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Behavioural and neural basis of anomalous motor learning in children with autism

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Behavioural and neural basis of anomalous motor learning in children with autism

Auteurs : Mollie K. Marko [États-Unis] ; Deana Crocetti [États-Unis] ; Thomas Hulst [Pays-Bas] ; Opher Donchin [Israël] ; Reza Shadmehr [États-Unis] ; Stewart H. Mostofsky [États-Unis]

Source :

Brain [ 0006-8950 ] ; 2015.

RBID : PMC:4339776

Abstract

Marko et al. show that during motor learning, children with autism are more sensitive to proprioceptive error and less sensitive to visual error than controls. These altered patterns of error sensitivity predict the volume of the anterior cerebellum—which supports this learning—and may affect the development of motor control.

Url:

http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4339776

DOI: 10.1093/brain/awu394
PubMed: 25609685
PubMed Central: 4339776

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PMC:4339776

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<author><name sortKey="Marko, Mollie K" sort="Marko, Mollie K" uniqKey="Marko M" first="Mollie K." last="Marko">Mollie K. Marko</name>
<affiliation wicri:level="1"><nlm:aff id="awu394-AFF1">1 Laboratory for Computational Motor Control, Department of Biomedical Engineering, Johns Hopkins School of Medicine, Baltimore, Maryland, USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>1 Laboratory for Computational Motor Control, Department of Biomedical Engineering, Johns Hopkins School of Medicine, Baltimore, Maryland</wicri:regionArea>
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<author><name sortKey="Crocetti, Deana" sort="Crocetti, Deana" uniqKey="Crocetti D" first="Deana" last="Crocetti">Deana Crocetti</name>
<affiliation wicri:level="1"><nlm:aff id="awu394-AFF2">2 Centre for Neurodevelopmental and Imaging Research, Kennedy Krieger Institute, Baltimore, Maryland, USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
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<author><name sortKey="Hulst, Thomas" sort="Hulst, Thomas" uniqKey="Hulst T" first="Thomas" last="Hulst">Thomas Hulst</name>
<affiliation wicri:level="1"><nlm:aff id="awu394-AFF3">3 Department of Neuroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
<country xml:lang="fr">Pays-Bas</country>
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<author><name sortKey="Donchin, Opher" sort="Donchin, Opher" uniqKey="Donchin O" first="Opher" last="Donchin">Opher Donchin</name>
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<author><name sortKey="Mostofsky, Stewart H" sort="Mostofsky, Stewart H" uniqKey="Mostofsky S" first="Stewart H." last="Mostofsky">Stewart H. Mostofsky</name>
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<author><name sortKey="Crocetti, Deana" sort="Crocetti, Deana" uniqKey="Crocetti D" first="Deana" last="Crocetti">Deana Crocetti</name>
<affiliation wicri:level="1"><nlm:aff id="awu394-AFF2">2 Centre for Neurodevelopmental and Imaging Research, Kennedy Krieger Institute, Baltimore, Maryland, USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
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<author><name sortKey="Hulst, Thomas" sort="Hulst, Thomas" uniqKey="Hulst T" first="Thomas" last="Hulst">Thomas Hulst</name>
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<country xml:lang="fr">Pays-Bas</country>
<wicri:regionArea>3 Department of Neuroscience, Erasmus MC, Rotterdam</wicri:regionArea>
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<author><name sortKey="Donchin, Opher" sort="Donchin, Opher" uniqKey="Donchin O" first="Opher" last="Donchin">Opher Donchin</name>
<affiliation wicri:level="1"><nlm:aff id="awu394-AFF4">4 The Motor Learning Laboratory, Department of Biomedical Engineering, Ben Gurion University of the Negev, Beersheba, Israel</nlm:aff>
<country xml:lang="fr">Israël</country>
<wicri:regionArea>4 The Motor Learning Laboratory, Department of Biomedical Engineering, Ben Gurion University of the Negev, Beersheba</wicri:regionArea>
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<author><name sortKey="Shadmehr, Reza" sort="Shadmehr, Reza" uniqKey="Shadmehr R" first="Reza" last="Shadmehr">Reza Shadmehr</name>
