Morphological evidence for multiple distinct channels of corticogeniculate feedback originating in mid-level extrastriate visual areas of the ferret.

Abstract

Complementary reciprocal feedforward and feedback circuits connecting the visual thalamus with the visual cortex are essential for visual perception. These circuits predominantly connect primary and secondary visual cortex with the dorsal lateral geniculate nucleus (LGN). Although there are direct geniculocortical inputs to extrastriate visual cortex, whether reciprocal corticogeniculate neurons exist in extrastriate cortex is not known. Here we utilized virus-mediated retrograde tracing to reveal the presence of corticogeniculate neurons in three mid-level extrastriate visual cortical areas in ferrets: PMLS, PLLS, and 21a. We observed corticogeniculate neurons in all three extrastriate areas, although the density of virus-labeled corticogeniculate neurons in extrastriate cortex was an order of magnitude less than that in areas 17 and 18. A cluster analysis of morphological metrics quantified following reconstructions of the full dendritic arborizations of virus-labeled corticogeniculate neurons revealed six distinct cell types. Similar corticogeniculate cell types to those observed in areas 17 and 18 were also observed in PMLS, PLLS, and 21a. However, these unique cell types were not equally distributed across the three extrastriate areas. The majority of corticogeniculate neurons per cluster originated in a single area, suggesting unique parallel organizations for corticogeniculate feedback from each extrastriate area to the LGN. Together, our findings demonstrate direct feedback connections from mid-level extrastriate visual cortex to the LGN, supporting complementary reciprocal circuits at multiple processing stages along the visual hierarchy. Importantly, direct reciprocal connections between the LGN and extrastriate cortex, that bypass V1, could provide a substrate for residual vision following V1 damage.