Differential Prefrontal White Matter Development in Chimpanzees and Humans
A comparison of developmental patterns of white matter (WM) within the prefrontal region between humans and nonhuman primates is key to understanding human brain evolution. WM mediates complex cognitive processes and has reciprocal connections with posterior processing regions [1, 2]. Although the d...
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Veröffentlicht in: | Current biology 2011-08, Vol.21 (16), p.1397-1402 |
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creator | Sakai, Tomoko Mikami, Akichika Tomonaga, Masaki Matsui, Mie Suzuki, Juri Hamada, Yuzuru Tanaka, Masayuki Miyabe-Nishiwaki, Takako Makishima, Haruyuki Nakatsukasa, Masato Matsuzawa, Tetsuro |
description | A comparison of developmental patterns of white matter (WM) within the prefrontal region between humans and nonhuman primates is key to understanding human brain evolution. WM mediates complex cognitive processes and has reciprocal connections with posterior processing regions [1, 2]. Although the developmental pattern of prefrontal WM in macaques differs markedly from that in humans [3], this has not been explored in our closest evolutionary relative, the chimpanzee. The present longitudinal study of magnetic resonance imaging scans demonstrated that the prefrontal WM volume in chimpanzees was immature and had not reached the adult value during prepuberty, as observed in humans but not in macaques. However, the rate of prefrontal WM volume increase during infancy was slower in chimpanzees than in humans. These results suggest that a less mature and more protracted elaboration of neuronal connections in the prefrontal portion of the developing brain existed in the last common ancestor of chimpanzees and humans, and that this served to enhance the impact of postnatal experiences on neuronal connectivity. Furthermore, the rapid development of the human prefrontal WM during infancy may help the development of complex social interactions, as well as the acquisition of experience-dependent knowledge and skills to shape neuronal connectivity.
► This is the first longitudinal investigation into brain development in chimpanzees ► Chimpanzees and humans share a protracted development of prefrontal white matter ► Only humans show a dramatic increase in prefrontal white matter during infancy ► This may help the development of human-specific cognition and neuronal connectivity |
doi_str_mv | 10.1016/j.cub.2011.07.019 |
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► This is the first longitudinal investigation into brain development in chimpanzees ► Chimpanzees and humans share a protracted development of prefrontal white matter ► Only humans show a dramatic increase in prefrontal white matter during infancy ► This may help the development of human-specific cognition and neuronal connectivity</description><identifier>ISSN: 0960-9822</identifier><identifier>EISSN: 1879-0445</identifier><identifier>DOI: 10.1016/j.cub.2011.07.019</identifier><identifier>PMID: 21835623</identifier><language>eng</language><publisher>England: Elsevier Inc</publisher><subject>adults ; Animals ; Biological Evolution ; Brain ; cognition ; Cognitive ability ; Development ; Evolution ; human development ; Humans ; infancy ; Longitudinal Studies ; Macaca ; Macaca mulatta ; Magnetic resonance imaging ; Magnetic Resonance Imaging - methods ; Nerve Fibers, Myelinated ; Neural networks ; Pan troglodytes ; Pan troglodytes - anatomy & histology ; Pan troglodytes - growth & development ; Prefrontal Cortex - anatomy & histology ; Prefrontal Cortex - growth & development ; Primates ; Social interactions ; Substantia alba</subject><ispartof>Current biology, 2011-08, Vol.21 (16), p.1397-1402</ispartof><rights>2011 Elsevier Ltd</rights><rights>Copyright © 2011 Elsevier Ltd. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c562t-1cc780b4dafe902eb7fcd18dfa0eb86796377ec1522b17f11eaaf1cfce1825f93</citedby><cites>FETCH-LOGICAL-c562t-1cc780b4dafe902eb7fcd18dfa0eb86796377ec1522b17f11eaaf1cfce1825f93</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0960982211007883$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21835623$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Sakai, Tomoko</creatorcontrib><creatorcontrib>Mikami, Akichika</creatorcontrib><creatorcontrib>Tomonaga, Masaki</creatorcontrib><creatorcontrib>Matsui, Mie</creatorcontrib><creatorcontrib>Suzuki, Juri</creatorcontrib><creatorcontrib>Hamada, Yuzuru</creatorcontrib><creatorcontrib>Tanaka, Masayuki</creatorcontrib><creatorcontrib>Miyabe-Nishiwaki, Takako</creatorcontrib><creatorcontrib>Makishima, Haruyuki</creatorcontrib><creatorcontrib>Nakatsukasa, Masato</creatorcontrib><creatorcontrib>Matsuzawa, Tetsuro</creatorcontrib><title>Differential Prefrontal White Matter Development in Chimpanzees and Humans</title><title>Current biology</title><addtitle>Curr Biol</addtitle><description>A comparison of developmental patterns of white matter (WM) within the prefrontal region between humans and nonhuman primates is key to understanding human brain evolution. WM mediates complex cognitive processes and has reciprocal connections with posterior processing regions [1, 2]. Although the developmental pattern of prefrontal WM in macaques differs markedly from that in humans [3], this has not been explored in our closest evolutionary relative, the chimpanzee. The present longitudinal study of magnetic resonance imaging scans demonstrated that the prefrontal WM volume in chimpanzees was immature and had not reached the adult value during prepuberty, as observed in humans but not in macaques. However, the rate of prefrontal WM volume increase during infancy was slower in chimpanzees than in humans. These results suggest that a less mature and more protracted elaboration of neuronal connections in the prefrontal portion of the developing brain existed in the last common ancestor of chimpanzees and humans, and that this served to enhance the impact of postnatal experiences on neuronal connectivity. Furthermore, the rapid development of the human prefrontal WM during infancy may help the development of complex social interactions, as well as the acquisition of experience-dependent knowledge and skills to shape neuronal connectivity.
