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Neural representations of ethologically relevant hand/mouth synergies in the human precentral gyrus

Identifieur interne : 000A76 ( Pmc/Checkpoint ); précédent : 000A75; suivant : 000A77

Neural representations of ethologically relevant hand/mouth synergies in the human precentral gyrus

Auteurs : Michel Desmurget [France] ; Nathalie Richard [France] ; Sylvain Harquel [France] ; Pierre Baraduc [France] ; Alexandru Szathmari [France] ; Carmine Mottolese [France] ; Angela Sirigu [France]

Source :

RBID : PMC:3992683

Abstract

Significance

The motor repertoire of infants is narrow. Yet newborns can accurately bring their hands toward their mouth for self-feeding, thumb-sucking, or perioral exploration, thus showing fine coordinated movement synergies between the hand and mouth. Here, we show that these gestures of high ethological value are selectively encoded in the human brain and represented as integrated primitives within the precentral gyrus, a key region for sensorimotor processing. These findings have major implications for our understanding of the organization and phylogenesis of motor functions in primates.


Url:
DOI: 10.1073/pnas.1321909111
PubMed: 24706796
PubMed Central: 3992683


Affiliations:


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PMC:3992683

Le document en format XML

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<title>Significance</title>
<p>The motor repertoire of infants is narrow. Yet newborns can accurately bring their hands toward their mouth for self-feeding, thumb-sucking, or perioral exploration, thus showing fine coordinated movement synergies between the hand and mouth. Here, we show that these gestures of high ethological value are selectively encoded in the human brain and represented as integrated primitives within the precentral gyrus, a key region for sensorimotor processing. These findings have major implications for our understanding of the organization and phylogenesis of motor functions in primates.</p>
</div>
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<journal-id journal-id-type="iso-abbrev">Proc. Natl. Acad. Sci. U.S.A</journal-id>
<journal-id journal-id-type="hwp">pnas</journal-id>
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<article-title>Neural representations of ethologically relevant hand/mouth synergies in the human precentral gyrus</article-title>
<alt-title alt-title-type="short">Merged hand/mouth neural representations in humans</alt-title>
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<name>
<surname>Desmurget</surname>
<given-names>Michel</given-names>
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<sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
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</contrib>
<contrib contrib-type="author">
<name>
<surname>Richard</surname>
<given-names>Nathalie</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Harquel</surname>
<given-names>Sylvain</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
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<contrib contrib-type="author">
<name>
<surname>Baraduc</surname>
<given-names>Pierre</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Szathmari</surname>
<given-names>Alexandru</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff3">
<sup>c</sup>
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<contrib contrib-type="author">
<name>
<surname>Mottolese</surname>
<given-names>Carmine</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff3">
<sup>c</sup>
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<surname>Sirigu</surname>
<given-names>Angela</given-names>
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<sup>a</sup>
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<sup>a</sup>
Centre de Neuroscience Cognitive,
<institution>Centre National de la Recherche Scientifique/Unité Mixte de Recherche 5229</institution>
, 69500 Bron,
<country>France</country>
;</aff>
<aff id="aff2">
<sup>b</sup>
<institution>Université Claude Bernard Lyon 1</institution>
, 69100 Villeurbanne,
<country>France</country>
; and</aff>
<aff id="aff3">
<sup>c</sup>
Department of Pediatric Neurosurgery,
<institution>Neurological Hospital Pierre Wertheimer</institution>
, 69500 Bron,
<country>France</country>
</aff>
</contrib-group>
<author-notes>
<corresp id="cor1">
<sup>1</sup>
To whom correspondence should be addressed. E-mail:
<email>sirigu@isc.cnrs.fr</email>
.</corresp>
<fn fn-type="edited-by">
<p>Edited by Jon H. Kaas, Vanderbilt University, Nashville, TN, and approved March 6, 2014 (received for review November 22, 2013)</p>
</fn>
<fn fn-type="con">
<p>Author contributions: M.D. and A. Sirigu designed research; M.D., S.H., A. Szathmari, C.M., and A. Sirigu performed research; M.D., N.R., S.H., P.B., and A. Sirigu analyzed data; and M.D., P.B., C.M., and A. Sirigu wrote the paper.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub">
