Cortically-Controlled Population Stochastic Facilitation as a Plausible Substrate for Guiding Sensory Transfer across the Thalamic Gateway

The thalamus is the primary gateway that relays sensory information to the cerebral cortex. While a single recipient cortical cell receives the convergence of many principal relay cells of the thalamus, each thalamic cell in turn integrates a dense and distributed synaptic feedback from the cortex. During sensory processing, the influence of this functional loop remains largely ignored. Using dynamic-clamp techniques in thalamic slices in vitro, we combined theoretical and experimental approaches to implement a realistic hybrid retino-thalamo-cortical pathway mixing biological cells and simulated circuits. The synaptic bombardment of cortical origin was mimicked through the injection of a stochastic mixture of excitatory and inhibitory conductances, resulting in a gradable correlation level of afferent activity shared by thalamic cells. The study of the impact of the simulated cortical input on the global retinocortical signal transfer efficiency revealed a novel control mechanism resulting from the collective resonance of all thalamic relay neurons. We show here that the transfer efficiency of sensory input transmission depends on three key features: i) the number of thalamocortical cells involved in the many-to-one convergence from thalamus to cortex, ii) the statistics of the corticothalamic synaptic bombardment and iii) the level of correlation imposed between converging thalamic relay cells. In particular, our results demonstrate counterintuitively that the retinocortical signal transfer efficiency increases when the level of correlation across thalamic cells decreases. This suggests that the transfer efficiency of relay cells could be selectively amplified when they become simultaneously desynchronized by the cortical feedback. When applied to the intact brain, this network regulation mechanism could direct an attentional focus to specific thalamic subassemblies and select the appropriate input lines to the cortex according to the descending influence of cortically-defined priors. Author Summary Most of the sensory information in the early visual system is relayed from the retina to the primary visual cortex through principal relay cells in the thalamus. While relay cells receive approximate to 7-16% of their synapses from retina, they integrate the synaptic barrage of a dense cortical feedback, which accounts for more than 60% of their total input. This feedback is thought to carry some form of prior resulting from the computation performed in cortical areas, which influences the response of relay cells, presumably by regulating the transfer of sensory information to cortical areas. Nevertheless, its statistical nature (input synchronization, excitation/inhibition ratio, etc.) and the cellular mechanisms gating thalamic transfer are largely ignored. Here we implemented hybrid circuits (biological and modeled cells) reproducing the main features of the thalamic gate and explored the functional impact of various statistics of the cortical input. We found that the regulation of sensory information is critically determined by the statistical coherence of the cortical synaptic bombardment associated with a stochastic facilitation process. We propose that this tuning mechanism could operate in the intact brain to selectively filter the sensory information reaching cortical areas according to attended features predesignated by the cortical feedback.