The role of visuomotor coupling in the development of sensory processing in mouse visual cortex

The current prevailing understanding of sensory processing in cortical areas is largely based on the presentation framework proposes that neural activity form presentations of external stimulus. However, with recent advances in technologies of recording neuronal activity in awake behaving animals, it has been shown that the primary visual cortex (V1) is also strongly driven by self-movement, suggesting that the presentation framework of visual cortex function is incomplete. Particularly, a subset of neurons in V1 selectively respond to transient visuomotor mismatches, and it could be explained by the predictive coding framework which postulates V1 compares the predicted and received visual input and sense the difference between the two. Experience of normal visuomotor coupling has been shown to be crucial for the development of visual-guided behavior, therefore it is likely that the prediction of visual input depends on the experience of visuomotor coupling, which shapes the functional development of V1. In the present study, we use a virtual reality system and trained dark-reared mice with either normal or random visuomotor coupling, and recorded the neural activity in layer 2/3 neurons of V1. We show that mismatch responses in excitatory neurons were strongly dependent on visuomotor experience. By recording several different types of layer 2/3 interneurons in V1 and manipulating their activity with designer receptor exclusively activated by designer drugs (DREADDs) or optogenetics tools, we propose a circuit model showing that the mismatch response could be the result of a disinhibition mediated by local somatostatin (SST) interneurons. Mismatch responses in both groups of mice with different visuomotor training conditions merged together after they were transferred to normal rearing environment. These data demonstrate that neurons in layer 2/3 mouse V1 computes a difference between an excitatory motor-related input and an inhibitory visual input, where the balance between the two inputs is finely tuned by visuomotor experience.