Corticogeniculate Feedback Sharpens the Temporal Resolution of LGN Responses

Corticogeniculate circuits connect the primary visual cortex with the visual thalamus in the feedback direction and are a subset of corticothalamic circuits that are ubiquitous across mammals and sensory systems. Corticogeniculate feedback is anatomically robust in that the number of synapses onto thalamic relay neurons originating from the cortex far outnumber those originating from the retina. However, the functional role of corticogeniculate feedback in vision has remained a stubborn puzzle in visual neuroscience. We employed a novel combination of virus-mediated gene delivery and optogenetics to selectively and reversibly manipulate the activity of corticogeniculate neurons in vivo. We recorded the responses of thalamic neurons in response to visual stimulation with additional optogenetic activation of corticogeniculate feedback. We discovered that corticogeniculate feedback dramatically sharpens the response precision of visual thalamic neurons. Specifically, stimulation of corticogeniculate feedback reduced onset response latencies, increased spike timing precision, and reduced the size of the classical receptive field among thalamic neurons. We propose a simple circuit-based model to explain these effects. Together, our findings suggest that corticogeniculate feedback controls the timing of thalamic responses to visual stimuli and broadly support the notion that the thalamus is much more than a simple relay of sensory information.