<affiliation wicri:level="1"><nlm:aff id="awu394-AFF1">1 Laboratory for Computational Motor Control, Department of Biomedical Engineering, Johns Hopkins School of Medicine, Baltimore, Maryland, USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>1 Laboratory for Computational Motor Control, Department of Biomedical Engineering, Johns Hopkins School of Medicine, Baltimore, Maryland</wicri:regionArea>
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<author><name sortKey="Mostofsky, Stewart H" sort="Mostofsky, Stewart H" uniqKey="Mostofsky S" first="Stewart H." last="Mostofsky">Stewart H. Mostofsky</name>
<affiliation wicri:level="1"><nlm:aff id="awu394-AFF2">2 Centre for Neurodevelopmental and Imaging Research, Kennedy Krieger Institute, Baltimore, Maryland, USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>2 Centre for Neurodevelopmental and Imaging Research, Kennedy Krieger Institute, Baltimore, Maryland</wicri:regionArea>
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<affiliation wicri:level="1"><nlm:aff id="awu394-AFF5">5 Departments of Neurology and Psychiatry and Behavioural Sciences, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>5 Departments of Neurology and Psychiatry and Behavioural Sciences, Johns Hopkins University School of Medicine, Baltimore, Maryland</wicri:regionArea>
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<series><title level="j">Brain</title>
<idno type="ISSN">0006-8950</idno>
<idno type="eISSN">1460-2156</idno>
<imprint><date when="2015">2015</date>
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<front><div type="abstract" xml:lang="en"><p>Marko <italic>et al.</italic>
 show that during motor learning, children with autism are more sensitive to proprioceptive error and less sensitive to visual error than controls. These altered patterns of error sensitivity predict the volume of the anterior cerebellum—which supports this learning—and may affect the development of motor control.</p>
</div>
</front>
</TEI>
<pmc article-type="research-article"><pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
  <front><journal-meta><journal-id journal-id-type="nlm-ta">Brain</journal-id>
<journal-id journal-id-type="iso-abbrev">Brain</journal-id>
<journal-id journal-id-type="publisher-id">brainj</journal-id>
<journal-id journal-id-type="hwp">brain</journal-id>
<journal-title-group><journal-title>Brain</journal-title>
</journal-title-group>
<issn pub-type="ppub">0006-8950</issn>
<issn pub-type="epub">1460-2156</issn>
<publisher><publisher-name>Oxford University Press</publisher-name>
</publisher>
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<article-meta><article-id pub-id-type="pmid">25609685</article-id>
<article-id pub-id-type="pmc">4339776</article-id>
<article-id pub-id-type="doi">10.1093/brain/awu394</article-id>
<article-id pub-id-type="publisher-id">awu394</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Original Articles</subject>
</subj-group>
</article-categories>
<title-group><article-title>Behavioural and neural basis of anomalous motor learning in children with autism</article-title>
</title-group>
<contrib-group><contrib contrib-type="author" corresp="yes"><name><surname>Marko</surname>
<given-names>Mollie K.</given-names>
</name>
<xref ref-type="aff" rid="awu394-AFF1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Crocetti</surname>
<given-names>Deana</given-names>
</name>
<xref ref-type="aff" rid="awu394-AFF2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hulst</surname>
<given-names>Thomas</given-names>
</name>
<xref ref-type="aff" rid="awu394-AFF3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Donchin</surname>
<given-names>Opher</given-names>
</name>
<xref ref-type="aff" rid="awu394-AFF4"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Shadmehr</surname>
<given-names>Reza</given-names>
</name>
<xref ref-type="aff" rid="awu394-AFF1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Mostofsky</surname>
<given-names>Stewart H.</given-names>
</name>
<xref ref-type="aff" rid="awu394-AFF2"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="awu394-AFF5"><sup>5</sup>
</xref>
</contrib>
<aff id="awu394-AFF1">1 Laboratory for Computational Motor Control, Department of Biomedical Engineering, Johns Hopkins School of Medicine, Baltimore, Maryland, USA</aff>
<aff id="awu394-AFF2">2 Centre for Neurodevelopmental and Imaging Research, Kennedy Krieger Institute, Baltimore, Maryland, USA</aff>
<aff id="awu394-AFF3">3 Department of Neuroscience, Erasmus MC, Rotterdam, The Netherlands</aff>
