-specific changes in response that were not expressed when tested without acetylcholine or when the muscarinic antagonist, atropine, was applied concomitantly, Our results suggest that both acquisition and recall can be controlled by the cortical release of acetylcholine.
Simultaneous multi-site recordings and iontophoretic drug and dye applications along the trigeminal system of anesthetized rats
A multi-electrode system that permits simultaneous recordings from multiple neurons and iontophoretic applications at two or three different brain sites during acute experiments is described. This system consists of two or three microdrive terminals, each of which includes four electrodes that can be moved independently and used for both extracellular recordings and microiontophoretic drug administration. Drug applications were performed during standard extracellular recordings of multiple single-units via specialized combined electrodes (CEs), which enable ejection of neuroactive substances and recording of neuronal activity from the same electrode. With this system, we were able to successfully record simultaneously from different levels (brainstem, thalamus, and cortex) of the vibrissal ascending pathway of the anesthetized rat. Herein, examples of simultaneous recordings from the brainstem and thalamus and from the thalamus and cortex are presented. An effect of iontophoretic applications of agonists and antagonists of metabotropic glutamate receptors (mGluRs) in the thalamus is demonstrated, and the extent of drug diffusion in the barrel cortex is demonstrated with biocytin. This new multi-electrode system will facilitate the study of transformations of sensory information acquired by the whiskers into cortical representations. (C) 1999 Elsevier Science B.V. All rights reserved.
(1998) Neural Computation. 10, 3, p. 597-650 Abstract
Peripheral sensory activity follows the temporal structure of input signals. Central sensory processing uses also rate coding, and motor outputs appear to be primarily encoded by rate. I propose here a simple, efficient structure, converting temporal coding to rate coding by neuronal phase-locked loops (PLL). The simplest form of a PLL includes a phase detector (that is, a neuronal-plausible version of an ideal coincidence detector) and a controllable local oscillator that are connected in a negative feedback loop. The phase detector compares the firing times of the local oscillator and the input and provides an output whose firing rate is monotonically related to the time difference. The output rate is fed back to the local oscillator and forces it to phase-lock to the input. Every temporal interval at the input is associated with a specific pair of output rate and time difference values; the higher the output rate, the further the local oscillator is driven from its intrinsic frequency. Sequences of input intervals, which by definition encode input information, are thus represented by sequences of firing rates at the PLL's output. The most plausible implementation of PLL circuits is by thalamocortical loops in which populations of thalamic "relay" neurons function as phase detectors that compare the timings of cortical oscillators and sensory signals. The output in this case is encoded by the thalamic population rate. This article presents and analyzes the algorithmic and the implementation levels of the proposed PLL model and describes the implementation of the PLL model to the primate tactile system.
(1998) Neuropharmacology. 37, 5-Apr, p. 633-655 Abstract
In this study, the necessary conditions, including those related to behavior, for lasting modifications to occur in correlated activity ('functional plasticity') were examined in the behaving monkey. Previously, in-vitro studies of neuronal plasticity yielded important information about possible mechanisms of synaptic plasticity, but could not be used to test their functionality in the intact, behaving brain. In-vivo studies usually focused on analysis of the responsiveness of single cells, but did not examine interactions between pairs of neurons. In this study, we combined the two approaches. This was achieved by recording extracellularly and simultaneously the spike activity of several single cells in the auditory cortex of the behaving monkey. The efficacy of neuronal interactions was estimated by measuring the correlation between firing times of pairs of single neurons. Using acoustic stimuli, a version of cellular conditioning was applied when the monkey performed an auditory discrimination task and when it did not. We found that: (i) functional plasticity is a function of the change in correlation, and not of the correlation or covariance per se, and (ii) functional plasticity depends critically on behavior. During behavior, an increase in the correlation caused a short-lasting strengthening of the neuronal coupling efficacy, and a decrease caused a short-lasting weakening. These findings indicate that neuronal plasticity in the auditory cortex obeys a version of Hebb's associative rule under strong behavioral control, as predicted by Thorndike's "Law of Effect". (C) 1998 Published by Elsevier Science Ltd. All rights reserved.