► This is the first longitudinal investigation into brain development in chimpanzees ► Chimpanzees and humans share a protracted development of prefrontal white matter ► Only humans show a dramatic increase in prefrontal white matter during infancy ► This may help the development of human-specific cognition and neuronal connectivity</description><subject>adults</subject><subject>Animals</subject><subject>Biological Evolution</subject><subject>Brain</subject><subject>cognition</subject><subject>Cognitive ability</subject><subject>Development</subject><subject>Evolution</subject><subject>human development</subject><subject>Humans</subject><subject>infancy</subject><subject>Longitudinal Studies</subject><subject>Macaca</subject><subject>Macaca mulatta</subject><subject>Magnetic resonance imaging</subject><subject>Magnetic Resonance Imaging - methods</subject><subject>Nerve Fibers, Myelinated</subject><subject>Neural networks</subject><subject>Pan troglodytes</subject><subject>Pan troglodytes - anatomy & histology</subject><subject>Pan troglodytes - growth & development</subject><subject>Prefrontal Cortex - anatomy & histology</subject><subject>Prefrontal Cortex - growth & development</subject><subject>Primates</subject><subject>Social interactions</subject><subject>Substantia alba</subject><issn>0960-9822</issn><issn>1879-0445</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kE1vFDEMhqMK1G6X_gAuMLdymcHOfCQRp2pLKagVSFD1GGUyDs1qPrbJTCX660m1hWNP9uHxa_th7C1CgYDNx21hl7bggFiAKADVAVuhFCqHqqpfsRWoBnIlOT9ixzFuAZBL1RyyI46yrBterti3c-8cBRpnb_rsRyAXpnFO7e2dnym7NvNMITunB-qn3ZCwzI_Z5s4POzM-EsXMjF12uQxmjG_Ya2f6SCfPdc1uLj7_2lzmV9-_fN2cXeU2rZxztFZIaKvOOFLAqRXOdig7Z4Ba2QjVlEKQxZrzFoVDJGMcWmcJJa-dKtfsdJ-7C9P9QnHWg4-W-t6MNC1RS1nJSjSiTuSHF0kEVVaVQCwTinvUhinGpEHvgh9M-JMg_SRbb3WSrZ9kaxA6yU4z757jl3ag7v_EP7sJeL8HnJm0-R181Dc_U0INAKXk6dM1-7QnKAl78BR0tJ5GS50PZGfdTf6FA_4CWlOY7A</recordid><startdate>20110823</startdate><enddate>20110823</enddate><creator>Sakai, Tomoko</creator><creator>Mikami, Akichika</creator><creator>Tomonaga, Masaki</creator><creator>Matsui, Mie</creator><creator>Suzuki, Juri</creator><creator>Hamada, Yuzuru</creator><creator>Tanaka, Masayuki</creator><creator>Miyabe-Nishiwaki, Takako</creator><creator>Makishima, Haruyuki</creator><creator>Nakatsukasa, Masato</creator><creator>Matsuzawa, Tetsuro</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</scope><scope>FBQ</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7TK</scope><scope>7X8</scope></search><sort><creationdate>20110823</creationdate><title>Differential Prefrontal White Matter Development in Chimpanzees and Humans</title><author>Sakai, Tomoko ; Mikami, Akichika ; Tomonaga, Masaki ; Matsui, Mie ; Suzuki, Juri ; Hamada, Yuzuru ; Tanaka, Masayuki ; Miyabe-Nishiwaki, Takako ; Makishima, Haruyuki ; Nakatsukasa, Masato ; Matsuzawa, Tetsuro</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c562t-1cc780b4dafe902eb7fcd18dfa0eb86796377ec1522b17f11eaaf1cfce1825f93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>adults</topic><topic>Animals</topic><topic>Biological Evolution</topic><topic>Brain</topic><topic>cognition</topic><topic>Cognitive ability</topic><topic>Development</topic><topic>Evolution</topic><topic>human development</topic><topic>Humans</topic><topic>infancy</topic><topic>Longitudinal Studies</topic><topic>Macaca</topic><topic>Macaca mulatta</topic><topic>Magnetic resonance imaging</topic><topic>Magnetic Resonance Imaging - methods</topic><topic>Nerve Fibers, Myelinated</topic><topic>Neural networks</topic><topic>Pan troglodytes</topic><topic>Pan troglodytes - anatomy & histology</topic><topic>Pan troglodytes - growth & development</topic><topic>Prefrontal Cortex - anatomy & histology</topic><topic>Prefrontal Cortex - growth & development</topic><topic>Primates</topic><topic>Social interactions</topic><topic>Substantia