<aff id="awu394-AFF4">4 The Motor Learning Laboratory, Department of Biomedical Engineering, Ben Gurion University of the Negev, Beersheba, Israel</aff>
<aff id="awu394-AFF5">5 Departments of Neurology and Psychiatry and Behavioural Sciences, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA</aff>
</contrib-group>
<author-notes><corresp>Correspondence to: Mollie Marko, 416 Traylor Building, 720 Rutland Ave, Johns Hopkins School of Medicine, Baltimore, MD 21205 USA. E-mail: <email>mkmarko@jhu.edu</email>
</corresp>
</author-notes>
<pub-date pub-type="ppub"><month>3</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="epub"><day>21</day>
<month>1</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>1</day>
<month>3</month>
<year>2016</year>
</pub-date>
<pmc-comment> PMC Release delay is 12 months and 
 						0 days and was based on the . </pmc-comment>
      <volume>138</volume>
<issue>3</issue>
<fpage>784</fpage>
<lpage>797</lpage>
<history><date date-type="received"><day>8</day>
<month>8</month>
<year>2014</year>
</date>
<date date-type="rev-recd"><day>9</day>
<month>10</month>
<year>2014</year>
</date>
<date date-type="accepted"><day>9</day>
<month>11</month>
<year>2014</year>
</date>
</history>
<permissions><copyright-statement>© The Author (2015). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved. For Permissions, please email: journals.permissions@oup.com</copyright-statement>
<copyright-year>2015</copyright-year>
</permissions>
<abstract abstract-type="precis"><p>Marko <italic>et al.</italic>
 show that during motor learning, children with autism are more sensitive to proprioceptive error and less sensitive to visual error than controls. These altered patterns of error sensitivity predict the volume of the anterior cerebellum—which supports this learning—and may affect the development of motor control.</p>
</abstract>
<abstract><p>Autism spectrum disorder is a developmental disorder characterized by deficits in social and communication skills and repetitive and stereotyped interests and behaviours. Although not part of the diagnostic criteria, individuals with autism experience a host of motor impairments, potentially due to abnormalities in how they learn motor control throughout development. Here, we used behavioural techniques to quantify motor learning in autism spectrum disorder, and structural brain imaging to investigate the neural basis of that learning in the cerebellum. Twenty children with autism spectrum disorder and 20 typically developing control subjects, aged 8–12, made reaching movements while holding the handle of a robotic manipulandum. In random trials the reach was perturbed, resulting in errors that were sensed through vision and proprioception. The brain learned from these errors and altered the motor commands on the subsequent reach. We measured learning from error as a function of the sensory modality of that error, and found that children with autism spectrum disorder outperformed typically developing children when learning from errors that were sensed through proprioception, but underperformed typically developing children when learning from errors that were sensed through vision. Previous work had shown that this learning depends on the integrity of a region in the anterior cerebellum. Here we found that the anterior cerebellum, extending into lobule VI, and parts of lobule VIII were smaller than normal in children with autism spectrum disorder, with a volume that was predicted by the pattern of learning from visual and proprioceptive errors. We suggest that the abnormal patterns of motor learning in children with autism spectrum disorder, showing an increased sensitivity to proprioceptive error and a decreased sensitivity to visual error, may be associated with abnormalities in the cerebellum.</p>
</abstract>
<kwd-group kwd-group-type="keywords"><kwd>error sensitivity</kwd>
<kwd>proprioception</kwd>
<kwd>motor learning</kwd>
<kwd>reaching</kwd>
<kwd>cerebellum</kwd>
<kwd>autism</kwd>
</kwd-group>
<counts><page-count count="14"></page-count>
</counts>
</article-meta>
</front>
</pmc>
</record>

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Behavioural and neural basis of anomalous motor learning in children with autism

Behavioural and neural basis of anomalous motor learning in children with autism

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Abstract

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