Visuomotor interactions in the mouse forebrain mediated by extrastriate cortico-cortical pathways

Abstract

The mammalian visual system can be broadly divided into two functional processing pathways: a dorsal stream supporting visually and spatially guided actions, and a ventral stream enabling object recognition. In rodents, the majority of visual signaling in the dorsal stream is transmitted to frontal motor cortices via extrastriate visual areas surrounding V1, but exactly where and to what extent V1 feeds into motor-projecting visual regions is not well known. To address this we employed a dual labeling strategy in male and female mice in which efferent projections from V1 were labeled anterogradely, and motor-projecting neurons in higher visual areas were labeled with retrogradely traveling adeno-associated virus (rAAV-retro) injected in M2. In flattened sections of dorsal cortex, the most pronounced colocalization V1 output and M2 input occurred in extrastriate areas AM, PM, RL and AL. Coronal sections further showed that neurons in both superficial and deep layers in these regions project to M2, but high resolution volumetric reconstructions revealed that the vast majority of putative synaptic contacts from V1 onto M2-projecting neurons occurred in layer 2/3. These findings support the existence of a dorsal processing stream in the mouse visual system, where visual signals reach motor cortex largely via feedforward projections in anteriorly and medially located extrastriate areas. Significance StatementVisually guided motor behavior depends on the long-distance relay of signals from visual cortex to frontal motor cortices, but the neuroanatomical connections linking visual and motor systems in rodents are not fully charted. Here, we characterized such pathways by injecting anterograde tracers in primary visual cortex (V1) and retrogradely traveling virus in motor cortex (M2), and visualizing where the projections overlapped. We found preferential colocalization of V1 output and M2-projecting neurons in anteriorly- and medially-located higher visual areas. 3D volumetric reconstructions further showed high rates of putative synaptic connections mainly in superficial layers. Thus, visual signals in the mouse dorsal visual stream reach motor areas at least in part via superficial, feedforward connections in a subset of extrastriate areas.