(1997) Proceedings of the National Academy of Sciences of the United States of America. 94, 21, p. 11633-11638 Abstract
The temporally encoded information obtained by vibrissal touch could be decoded ''passively,'' involving only input-driven elements, or ''actively,'' utilizing intrinsically driven oscillators, A previous study suggested that the trigeminal somatosensory system of rats bees not obey the bottom-up order of activation predicted by passive decoding, Thus, we have tested whether this system obeys the predictions of active decoding, We have studied cortical single units in the somatosensory cortices of anesthetized rats and guinea pigs and found that about a quarter of them exhibit clear spontaneous oscillations, many of them around whisking frequencies (approximate to 10 Hz), The frequencies of these oscillations could be controlled locally by glutamate. These oscillations could be forced to track the frequency of induced rhythmic whisker movements at a stable, frequency-dependent, phase difference, During these stimulations, the response intensities of multiunits at the thalamic recipient layers of the cortex decreased, and their latencies increased, with increasing input frequency, These observations are consistent with thalamocortical loops implementing phase-locked loops, circuits that are most efficient in decoding temporally encoded information like that obtained by active vibrissal touch, According to this model, and consistent with our results, populations of thalamic ''relay'' neurons function as phase ''comparators'' that compare cortical timing expectations with the actual input timing and represent the difference by their population output rate.
(1997) Journal of Comparative Neurology. 385, 4, p. 515-527 Abstract
The arrangements of vibrissae in guinea pigs and golden hamsters were previously reported to be different from those in mice and rats. Whereas the mystacial pads in mice and rats include four straddlers and five rows of vibrissae, guinea pigs were described to possess six rows of irregularly aligned mystacial vibrissae and no straddlers, and golden hamsters to include seven vibrissal rows and also no straddlers. We found that all of these four species possess similar vibrissal arrangements within the mystacial pad. To demonstrate this similarity, we developed a new method of sinus hair visualization in flattened and cleared preparations of the mystacial pad. Intrinsic muscles of the mystacial pad that were revealed in thick histological preparations showed clearly the structural and functional relationships between straddlers and vibrissal rows. To verify this finding, and to extend the knowledge of vibrissal cortical representations in guinea pigs and golden hamsters, we have investigated the spatial organization and the functional vibrissal representations of barrels in the posteromedial barrel subfield (PMBSF) of these rodents. The barrel morphology was clearly preserved in Nissl-stained sections and sections processed for cytochrome oxidase of flattened cerebral cortices. We demonstrate that the vibrissal arrangement in the mystacial pad is replicated in the PMBSF of guinea pigs and golden hamsters and that this arrangement is similar to that found in mice and rats. To facilitate comparative studies, these findings strongly recommend the use, in guinea pigs and golden hamsters, of the same classifications and nomenclatures that are used in mice and rats to describe mystacial vibrissae and cortical barrels. (C) 1997 Wiley-Liss, Inc.
Differential effects of acetylcholine on neuronal activity and interactions in the auditory cortex of the guinea-pig
During normal brain operations, cortical neurons are subjected to continuous cholinergic modulations. In vitro studies have indicated that, in addition to affecting general cellular excitability, acetylcholine also modulates synaptic transmission. Whether these cholinergic mechanisms lead to a modulation of functional connectivity in vivo is not yet known. Herein, the effects were studied of an iontophoretic application of acetylcholine and of the muscarinic agonist, carbachol, on the ongoing activity and co-activity of neurons simultaneously recorded in the auditory cortex of the anaesthetized guinea-pig. Iontophoresis of cholinergic agonists mainly affected the spontaneous firing rates of auditory neurons, affected autocorrelations less (in most cases their central peak areas were reduced), and rarely affected cross-correlations. These findings are consistent with cholinergic agonists primarily affecting the excitability of cortical neurons rather than the strength of cortical connections. However, when changes of cross-correlations occurred, they were usually not correlated with concomitant changes in average firing rates nor with changes in autocorrelations, which suggests a secondary cholinergic effect on specific cortico-cortical or thalamo-cortical connections.
