Selected publications

Learning new rules and adopting novel behavioral policies is a prominent adaptive behavior of primates. Westudied the dynamics of single neurons in the dorsal anterior cingulate cortex and putamen of monkeys whilethey learned new classification tasks every few days over a fixed set of multi-cue patterns. Representing therules and the neuronal selectivity as vectors in the space spanned by a set of stimulus features allowed us tocharacterize neuronal dynamics in geometrical terms. We found that neurons in the cingulate cortex mainlyrotated toward the rule, implying a policy search, whereas neurons in the putamen showed a magnitude in-crease that followed the rotation of cortical neurons, implying strengthening of confidence for the newly ac-quired rule-based policy. Further, the neural representation at the end of a session predicted next-daybehavior, reflecting overnight retention. The novel framework for characterization of neural dynamics sug-gests complementing roles for the putamen and the anterior cingulate cortex.

The social interactions underlying group foraging and their benefits have been mostly studied using mechanistic models replicating qualitative features of group behavior, and focused on a single resource or a few clustered ones. Here, we tracked groups of freely foraging adult zebrafish with spatially dispersed food items and found that fish perform stereotypical maneuvers when consuming food, which attract neighboring fish. We then present a mathematical model, based on inferred functional interactions between fish, which accurately describes individual and group foraging of real fish. We show that these interactions allow fish to combine individual and social information to achieve near-optimal foraging efficiency and promote income equality within groups. We further show that the interactions that would maximize efficiency in these social foraging models depend on group size, but not on food distribution - suggesting that fish may adaptively pick the subgroup of neighbors they 'listen to' to determine their own behavior.

Information is carried in the brain by the joint spiking patterns of large groups of noisy, unreliable neurons. This noise limits the capacity of the neural code and determines how information can be transmitted and read-out. To accurately decode, the brain must overcome this noise and identify which patterns are semantically similar. We use models of network encoding noise to learn a thesaurus for populations of neurons in the vertebrate retina responding to artificial and natural videos, measuring the similarity between population responses to visual stimuli based on the information they carry. This thesaurus reveals that the code is organized in clusters of synonymous activity patterns that are similar in meaning but may differ considerably in their structure. This organization is highly reminiscent of the design of engineered codes. We suggest that the brain may use this structure and show how it allows accurate decoding of novel stimuli from novel spiking patterns.

Pattern classification learning tasks are commonly used to explore learning strategies in human subjects. The universal and individual traits of learning such tasks reflect our cognitive abilities and have been of interest both psychophysically and clinically. From a computational perspective, these tasks are hard, because the number of patterns and rules one could consider even in simple cases is exponentially large. Thus, when we learn to classify we must use simplifying assumptions and generalize. Studies of human behavior in probabilistic learning tasks have focused on rules in which pattern cues are independent, and also described individual behavior in terms of simple, single-cue, feature-based models. Here, we conducted psychophysical experiments in which people learned to classify binary sequences according to deterministic rules of different complexity, including high-order, multicue-dependent rules. We show that human performance on such tasks is very diverse, but that a class of reinforcement learning-like models that use a mixture of features captures individual learning behavior surprisingly well. These models reflect the important role of subjects' priors, and their reliance on high-order features even when learning a low-order rule. Further, we show that these models predict future individual answers to a high degree of accuracy. We then use these models to build personally optimized teaching sessions and boost learning.

In retina and in cortical slice the collective response of spiking neural populations is well described by "maximum-entropy" models in which only pairs of neurons interact. We asked, how should such interactions be organized to maximize the amount of information represented in population responses? To this end, we extended the linear-nonlinear-Poisson model of single neural response to include pairwise interactions, yielding a stimulus-dependent, pairwise maximum-entropy model. We found that as we varied the noise level in single neurons and the distribution of network inputs, the optimal pairwise interactions smoothly interpolated to achieve network functions that are usually regarded as discrete-stimulus decorrelation, error correction, and independent encoding. These functions reflected a trade-off between efficient consumption of finite neural bandwidth and the use of redundancy to mitigate noise. Spontaneous activity in the optimal network reflected stimulus-induced activity patterns, and single-neuron response variability overestimated network noise. Our analysis suggests that rather than having a single coding principle hardwired in their architecture, networks in the brain should adapt their function to changing noise and stimulus correlations.

A key issue in understanding the neural code for an ensemble of neurons is the nature and strength of correlations between neurons and how these correlations are related to the stimulus. The issue is complicated by the fact that there is not a single notion of independence or lack of correlation. We distinguish three kinds: ( 1) activity independence; ( 2) conditional independence; and ( 3) information independence. Each notion is related to an information measure: the information between cells, the information between cells given the stimulus, and the synergy of cells about the stimulus, respectively. We show that these measures form an interrelated framework for evaluating contributions of signal and noise correlations to the joint information conveyed about the stimulus and that at least two of the three measures must be calculated to characterize a population code. This framework is compared with others recently proposed in the literature. In addition, we distinguish questions about how information is encoded by a population of neurons from how that information can be decoded. Although information theory is natural and powerful for questions of encoding, it is not sufficient for characterizing the process of decoding. Decoding fundamentally requires an error measure that quantifies the importance of the deviations of estimated stimuli from actual stimuli. Because there is no a priori choice of error measure, questions about decoding cannot be put on the same level of generality as for encoding.