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

IF 3.1 Q2 NEUROSCIENCES
AIMS Neuroscience Pub Date : 2022-09-09 eCollection Date: 2022-01-01 DOI:10.3934/Neuroscience.2022021
Yang Yu, Tsuyoshi Setogawa, Jumpei Matsumoto, Hiroshi Nishimaru, Hisao Nishijo
{"title":"Neural basis of topographical disorientation in the primate posterior cingulate gyrus based on a labeled graph.","authors":"Yang Yu, Tsuyoshi Setogawa, Jumpei Matsumoto, Hiroshi Nishimaru, Hisao Nishijo","doi":"10.3934/Neuroscience.2022021","DOIUrl":null,"url":null,"abstract":"<p><p>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.</p>","PeriodicalId":7732,"journal":{"name":"AIMS Neuroscience","volume":"9 3","pages":"373-394"},"PeriodicalIF":3.1000,"publicationDate":"2022-09-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9581735/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"AIMS Neuroscience","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.3934/Neuroscience.2022021","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2022/1/1 0:00:00","PubModel":"eCollection","JCR":"Q2","JCRName":"NEUROSCIENCES","Score":null,"Total":0}
引用次数: 0

Abstract

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.

Abstract Image

Abstract Image

Abstract Image

基于标签图的灵长类后扣带回地形迷失的神经基础。
扣带回后部(PCG)(包括脾后部皮层(RSC)和扣带回后部皮层(PCC))发生病变的患者无法在熟悉的环境中导航,也无法在熟悉环境的二维地图上绘制路线。这表明,找到通往目标的正确路线所需的环境地形知识(即认知地图)在 PCG 中有所体现,而患者缺乏这种知识。然而,灵长类动物出现这些症状的神经元水平的理论背景尚不清楚。最近的行为学研究表明,人类的空间知识是基于一个标签图构建的,该标签图由地点(节点)之间的拓扑连接(边)组成,其中包含局部度量信息,如节点之间的距离(边权重)和边之间的角度(节点标签)。我们假设,PCG 中的群体神经活动可能代表了基于标记图的此类知识,从而对三维环境和二维地图中的路线进行编码。由于之前没有数据可以验证这一假设,我们记录了一只猴子在完成虚拟导航和类似地图绘制任务时的 PCG 神经元活动。结果表明,大多数 PCG 神经元对环境的空间参数(包括地点、头部方向和特定奖励区域的奖励传递)有不同的反应。基于标记图的数据分析表明,PCG 神经元群的活动代表了三维和二维虚拟环境中的行进距离、位置、运动方向和导航路线。这些结果支持了这一假设,并为基于标签图的熟悉环境表征提供了神经元基础,这与从人类临床病理学研究中推断出的 PCG 功能是一致的。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
AIMS Neuroscience
AIMS Neuroscience NEUROSCIENCES-
CiteScore
4.20
自引率
0.00%
发文量
26
审稿时长
8 weeks
期刊介绍: AIMS Neuroscience is an international Open Access journal devoted to publishing peer-reviewed, high quality, original papers from all areas in the field of neuroscience. The primary focus is to provide a forum in which to expedite the speed with which theoretical neuroscience progresses toward generating testable hypotheses. In the presence of current and developing technology that offers unprecedented access to functions of the nervous system at all levels, the journal is designed to serve the role of providing the widest variety of the best theoretical views leading to suggested studies. Single blind peer review is provided for all articles and commentaries.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信