In every mammalian sensory system, descending corticothalamic projections, which originate in multiple cortical areas and reach several thalamic relay nuclei, far outnumber the terminals of parallel feedforward projections that carry information from the periphery to the same thalamic structures. Despite numerous studies and a series of theories which have attempted to illuminate the role of these massive descending feedback projections in sensory information processing, the functional relevance of these pathways remains largely unknown. Here, we propose to investigate the physiological contribution of somatosensory corticothalamic projections to the tactile responses of neurons located in the main thalamic relay nucleus of the trigeminal system, the ventral posterior medial nucleus. Based on extensive preliminary data, we propose that, by providing both excitatory and inhibitory influences to the somatosensory thalamus, corticofugal projections endow thalamic neurons with the ability to enhance the differences between orthogonal tactile stimuli and modify the type of information transmitted to the cortex according to the behavioral state of the animal. The functional roles of cortical feedback projections will be assessed by a series of experiments that combine simultaneous multi-site neural ensemble recordings and reversible cortical inactivation, in behaving animals. The activity of large populations of single cortical and thalamic neurons will be simultaneously recorded in the same rat, while its facial whiskers are stimulated with complex tactile stimuli generated either passively or during an active behavioral whisker-dependant discrimination task. Focal regions of the primary somatosensory cortex will be reversibly inactivated during these simultaneous thalamocortical recordings. This will allow us to evaluate how cortical projections contribute to the generation of thalamic sensory responses to complex tactile stimuli. We predict that in rats cortical feedback facilitates the thalamic responses to a whisker column stimulus, while suppressing responses to a whisker row. Modifications in the balance of these contrasting influences should also account for the observation that VPM neurons become capable of integrating rapid sequences of whisker column stimuli generated during active whisker exploration.
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