Developmental neuronal origin regulates neocortical map formation

Summary: Sensory neurons in the neocortex exhibit distinct functional selectivity to constitute the neural map. While neocortical map of the visual cortex in higher mammals is clustered, it displays a striking “salt-and-pepper” pattern in rodents. However, little is known about the origin and basis...

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Main Authors: Yang Lin, Xin-Jun Zhang, Jiajun Yang, Shuo Li, Laura Li, Xiaohui Lv, Jian Ma, Song-Hai Shi
Format: Article
Language:English
Published: Elsevier 2023-03-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S221112472300181X
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author Yang Lin
Xin-Jun Zhang
Jiajun Yang
Shuo Li
Laura Li
Xiaohui Lv
Jian Ma
Song-Hai Shi
author_facet Yang Lin
Xin-Jun Zhang
Jiajun Yang
Shuo Li
Laura Li
Xiaohui Lv
Jian Ma
Song-Hai Shi
author_sort Yang Lin
collection DOAJ
description Summary: Sensory neurons in the neocortex exhibit distinct functional selectivity to constitute the neural map. While neocortical map of the visual cortex in higher mammals is clustered, it displays a striking “salt-and-pepper” pattern in rodents. However, little is known about the origin and basis of the interspersed neocortical map. Here we report that the intricate excitatory neuronal kinship-dependent synaptic connectivity influences precise functional map organization in the mouse primary visual cortex. While sister neurons originating from the same neurogenic radial glial progenitors (RGPs) preferentially develop synapses, cousin neurons derived from amplifying RGPs selectively antagonize horizontal synapse formation. Accordantly, cousin neurons in similar layers exhibit clear functional selectivity differences, contributing to a salt-and-pepper architecture. Removal of clustered protocadherins (cPCDHs), the largest subgroup of the diverse cadherin superfamily, eliminates functional selectivity differences between cousin neurons and alters neocortical map organization. These results suggest that developmental neuronal origin regulates neocortical map formation via cPCDHs.
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spelling doaj.art-78f18c874b03496b9869e4ffd93aed182023-02-27T04:07:07ZengElsevierCell Reports2211-12472023-03-01423112170Developmental neuronal origin regulates neocortical map formationYang Lin0Xin-Jun Zhang1Jiajun Yang2Shuo Li3Laura Li4Xiaohui Lv5Jian Ma6Song-Hai Shi7IDG/McGovern Institute for Brain Research, Tsinghua-Peking Center for Life Sciences, Beijing Frontier Research Center for Biological Structure, Beijing Advanced Innovation Center for Structural Biology, School of Life Sciences, Tsinghua University, Beijing 100084, ChinaDevelopmental Biology Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, 1275 York Avenue, New York, NY 10065, USAIDG/McGovern Institute for Brain Research, Tsinghua-Peking Center for Life Sciences, Beijing Frontier Research Center for Biological Structure, Beijing Advanced Innovation Center for Structural Biology, School of Life Sciences, Tsinghua University, Beijing 100084, ChinaIDG/McGovern Institute for Brain Research, Tsinghua-Peking Center for Life Sciences, Beijing Frontier Research Center for Biological Structure, Beijing Advanced Innovation Center for Structural Biology, School of Life Sciences, Tsinghua University, Beijing 100084, ChinaIDG/McGovern Institute for Brain Research, Tsinghua-Peking Center for Life Sciences, Beijing Frontier Research Center for Biological Structure, Beijing Advanced Innovation Center for Structural Biology, School of Life Sciences, Tsinghua University, Beijing 100084, ChinaIDG/McGovern Institute for Brain Research, Tsinghua-Peking Center for Life Sciences, Beijing Frontier Research Center for Biological Structure, Beijing Advanced Innovation Center for Structural Biology, School of Life Sciences, Tsinghua University, Beijing 100084, ChinaIDG/McGovern Institute for Brain Research, Tsinghua-Peking Center for Life Sciences, Beijing Frontier Research Center for Biological Structure, Beijing Advanced Innovation Center for Structural Biology, School of Life Sciences, Tsinghua University, Beijing 100084, ChinaIDG/McGovern Institute for Brain Research, Tsinghua-Peking Center for Life Sciences, Beijing Frontier Research Center for Biological Structure, Beijing Advanced Innovation Center for Structural Biology, School of Life Sciences, Tsinghua University, Beijing 100084, China; Chinese Institute for Brain Research, Beijing, China; Corresponding authorSummary: Sensory neurons in the neocortex exhibit distinct functional selectivity to constitute the neural map. While neocortical map of the visual cortex in higher mammals is clustered, it displays a striking “salt-and-pepper” pattern in rodents. However, little is known about the origin and basis of the interspersed neocortical map. Here we report that the intricate excitatory neuronal kinship-dependent synaptic connectivity influences precise functional map organization in the mouse primary visual cortex. While sister neurons originating from the same neurogenic radial glial progenitors (RGPs) preferentially develop synapses, cousin neurons derived from amplifying RGPs selectively antagonize horizontal synapse formation. Accordantly, cousin neurons in similar layers exhibit clear functional selectivity differences, contributing to a salt-and-pepper architecture. Removal of clustered protocadherins (cPCDHs), the largest subgroup of the diverse cadherin superfamily, eliminates functional selectivity differences between cousin neurons and alters neocortical map organization. These results suggest that developmental neuronal origin regulates neocortical map formation via cPCDHs.http://www.sciencedirect.com/science/article/pii/S221112472300181XCP: Neuroscience
spellingShingle Yang Lin
Xin-Jun Zhang
Jiajun Yang
Shuo Li
Laura Li
Xiaohui Lv
Jian Ma
Song-Hai Shi
Developmental neuronal origin regulates neocortical map formation
Cell Reports
CP: Neuroscience
title Developmental neuronal origin regulates neocortical map formation
title_full Developmental neuronal origin regulates neocortical map formation
title_fullStr Developmental neuronal origin regulates neocortical map formation
title_full_unstemmed Developmental neuronal origin regulates neocortical map formation
title_short Developmental neuronal origin regulates neocortical map formation
title_sort developmental neuronal origin regulates neocortical map formation
topic CP: Neuroscience
url http://www.sciencedirect.com/science/article/pii/S221112472300181X
work_keys_str_mv AT yanglin developmentalneuronaloriginregulatesneocorticalmapformation
AT xinjunzhang developmentalneuronaloriginregulatesneocorticalmapformation
AT jiajunyang developmentalneuronaloriginregulatesneocorticalmapformation
AT shuoli developmentalneuronaloriginregulatesneocorticalmapformation
AT laurali developmentalneuronaloriginregulatesneocorticalmapformation
AT xiaohuilv developmentalneuronaloriginregulatesneocorticalmapformation
AT jianma developmentalneuronaloriginregulatesneocorticalmapformation
AT songhaishi developmentalneuronaloriginregulatesneocorticalmapformation