A compact spatial map in V2 visual cortex

Summary Vision plays a critical role in guiding spatial navigation. A traditional view of the visual cortex is to compute a world-centered map of visual space, and visual neurons exhibit diverse tunings to simple or complex visual features. The neural representation of spatio-visual map in the visual cortex is thought to be transformed from spatial modulation signals at the hippocampal-entorhinal system. Although visual thalamic and cortical neurons have been shown to be modulated by spatial signals during navigation, the exact source of spatially modulated neurons within the visual circuit has never been identified, and the neural correlate underpinning a visuospatial or spatio-visual map remains elusive. To search for direct visuospatial and visuodirectional signals, here we record in vivo extracellular spiking activity in the secondary visual cortex (V2) from freely foraging rats in a naturalistic environment. We identify that V2 neurons forms a complete spatio-visual map with a wide range of spatial tunings, which resembles the classical spatial map that includes the place, head-direction, border, grid and conjunctive cells reported in the hippocampal-entorhinal network. These spatially tuned V2 neurons display stable responses to external visual cues, and are robust with respect to non- spatial environmental changes. Spatially and directionally tuned V2 neuronal firing persists in darkness, suggesting that this spatio-visual map is not completely dependent on visual inputs. Identification of functionally distinct spatial cell types in visual cortex expands its classical role of information coding beyond a retinotopic map of the eye-centered world.