Higher-order (HO) thalamic nuclei interact extensively and reciprocally with the cerebral cortex. These corticothalamic (CT) interactions are thought to be important for sensation and perception, attention, and many other important brain functions. CT projections to HO thalamic nuclei, such as the visual pulvinar, originate from two different excitatory populations in cortical layers 5 and 6, whereas first-order nuclei (such as the dorsolateral geniculate nucleus; dLGN) only receive layer 6 CT input. It has been proposed that these layer 5 and layer 6 CT pathways have different functional influences on the HO thalamus, but this has never been directly tested. By optogenetically inactivating different CT populations in the primary visual cortex (V1) and recording single-unit activity from V1, dLGN, and pulvinar of awake mice, we demonstrate that layer 5, but not layer 6, CT projections drive visual responses in the pulvinar, even while both pathways provide retinotopic, baseline excitation to their thalamic targets. Inactivating the superior colliculus also suppressed visual responses in the same subregion of the pulvinar, demonstrating that cortical layer 5 and subcortical inputs both contribute to HO visual thalamic activity-even at the level of putative single neurons. Altogether, these results indicate a functional division of "driver" and "modulator" CT pathways from V1 to the visual thalamus in vivo.
Keywords: colliculus; corticothalamic; optogenetics; pulvinar; retinotopy; thalamus; visual cortex.
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