Parallel streams of direct corticogeniculate feedback from mid-level extrastriate cortex in the macaque monkey

Abstract

First order thalamic nuclei receive feedforward signals from peripheral receptors and relay these signals to primary sensory cortex. Primary sensory cortex, in turn, provides reciprocal feedback to first order thalamus. Because the vast majority of sensory thalamocortical inputs target primary sensory cortex, their complementary corticothalamic neurons are assumed to be similarly restricted to primary sensory cortex. We upend this assumption by characterizing morphologically diverse neurons in multiple mid-level visual cortical areas of the primate (Macaca mulatta) brain that provide direct feedback to the primary visual thalamus, the dorsal lateral geniculate nucleus (LGN). Although the majority of geniculocortical neurons project to primary visual cortex (V1), a minority, located mainly in the koniocellular LGN layers, provide direct input to extrastriate visual cortex. These “V1-bypassing” projections may be implicated in blindsight. We hypothesized that geniculocortical inputs directly targeting extrastriate cortex should be complemented by reciprocal corticogeniculate circuits. Using virus-mediated circuit tracing, we discovered corticogeniculate neurons throughout three mid-level extrastriate areas: MT, MST, and V4. Quantitative morphological analyses revealed non-uniform distributions of unique cell types across areas. Many extrastriate corticogeniculate neurons had spiny stellate morphology, suggesting possible targeting of koniocellular LGN layers. Importantly though, multiple morphological types were observed across areas. Such morphological diversity could suggest parallel streams of V1-bypassing corticogeniculate feedback at multiple stages of the visual processing hierarchy. Furthermore, the presence of corticogeniculate neurons across visual cortex necessitates a reevaluation of the LGN as a hub for visual information rather than a simple relay.

Significance Statement First order thalamic nuclei are most strongly connected in feedforward and feedback directions with primary sensory cortex. In the visual system, direct feedforward circuits link the visual thalamus with higher-order, extrastriate visual areas, although the function of these less-common pathways remains unknown. Here we demonstrate for the first time the presence of complementary direct feedback connections between multiple extrastriate visual cortical areas and the visual thalamus in the primate brain. Although sparse, extrastriate corticogeniculate circuits are consistently present and contain morphologically diverse neurons, suggesting parallel streams of extrastriate feedback. These findings indicate an evolutionary conservation of circuits that integrate information from throughout the visual processing hierarchy within the visual thalamus.