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Neural basis of topographical disorientation in the primate posterior cingulate gyrus based on a labeled graph

  • Received: 23 June 2022 Revised: 29 August 2022 Accepted: 06 September 2022 Published: 09 September 2022
  • Patients with lesions in the posterior cingulate gyrus (PCG), including the retrosplenial cortex (RSC) and posterior cingulate cortex (PCC), cannot navigate in familiar environments, nor draw routes on a 2D map of the familiar environments. This suggests that the topographical knowledge of the environments (i.e., cognitive map) to find the right route to a goal is represented in the PCG, and the patients lack such knowledge. However, theoretical backgrounds in neuronal levels for these symptoms in primates are unclear. Recent behavioral studies suggest that human spatial knowledge is constructed based on a labeled graph that consists of topological connections (edges) between places (nodes), where local metric information, such as distances between nodes (edge weights) and angles between edges (node labels), are incorporated. We hypothesize that the population neural activity in the PCG may represent such knowledge based on a labeled graph to encode routes in both 3D environments and 2D maps. Since no previous data are available to test the hypothesis, we recorded PCG neuronal activity from a monkey during performance of virtual navigation and map drawing-like tasks. The results indicated that most PCG neurons responded differentially to spatial parameters of the environments, including the place, head direction, and reward delivery at specific reward areas. The labeled graph-based analyses of the data suggest that the population activity of the PCG neurons represents the distance traveled, locations, movement direction, and navigation routes in the 3D and 2D virtual environments. These results support the hypothesis and provide a neuronal basis for the labeled graph-based representation of a familiar environment, consistent with PCG functions inferred from the human clinicopathological studies.

    Citation: Yang Yu, Tsuyoshi Setogawa, Jumpei Matsumoto, Hiroshi Nishimaru, Hisao Nishijo. Neural basis of topographical disorientation in the primate posterior cingulate gyrus based on a labeled graph[J]. AIMS Neuroscience, 2022, 9(3): 373-394. doi: 10.3934/Neuroscience.2022021

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  • Patients with lesions in the posterior cingulate gyrus (PCG), including the retrosplenial cortex (RSC) and posterior cingulate cortex (PCC), cannot navigate in familiar environments, nor draw routes on a 2D map of the familiar environments. This suggests that the topographical knowledge of the environments (i.e., cognitive map) to find the right route to a goal is represented in the PCG, and the patients lack such knowledge. However, theoretical backgrounds in neuronal levels for these symptoms in primates are unclear. Recent behavioral studies suggest that human spatial knowledge is constructed based on a labeled graph that consists of topological connections (edges) between places (nodes), where local metric information, such as distances between nodes (edge weights) and angles between edges (node labels), are incorporated. We hypothesize that the population neural activity in the PCG may represent such knowledge based on a labeled graph to encode routes in both 3D environments and 2D maps. Since no previous data are available to test the hypothesis, we recorded PCG neuronal activity from a monkey during performance of virtual navigation and map drawing-like tasks. The results indicated that most PCG neurons responded differentially to spatial parameters of the environments, including the place, head direction, and reward delivery at specific reward areas. The labeled graph-based analyses of the data suggest that the population activity of the PCG neurons represents the distance traveled, locations, movement direction, and navigation routes in the 3D and 2D virtual environments. These results support the hypothesis and provide a neuronal basis for the labeled graph-based representation of a familiar environment, consistent with PCG functions inferred from the human clinicopathological studies.



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    Acknowledgments



    This research was supported by the Takeda Science Foundation and a research grant from the University of Toyama.

    Conflict of interest



    The authors declare no conflict of interest.

    Author contributions



    HisN and HirN conceived the study and designed the experiment. YY, TS, and HisN performed the experiment. YY, TS, HisN and JM analyzed data and wrote the paper. HisN, HirN, JM, and AB revised the paper. All the authors discussed the results and commented on the manuscript, and read and approved the final manuscript.

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