(1996) Journal of Physiology Paris. 90, 5-6, p. 353-360 Abstract
Plasticity of neuronal covariances (functional plasticity) is controlled by behavior (Ahissar et al (1992) Science 257, 1412-1415). Whether this behavioral control involves neuromodulatory systems was tested by examining the effect of acetylcholine (ACh) and noradrenaline (NE) on functional plasticity in anesthetized animals and by comparing the effects of these neuromodulators in an anesthetized preparation to that of behavior in awake animals. Local iontophoretic applications of these drugs during manipulations of activity covariance in guinea pig auditory cortex did not mimic the behavioral control of functional plasticity that was previously observed in awake monkeys. Thus, the hypotheses according to which these neuromodulators control functional plasticity independent of their concentration and time of release were not supported by our data. The significant plasticity induced nevertheless, by some of the conditionings in the presence of ACh and NE, suggests that factors, other than those that were experimentally controlled, could regulate this plasticity. These factors could be among others the timing of drug(s) applications relative to the conditioning time, the local concentrations of the drug(s) and/or the site of application with respect to the relevant synapses.
(1995) Behavioral and Brain Sciences. 18, 4, p. 626-627 Abstract
Persistent activity can be the product of mechanisms other than attractor reverberations. The single-unit data presented by Amit cannot discriminate between the different mechanisms. In fact, single-unit data dot not appear to be adequate for testing neural network models.
(1995) Journal of Neuroscience Methods. 56, 2, p. 125-131 Abstract
A remotely controlled multi-electrode array, equipped with a combined electrode (CE) and 3 regular tungsten in-glass electrodes (TEs) is described. The CE enables ejection of different neuroactive substances from 6 barrels and recording of single-unit activity from the etched tungsten rod placed in the central glass capillary. The CE is prepared with standard tungsten rod, glass-capillaries, and regular micropipette pullers. Such CEs possess a good stiffness-flexibility balance, length, easy cell isolation, high stability of recordings, effective ejection properties, and ability to survive penetration of dura. The efficiency of a 4-electrode array, including the CE, was tested by recording the effects of extracellularly ejected drugs (glutamate, acetylcholine and atropine) on single neurons in the auditory cortex of anesthetized guinea pigs. Induced modifications of single-neuron firing patterns and evoked responses were in agreement with the known effects of individual and combined applications of these drugs. Using this multi-electrode array and spike sorting techniques, the pharmacological environment of up to 12 simultaneously recorded cells can be modulated, and its effect on single neurons and on their interactions can be monitored at distances of up to 900 mu m from the CE's tip.
(1994) Current Opinion in Neurobiology. 4, 4, p. 580-587 Abstract
Recent studies have focused on the mechanisms and conditions yielding the short- and long-term plasticity exhibited by neuronal responses in the primary auditory cortex of adults. These investigations have examined factors operating at the cellular and intercellular levels, the effects of global behavioral states and the role of the cholinergic system, which could mediate between the global and local levels. A behaviorally gated unsupervised Hebbian-covariance rule can explain most of the bottom-up driven changes that were observed following sensory manipulation. However, additional supervised learning mechanisms are probably required to generate behavioral improvement. This suggestion has not yet been tested directly.
Dynamics of coherence in cortical neural activity: Experimental observations and functional interpretations[All authors]
We present results from an ongoing electrophysiological study of cortical function in the awake, behaving monkey. Single and multiple neuron activity is recorded from the frontal cortex, while the monkey is engaged in a sensory-motor association task. Results show that neighboring neurons in the frontal cortex may be functionally related and share common features. However, even when neurons were reduced by the same microelectrode, they were not all activated in unison, nor did they all show the same functional properties. Correlation analysis reveals that interactions between neurons may strongly depend on stimulus context and/or behavioral state. Moreover, the interactions may be highly dynamic, with time constants of modulation as low as tens of milliseconds. These findings point at the need to distinguish between anatomical connectivity and functional coupling. The underlying mechanisms as well as the functional implications of such dynamic coupling in cortical networks are discussed.
