A compact spatial map in V2 visual cortex

Abstract

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.

The RIFF: an automated environment for studying the neural basis of auditory-guided complex behavior

“…Thus, the spatially-tuned neurons described here are intermixed with neurons that do not differ much in their response properties from neurons in the primary auditory cortex. This evidence provided here adds to other recent studies that described spatially tuned neurons in many structures outside the hippocampal system 50, 51 , including visual cortex 52 , somatosensory cortex 53 , retrosplenial cortex 54 , and premotor cortex 55 . The role of these neurons in auditory processing, as well as in spatial navigation, requires further study.…”

Are Grid-Like Representations a Component of All Perception and Cognition?

“…Similarly, grid-like computation can be implemented in the somatosensory cortical columns to track the location of tactile features relative to the objects being touched. In the case of rat V2 grid cells, theory-driven hypotheses have been confirmed by preliminary experimental findings (Hawkins et al, 2019 ; Long et al, 2021a ). In the previous report, S1 grid cells were recorded across Layer IV-VI of the rat S1HL (hindlimb) area, and V2 grid cells were recorded across superficial and deep layers of the rat V2M area (Long and Zhang, 2021 ; Long et al, 2021a ); and some evidence has shown clustered or columnar structures in the primary and secondary areas of these sensory cortices (Horton and Adams, 2005 ; Laramee et al, 2013 ; Hubatz et al, 2020 ).…”

“…Notably, grid-like representations not only appear in the human mEC, but also in other traditionally thought non-spatial frontal brain areas, such as the human orbitofrontal cortex (OFC), ventromedial prefrontal cortex (vmPFC) and anterior and posterior cingulate cortex (ACC and PCC) (Constantinescu et al, 2016 ; Bao et al, 2019 ). Recently, grid cells have also been discovered in the rat primary somatosensory cortex (S1) (Long and Zhang, 2021 ) and the secondary visual cortex (V2) (Long et al, 2021a ). What are the roles and functional significance of these sensory cortical grid cells?…”

“…(A) Electrophysiological data show grid-like firing patterns from the rat primary somatosensory cortex (S1) (images are modified from Long and Zhang, 2021 , Cell Research ; reprinted with permission, Creative Commons CC BY license) and the secondary visual cortex (V2) while animals navigated in an open field arena. Color bar shows the firing rate in spikes/s (figure is modified from Long et al, 2021a , bioRxiv). (B) Human invasive electrophysiological data show grid-like representations in the anterior cingulate cortex during a virtual navigation task.…”

Uncovering spatial representations from spatiotemporal patterns of rodent hippocampal field potentials

“…Although we only investigated the rodent hippocampal circuit in this study, our “place” decoding analysis and methods can be readily applied to other rodent neocortical areas that encode spatial information, such as the entorhinal cortex, retrosplenial cortex, parietal cortex, primary somatosensory cortex, and primary and secondary visual cortices ( Hafting et al, 2005 ; Whitlock et al, 2008 ; Mao et al, 2017 ; Ji and Wilson, 2007 ; Haggerty and Ji, 2015 ; Hu et al, 2018 ; Long and Zhang, 2021 ; Long et al, 2021 ). Moreover, it has been shown that these sensory “place cells” are also modulated with local cortical theta rhythms during run behaviors and preserved phase precession ( Long and Zhang, 2021 ; Long et al, 2021 ). To date, experimental evidence of spatial modulated responses across many neocortical areas beyond the traditional hippocampal formation has been accumulating.…”