Imbalance adaptation of excitation and inhibition increases the throughput of information to the cortex
The response of neurons to natural stimulation depends on the past history of stimulation. Sensitivity increases during periods of weak stimulation, whereas when the background stimulation is strong the sensitivity is reduced. This form of gain control is called sensory adaptation. Our research is focused on the mechanisms of adaptation in the cortex and the thalamus. We have found that cortical adaptation is highly specific to the stimulated whisker and thus indicate that inputs from different whiskers undergo independent adaptation paths. We also study how adaptation affects the balance between excitation and inhibition. Our data provide direct indication for faster adaptation rate of inhibition, when compared to excitation.
From brainstem to cortex
Parallel processing and adaptation are central hallmarks of sensory systems. It was previously suggested that parallel streams may resolve the coding ambiguity associated inherently with adaptation. Both major ascending pathways in the tactile system, the lemniscal and paralemniscal, undergo profound adaptation. We investigated the adaptation properties of these pathways using in vivo intracellular recordings at their divergence point, the brainstem trigeminal complex. Unexpectedly, increasing the intensity of stimulation entailed opposite adaptation effects in these pathways. Specifically, increasing the intensity caused less adaptation in the lemniscal pathway and more in the paralemniscal pathway. Consequently, increasing intensity sharpens lemniscal receptive field profiles as adaptation progresses. Notably, we found specific adaptation ‘signatures’ across cortical layers matching the brainstem’s adaptation profiles, as expected from anatomical projections. Given the orthogonal behavior of these parallel pathways, combining their inputs may resolve the inherent ambiguity of adaptive coding.
Adaptation is typically associated with attenuation of neuronal response during sustained or repetitive sensory stimulation and a gradual recovery of the response afterword. To test how the response recovers following adaptation we recorded in-vivo the membrane potential of putative layer IV cells of the barrel cortex by applying a test stimulus following adapting the response of the principal whisker. Unexpectedly, in more than 30% of the cells the subthreshold and firing response to test stimulation during the recovery period facilitated significantly, peaking at different time intervals (<1 sec) after the adapting stimulation across the population. Recordings under different holding currents revealed that the enhanced response to test stimulus was associated with delayed recovery of evoked inhibition from adaptation compared to excitation. Hence, our data provides the first mechanistic explanation of sensory facilitation following adaptation and suggest that adaptation may increases the sensitivity of cortical neurons to sensory stimulation by altering the balance between excitation and inhibition
Cortical receptive fields
Neurons in the barrel cortex and the thalamus respond preferentially to stimulation of one whisker (the principal whisker) and weakly to several adjacent whiskers. Cortical neurons, unlike thalamic cells, gradually adapt to repeated whisker stimulations. Whether cortical adaptation is specific to the stimulated whisker is not known. The aim of this intracellular study was to determine whether the response of a cortical cell to stimulation of an adjacent whisker would be affected by previous adaptation induced by stimulation of the principal whisker and vice versa. Using a high-frequency stimulation that causes substantial adaptation in the cortex and much less adaptation in the thalamus, we show that cortical adaptation evoked by a train of stimuli applied to one whisker does not affect the synaptic response to subsequent stimulation of a neighboring whisker. Our data indicate that intrinsic mechanisms are not involved in cortical adaptation. Thalamic recordings obtained under the same conditions demonstrated that an adjacent whisker response was not generated in the thalamus, indicating that the observed whisker-specific adaptation results from diverging thalamic inputs or from cortical integration.