Dependence of Cortical Plasticity on Correlated Activity of Single Neurons and on Behavioral Context
It has not been possible to analyze the cellular mechanisms underlying learning in behaving mammals because of the difficulties in recording intracellularly from awake animals. Therefore, in the present study of neuronal plasticity in behaving monkeys, the net effect of a single neuron on another neuron (the "functional connection") was evaluated by cross-correlating the times of firing of the two neurons. When two neurons were induced to fire together within a short time window, the functional connection between them was potentiated, and when simultaneous firing was prevented, the connection was depressed. These modifications were strongly dependent on the behavioral context of the stimuli that induced them. The results indicate that changes in the temporal contingency between neurons are often necessary, but not sufficient, for cortical plasticity in the adult monkey: behavioral relevance is required.
Encoding of sound-source location and movement: activity of single neurons and interactions between adjacent neurons in the monkey auditory cortex
1. Neuronal mechanisms for decoding sound azimuth and angular movement were studied by recordings of several single units in parallel in the core areas of the auditory cortex of the macaque monkey. The activity of 180 units was recorded during the presentation of moving and static sound stimuli. Both the activity of single units and the interactions between neighboring neurons in response to each stimulus were analyzed.2. Sixty-two percent of the units showed significant modulation of their firing rates as a function of the stimulus azimuth. Contralateral stimuli were preferred by the majority (approximately 60%) of these neurons. Thirty-five percent of the units showed mild but statistically significant modulation of their firing rates, which was specifically attributed to the angular movement of the sound source.3. Eighty-nine percent of the "movement-sensitive" units were also "azimuth sensitive." The sound source's azimuth determined the pattern of the response components (on, sustained, off), whereas the source's movement affected only the magnitude of these components, typically the sustained component. Most neurons for which the sustained response to static sounds was greater for contralateral than ipsilateral stimuli preferred moving sounds that were moving into the contralateral hemifield.4. Cross-correlation analysis was carried out for 245 neuron pairs. Cross-correlograms were computed for each pair under all stimulus conditions to allow comparison of the neuronal interactions under the various conditions. The shapes of some correlograms (after subtraction of direct stimulus effects) were dependent on specific stimulus conditions, suggesting that the effective connectivity between these neurons depended on the location and/or movement of the sound stimuli. Furthermore, joint peristimulus time (JPST) analysis indicated that modifications of connectivity may be temporally related to the stimulus and may occur over short periods of time. These results could not have been predicted from analysis of the independent single-unit responses to the stimuli.5. The data suggest that both firing rates and correlated activity between adjacent neurons in the auditory cortex encode sound location and movement.
(1991) Journal fur Hirnforschung. 32, 6, p. 735-743 AbstractNeural interactions in the frontal cortex of a behaving monkey: signs of dependence on stimulus context and behavioral state[All authors]
In order to gain an understanding of the processes taking place within and between neuronal assemblies, we made simultaneous recordings of spike trains from groups of up to 1 1 neurons in the frontal cortex of a rhesus monkey, that was trained to perform a sensorimotor behavioral task. We report here on preliminary results from correlation analysis of these neuronal activities, with special emphasis on signs of behaviorally induced modifications of neural interaction, possibly due to rapid modulations of discharge synchronization among the neurons. Our findings suggest that different functional groups of neurons may co-exist within each small volume of cortex, and that neurons may be dynamically recruited into such a group to fulfil a specific function.
Oscillatory activity of single units in a somatosensory cortex of an awake monkey and their possible role in texture analysis
Neuronal activity was extracellularly recorded in the cortex of an awake monkey (Macaca fascicularis). Single units displaying oscillatory firing patterns were found in the upper bank of the lateral sulcus in a region where most of the neurons responded to somatosensory stimuli. The spectral energies of the oscillating activity were distributed in a trimodal fashion--0-15, 15-50, and 80-250 Hz--with the most common frequencies around 30 Hz. The oscillatory activity was not affected by anesthesia, but it was often reduced by tactile stimulation or self-initiated movements. Analysis of the spike trains suggests that the majority of oscillatory activity was intrinsically generated by the neurons. A neural model of texture analysis is offered based on a corticothalamic phase-locked loop. The newly identified oscillators play a key role in this model. The relevance of the model to physiological, anatomical, and psychophysical data, as well as testable predictions, are discussed.