alba</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sakai, Tomoko</creatorcontrib><creatorcontrib>Mikami, Akichika</creatorcontrib><creatorcontrib>Tomonaga, Masaki</creatorcontrib><creatorcontrib>Matsui, Mie</creatorcontrib><creatorcontrib>Suzuki, Juri</creatorcontrib><creatorcontrib>Hamada, Yuzuru</creatorcontrib><creatorcontrib>Tanaka, Masayuki</creatorcontrib><creatorcontrib>Miyabe-Nishiwaki, Takako</creatorcontrib><creatorcontrib>Makishima, Haruyuki</creatorcontrib><creatorcontrib>Nakatsukasa, Masato</creatorcontrib><creatorcontrib>Matsuzawa, Tetsuro</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>AGRIS</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Current biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sakai, Tomoko</au><au>Mikami, Akichika</au><au>Tomonaga, Masaki</au><au>Matsui, Mie</au><au>Suzuki, Juri</au><au>Hamada, Yuzuru</au><au>Tanaka, Masayuki</au><au>Miyabe-Nishiwaki, Takako</au><au>Makishima, Haruyuki</au><au>Nakatsukasa, Masato</au><au>Matsuzawa, Tetsuro</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Differential Prefrontal White Matter Development in Chimpanzees and Humans</atitle><jtitle>Current biology</jtitle><addtitle>Curr Biol</addtitle><date>2011-08-23</date><risdate>2011</risdate><volume>21</volume><issue>16</issue><spage>1397</spage><epage>1402</epage><pages>1397-1402</pages><issn>0960-9822</issn><eissn>1879-0445</eissn><abstract>A comparison of developmental patterns of white matter (WM) within the prefrontal region between humans and nonhuman primates is key to understanding human brain evolution. WM mediates complex cognitive processes and has reciprocal connections with posterior processing regions [1, 2]. Although the developmental pattern of prefrontal WM in macaques differs markedly from that in humans [3], this has not been explored in our closest evolutionary relative, the chimpanzee. The present longitudinal study of magnetic resonance imaging scans demonstrated that the prefrontal WM volume in chimpanzees was immature and had not reached the adult value during prepuberty, as observed in humans but not in macaques. However, the rate of prefrontal WM volume increase during infancy was slower in chimpanzees than in humans. These results suggest that a less mature and more protracted elaboration of neuronal connections in the prefrontal portion of the developing brain existed in the last common ancestor of chimpanzees and humans, and that this served to enhance the impact of postnatal experiences on neuronal connectivity. Furthermore, the rapid development of the human prefrontal WM during infancy may help the development of complex social interactions, as well as the acquisition of experience-dependent knowledge and skills to shape neuronal connectivity.
► This is the first longitudinal investigation into brain development in chimpanzees ► Chimpanzees and humans share a protracted development of prefrontal white matter ► Only humans show a dramatic increase in prefrontal white matter during infancy ► This may help the development of human-specific cognition and neuronal connectivity</abstract><cop>England</cop><pub>Elsevier Inc</pub><pmid>21835623</pmid><doi>10.1016/j.cub.2011.07.019</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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subjects | adults Animals Biological Evolution Brain cognition Cognitive ability Development Evolution human development Humans infancy Longitudinal Studies Macaca Macaca mulatta Magnetic resonance imaging Magnetic Resonance Imaging - methods Nerve Fibers, Myelinated Neural networks Pan troglodytes Pan troglodytes - anatomy & histology Pan troglodytes - growth & development Prefrontal Cortex - anatomy & histology Prefrontal Cortex - growth & development Primates Social interactions Substantia alba |
title | Differential Prefrontal White Matter Development in Chimpanzees and Humans |
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