<day>15</day>
<month>4</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="epub">
<day>31</day>
<month>3</month>
<year>2014</year>
</pub-date>
<volume>111</volume>
<issue>15</issue>
<fpage>5718</fpage>
<lpage>5722</lpage>
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<abstract abstract-type="executive-summary">
<title>Significance</title>
<p>The motor repertoire of infants is narrow. Yet newborns can accurately bring their hands toward their mouth for self-feeding, thumb-sucking, or perioral exploration, thus showing fine coordinated movement synergies between the hand and mouth. Here, we show that these gestures of high ethological value are selectively encoded in the human brain and represented as integrated primitives within the precentral gyrus, a key region for sensorimotor processing. These findings have major implications for our understanding of the organization and phylogenesis of motor functions in primates.</p>
</abstract>
<abstract>
<p>Complex motor responses are often thought to result from the combination of elemental movements represented at different neural sites. However, in monkeys, evidence indicates that some behaviors with critical ethological value, such as self-feeding, are represented as motor primitives in the precentral gyrus (PrG). In humans, such primitives have not yet been described. This could reflect well-known interspecies differences in the organization of sensorimotor regions (including PrG) or the difficulty of identifying complex neural representations in peroperative settings. To settle this alternative, we focused on the neural bases of hand/mouth synergies, a prominent example of human behavior with high ethological value. By recording motor- and somatosensory-evoked potentials in the PrG of patients undergoing brain surgery (2–60 y), we show that two complex nested neural representations can mediate hand/mouth actions within this structure: (
<italic>i</italic>
) a motor representation, resembling self-feeding, where electrical stimulation causes the closing hand to approach the opening mouth, and (
<italic>ii</italic>
) a motor–sensory representation, likely associated with perioral exploration, where cross-signal integration is accomplished at a cortical site that generates hand/arm actions while receiving mouth sensory inputs. The first finding extends to humans’ previous observations in monkeys. The second provides evidence that complex neural representations also exist for perioral exploration, a finely tuned skill requiring the combination of motor and sensory signals within a common control loop. These representations likely underlie the ability of human children and newborns to accurately produce coordinated hand/mouth movements, in an otherwise general context of motor immaturity.</p>
</abstract>
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<name sortKey="Desmurget, Michel" sort="Desmurget, Michel" uniqKey="Desmurget M" first="Michel" last="Desmurget">Michel Desmurget</name>
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<name sortKey="Baraduc, Pierre" sort="Baraduc, Pierre" uniqKey="Baraduc P" first="Pierre" last="Baraduc">Pierre Baraduc</name>
<name sortKey="Baraduc, Pierre" sort="Baraduc, Pierre" uniqKey="Baraduc P" first="Pierre" last="Baraduc">Pierre Baraduc</name>
<name sortKey="Desmurget, Michel" sort="Desmurget, Michel" uniqKey="Desmurget M" first="Michel" last="Desmurget">Michel Desmurget</name>
<name sortKey="Harquel, Sylvain" sort="Harquel, Sylvain" uniqKey="Harquel S" first="Sylvain" last="Harquel">Sylvain Harquel</name>
<name sortKey="Harquel, Sylvain" sort="Harquel, Sylvain" uniqKey="Harquel S" first="Sylvain" last="Harquel">Sylvain Harquel</name>
<name sortKey="Mottolese, Carmine" sort="Mottolese, Carmine" uniqKey="Mottolese C" first="Carmine" last="Mottolese">Carmine Mottolese</name>
<name sortKey="Mottolese, Carmine" sort="Mottolese, Carmine" uniqKey="Mottolese C" first="Carmine" last="Mottolese">Carmine Mottolese</name>
<name sortKey="Richard, Nathalie" sort="Richard, Nathalie" uniqKey="Richard N" first="Nathalie" last="Richard">Nathalie Richard</name>
<name sortKey="Richard, Nathalie" sort="Richard, Nathalie" uniqKey="Richard N" first="Nathalie" last="Richard">Nathalie Richard</name>
<name sortKey="Sirigu, Angela" sort="Sirigu, Angela" uniqKey="Sirigu A" first="Angela" last="Sirigu">Angela Sirigu</name>
<name sortKey="Sirigu, Angela" sort="Sirigu, Angela" uniqKey="Sirigu A" first="Angela" last="Sirigu">Angela Sirigu</name>
<name sortKey="Szathmari, Alexandru" sort="Szathmari, Alexandru" uniqKey="Szathmari A" first="Alexandru" last="Szathmari">Alexandru Szathmari</name>
<name sortKey="Szathmari, Alexandru" sort="Szathmari, Alexandru" uniqKey="Szathmari A" first="Alexandru" last="Szathmari">Alexandru Szathmari</name>
</country>
</tree>
</affiliations>
</record>

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