Interdigitating Modules for Visual Processing During Locomotion and Rest in Mouse V1

Layer 1 of V1 has been shown to receive locomotion-related signals from the dorsal lateral geniculate (dLGN) and lateral posterior (LP) thalamic nuclei (Roth et al., 2016). Inputs from the dLGN terminate in M2+ patches while inputs from LP target M2- interpatches (DSouza et al., 2019) suggesting that motion related signals are processed in distinct networks. Here, we investigated by calcium imaging in head-fixed awake mice whether L2/3 neurons underneath L1 M2+ and M2- modules are differentially activated by locomotion, and whether distinct networks of feedback connections from higher cortical areas to L1 may contribute to these differences. We found that strongly locomotion-modulated cell clusters during visual stimulation were aligned with M2- interpatches, while weakly modulated cells clustered under M2+ patches. Unlike M2+ patch cells, pairs of M2- interpatch cells showed increased correlated variability of calcium transients when the sites in the visuotopic map were far apart, suggesting that activity is integrated across large parts of the visual field. Pathway tracing further suggests that strong locomotion modulation in L2/3 M2- interpatch cells of V1 relies on looped, like-to-like networks between apical dendrites of MOs-, PM- and RSP-projecting neurons and feedback input from these areas to L1. M2- interpatches receive strong inputs from SST neurons, suggesting that during locomotion these interneurons influence the firing of specific subnetworks by controlling the excitability of apical dendrites in M2- interpatches. eLife digestDuring body, head and eye movements, many cells in the visual system increase their firing rate in order to distinguish between self-generated and externally generated image motion. While progress has been made in determining the brain circuits and cell types underlying this state-dependent signal, it is not known whether movement-modulated cells in primary visual cortex (V1) are distributed randomly or are spatially clustered. Meier et al., found that locomotion modulation is greater in periodically spaced clusters of layer (L) 2/3, which are aligned with M2 muscarinic acetylcholine receptor-negative interpatches of L1. Cells aligned with interpatches have higher sensitivity to the direction of visual motion at high speed (Ji et al., 2015). Cell pairs between visuotopically distant interpatch clusters show increased response correlations, suggesting signal integration across large parts of the visual field. The results further demonstrate that L1 M2- interpatches are densely innervated by somatostatin (SST)-expressing neurons, are targets of apical dendrites of MOs-(secondary motor cortex), PM-(posteromedial area) and RSP-(posterior retrosplenial cortex)-projecting neurons and are recipients of inputs from these sources. This indicates that L1 interpatches in V1 are targets for non-retinal movement-related feedback signals.