Modular Organization of Signal Transmission in Primate Somatosensory Cortex

Axonal patches are known as the major sites of synaptic connections in the cerebral cortex of higher order mammals. However, the functional role of these patches is highly debated. Patches are formed by populations of nearby neurons in a topographic manner and are recognized as the termination field...

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Main Authors: Yaqub Mir, László Zalányi, Emese Pálfi, Mária Ashaber, Anna W. Roe, Robert M. Friedman, László Négyessy
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-07-01
Series:Frontiers in Neuroanatomy
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnana.2022.915238/full
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author Yaqub Mir
Yaqub Mir
László Zalányi
Emese Pálfi
Mária Ashaber
Anna W. Roe
Anna W. Roe
Anna W. Roe
Robert M. Friedman
László Négyessy
author_facet Yaqub Mir
Yaqub Mir
László Zalányi
Emese Pálfi
Mária Ashaber
Anna W. Roe
Anna W. Roe
Anna W. Roe
Robert M. Friedman
László Négyessy
author_sort Yaqub Mir
collection DOAJ
description Axonal patches are known as the major sites of synaptic connections in the cerebral cortex of higher order mammals. However, the functional role of these patches is highly debated. Patches are formed by populations of nearby neurons in a topographic manner and are recognized as the termination fields of long-distance lateral connections within and between cortical areas. In addition, axons form numerous boutons that lie outside the patches, whose function is also unknown. To better understand the functional roles of these two distinct populations of boutons, we compared individual and collective morphological features of axons within and outside the patches of intra-areal, feedforward, and feedback pathways by way of tract tracing in the somatosensory cortex of New World monkeys. We found that, with the exception of tortuosity, which is an invariant property, bouton spacing and axonal convergence properties differ significantly between axons within patch and no-patch domains. Principal component analyses corroborated the clustering of axons according to patch formation without any additional effect by the type of pathway or laminar distribution. Stepwise logistic regression identified convergence and bouton density as the best predictors of patch formation. These findings support that patches are specific sites of axonal convergence that promote the synchronous activity of neuronal populations. On the other hand, no-patch domains could form a neuroanatomical substrate to diversify the responses of cortical neurons.
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spelling doaj.art-64fdbf66c94d4f7da1c7bc4e13d0178b2022-12-22T01:21:53ZengFrontiers Media S.A.Frontiers in Neuroanatomy1662-51292022-07-011610.3389/fnana.2022.915238915238Modular Organization of Signal Transmission in Primate Somatosensory CortexYaqub Mir0Yaqub Mir1László Zalányi2Emese Pálfi3Mária Ashaber4Anna W. Roe5Anna W. Roe6Anna W. Roe7Robert M. Friedman8László Négyessy9Theoretical Neuroscience and Complex Systems Group, Department of Computational Sciences, Wigner Research Centre for Physics, Budapest, HungaryJános Szentágothai Doctoral School of Neurosciences, Semmelweis University, Budapest, HungaryTheoretical Neuroscience and Complex Systems Group, Department of Computational Sciences, Wigner Research Centre for Physics, Budapest, HungaryDepartment of Anatomy, Histology and Embryology, Semmelweis University, Budapest, HungaryCalifornia Institute of Technology, Department of Biology and Biological Engineering, Pasadena, CA, United StatesDivision of Neuroscience, Oregon National Primate Research Center, Oregon Health and Science University, Beaverton, OR, United StatesInterdisciplinary Institute of Neuroscience and Technology, School of Medicine, Zhejiang University, Hangzhou, ChinaKey Laboratory of Biomedical Engineering of Ministry of Education, College of Biomedical Engineering and Instrument Science, Zhejiang University, Hangzhou, ChinaDivision of Neuroscience, Oregon National Primate Research Center, Oregon Health and Science University, Beaverton, OR, United StatesTheoretical Neuroscience and Complex Systems Group, Department of Computational Sciences, Wigner Research Centre for Physics, Budapest, HungaryAxonal patches are known as the major sites of synaptic connections in the cerebral cortex of higher order mammals. However, the functional role of these patches is highly debated. Patches are formed by populations of nearby neurons in a topographic manner and are recognized as the termination fields of long-distance lateral connections within and between cortical areas. In addition, axons form numerous boutons that lie outside the patches, whose function is also unknown. To better understand the functional roles of these two distinct populations of boutons, we compared individual and collective morphological features of axons within and outside the patches of intra-areal, feedforward, and feedback pathways by way of tract tracing in the somatosensory cortex of New World monkeys. We found that, with the exception of tortuosity, which is an invariant property, bouton spacing and axonal convergence properties differ significantly between axons within patch and no-patch domains. Principal component analyses corroborated the clustering of axons according to patch formation without any additional effect by the type of pathway or laminar distribution. Stepwise logistic regression identified convergence and bouton density as the best predictors of patch formation. These findings support that patches are specific sites of axonal convergence that promote the synchronous activity of neuronal populations. On the other hand, no-patch domains could form a neuroanatomical substrate to diversify the responses of cortical neurons.https://www.frontiersin.org/articles/10.3389/fnana.2022.915238/fullanterograde labelingboutonconvergencemultivariate analysissquirrel monkey
spellingShingle Yaqub Mir
Yaqub Mir
László Zalányi
Emese Pálfi
Mária Ashaber
Anna W. Roe
Anna W. Roe
Anna W. Roe
Robert M. Friedman
László Négyessy
Modular Organization of Signal Transmission in Primate Somatosensory Cortex
Frontiers in Neuroanatomy
anterograde labeling
bouton
convergence
multivariate analysis
squirrel monkey
title Modular Organization of Signal Transmission in Primate Somatosensory Cortex
title_full Modular Organization of Signal Transmission in Primate Somatosensory Cortex
title_fullStr Modular Organization of Signal Transmission in Primate Somatosensory Cortex
title_full_unstemmed Modular Organization of Signal Transmission in Primate Somatosensory Cortex
title_short Modular Organization of Signal Transmission in Primate Somatosensory Cortex
title_sort modular organization of signal transmission in primate somatosensory cortex
topic anterograde labeling
bouton
convergence
multivariate analysis
squirrel monkey
url https://www.frontiersin.org/articles/10.3389/fnana.2022.915238/full
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