The sensory neocortex consists of hierarchically-organized areas reciprocally connected via feedforward and feedback circuits. Feedforward connections shape the receptive field properties of neurons in higher areas within parallel streams specialized in processing specific stimulus attributes. Feedback connections have been implicated in top-down modulations, such as attention, prediction and sensory context. However, their computational role remains unknown, partly because we lack knowledge about rules of feedback connectivity to constrain models of feedback function. For example, it is unknown whether feedback connections maintain stream-specific segregation, or integrate information across parallel streams. Using viral-mediated labeling of feedback connections arising from specific cytochrome-oxidase stripes of macaque visual area V2, here we show that feedback to the primary visual cortex (V1) is organized into parallel streams resembling the reciprocal feedforward pathways. This suggests that functionally-specialized V2 feedback channels modulate V1 responses to specific stimulus attributes, an organizational principle potentially extending to feedback pathways in other sensory systems.

The sensory neocortex consists of hierarchically-organized areas reciprocally connected via feedforward and feedback circuits. Feedforward connections shape the receptive field properties of neurons in higher areas within parallel streams specialized in processing specific stimulus attributes. Feedback connections, instead, have been implicated in top-down modulations, such as attention, prediction and sensory context. However, their computational role remains unknown, partly because we lack knowledge about rules of feedback connectivity to constrain models of feedback function. For example, it is unknown whether feedback connections maintain stream-specific segregation, or integrate information across parallel streams. Using selective viral-mediated labeling of feedback connections arising from specific cytochrome-oxidase stripes of macaque visual area V2, we find that feedback to the primary visual cortex (V1) is organized into parallel streams resembling the reciprocal feedforward pathways. These results suggest that specialized V2 feedback channels serve to modulate V1 responses to specific stimulus attributes, an organizational principle that could extend to other feedback pathways in sensory systems.Here we have investigated the anatomical and functional organization of FB connections to the primary visual cortex (V1) arising from the secondary visual area (V2) in the macaque monkey. This FB pathway is well suited to address questions of anatomical and functional specificity and parallel FB pathways, because V2 is partitioned into cytochrome-oxidase (CO) stripe compartments that receive segregated FF projections from specific V1 CO compartments and layers Hubel, 1984,1987), and CO compartments in V1 and V2 have specialized functional properties and maps Sincich and Horton, 2005). It is now well established that CO blobs project predominantly to V2 CO thin stripes, while V1 interblobs project to V2 thick and pale stripes (Federer et al., 2009;Sincich and Horton, 2002).These projections arise predominantly from V1 layers (L) 2/3, and 4B, and sparsely from 4A and 5/6, with L4B projecting more heavily to thick stripes compared to other stripe types (Federer et al., 2013;Sincich et al., 2010). However, it is debated whether V2-to-V1 FB connections form similar parallel pathways that segregate within V1 CO compartments (Angelucci et al., 2002a,b;Shmuel et al., 2005), therefore maintaining stream specificity, or diffusely project to all compartments (Stettler et al., 2002), thus integrating information across parallel streams. This controversy is primarily due to the lack, in previous anatomical studies, of sensitive anterograde neuroanatomical tracers capable of labeling V2-to-V1 axons fully and selectively, without also labeling the reciprocal V1-to-V2 FF projections. Here, using selective viral-mediated labeling of FB connections arising from specific V2 CO stripes, we show that, like V1-to-V2 FF connections, V2 FB connections to V1 are organized into multiple parallel streams that segregate within the CO comp...