Unilateral Lesion of Dopamine Neurons Induces Grooming Asymmetry in the Mouse
Identifieur interne : 000085 ( Pmc/Curation ); précédent : 000084; suivant : 000086Unilateral Lesion of Dopamine Neurons Induces Grooming Asymmetry in the Mouse
Auteurs : Assunta Pelosi [France] ; Jean-Antoine Girault [France] ; Denis Hervé [France]Source :
- PLoS ONE [ 1932-6203 ] ; 2015.
Abstract
Grooming behaviour is the most common innate behaviour in animals. In rodents, it consists of sequences of movements organized in four phases, executed symmetrically on both sides of the animal and creating a syntactic chain of behavioural events. The grooming syntax can be altered by stress and novelty, as well as by several mutations and brain lesions. Grooming behaviour is known to be affected by alterations of the dopamine system, including dopamine receptor modulation, dopamine alteration in genetically modified animals, and after brain lesion. While a lot is known about the initiation and syntactic modifications of this refined sequence of movements, effects of unilateral lesion of dopamine neurons are unclear particularly regarding the symmetry of syntactic chains. In the present work we studied grooming in mice unilaterally lesioned in the medial forebrain bundle by 6-hydroxydopamine. We found a reduction in completion of grooming bouts, associated with reduction in number of transitions between grooming phases. The data also revealed the development of asymmetry in grooming behaviour, with reduced tendency to groom the contralateral side to the lesion. Symmetry was recovered following treatment with L-DOPA. Thus, the present work shows that unilateral lesion of dopamine neurons reduces self-grooming behaviour by affecting duration and numbers of events. It produces premature discontinuation of grooming chains but the sequence syntax remains correct. This deficient grooming could be considered as an intrinsic symptom of Parkinson’s disease in animal models and could present some similarities with abnormalities of motor movement sequencing seen in patients. Our study also suggests grooming analysis as an additional method to screen parkinsonism in animal models.
Url:
DOI: 10.1371/journal.pone.0137185
PubMed: 26397369
PubMed Central: 4580614
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<front><div type="abstract" xml:lang="en"><p>Grooming behaviour is the most common innate behaviour in animals. In rodents, it consists of sequences of movements organized in four phases, executed symmetrically on both sides of the animal and creating a syntactic chain of behavioural events. The grooming syntax can be altered by stress and novelty, as well as by several mutations and brain lesions. Grooming behaviour is known to be affected by alterations of the dopamine system, including dopamine receptor modulation, dopamine alteration in genetically modified animals, and after brain lesion. While a lot is known about the initiation and syntactic modifications of this refined sequence of movements, effects of unilateral lesion of dopamine neurons are unclear particularly regarding the symmetry of syntactic chains. In the present work we studied grooming in mice unilaterally lesioned in the medial forebrain bundle by 6-hydroxydopamine. We found a reduction in completion of grooming bouts, associated with reduction in number of transitions between grooming phases. The data also revealed the development of asymmetry in grooming behaviour, with reduced tendency to groom the contralateral side to the lesion. Symmetry was recovered following treatment with L-DOPA. Thus, the present work shows that unilateral lesion of dopamine neurons reduces self-grooming behaviour by affecting duration and numbers of events. It produces premature discontinuation of grooming chains but the sequence syntax remains correct. This deficient grooming could be considered as an intrinsic symptom of Parkinson’s disease in animal models and could present some similarities with abnormalities of motor movement sequencing seen in patients. Our study also suggests grooming analysis as an additional method to screen parkinsonism in animal models.</p>
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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id>
<journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">plosone</journal-id>
<journal-title-group><journal-title>PLoS ONE</journal-title>
</journal-title-group>
<issn pub-type="epub">1932-6203</issn>
<publisher><publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, CA USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">26397369</article-id>
<article-id pub-id-type="pmc">4580614</article-id>
<article-id pub-id-type="doi">10.1371/journal.pone.0137185</article-id>
<article-id pub-id-type="publisher-id">PONE-D-15-23553</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Unilateral Lesion of Dopamine Neurons Induces Grooming Asymmetry in the Mouse</article-title>
<alt-title alt-title-type="running-head">Grooming Asymmetry after Unilateral Lesion</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Pelosi</surname>
<given-names>Assunta</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff003"><sup>3</sup>
</xref>
<xref rid="cor001" ref-type="corresp">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Girault</surname>
<given-names>Jean-Antoine</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff003"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hervé</surname>
<given-names>Denis</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff003"><sup>3</sup>
</xref>
<xref rid="cor001" ref-type="corresp">*</xref>
</contrib>
</contrib-group>
<aff id="aff001"><label>1</label>
<addr-line>Inserm UMR-S 839, 75005, Paris, France</addr-line>
</aff>
<aff id="aff002"><label>2</label>
<addr-line>Institut du Fer à Moulin, 75005, Paris, France</addr-line>
</aff>
<aff id="aff003"><label>3</label>
<addr-line>Sorbonne Universités, Université Pierre et Marie Curie (UPMC, Paris-6), Paris, France</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Aumann</surname>
<given-names>Tim Douglas</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1"><addr-line>Florey Institute of Neuroscience & Mental Health, AUSTRALIA</addr-line>
</aff>
<author-notes><fn fn-type="conflict" id="coi001"><p><bold>Competing Interests: </bold>
The authors have declared that no competing interests exist.</p>
</fn>
<fn fn-type="con" id="contrib001"><p>Conceived and designed the experiments: AP DH JAG. Performed the experiments: AP. Analyzed the data: AP. Wrote the paper: AP DH JAG.</p>
</fn>
<corresp id="cor001">* E-mail: <email>assunta.pelosi@inserm.fr</email>
(AP); <email>denis.herve@inserm.fr</email>
(DH)</corresp>
</author-notes>
<pub-date pub-type="epub"><day>23</day>
<month>9</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="collection"><year>2015</year>
</pub-date>
<volume>10</volume>
<issue>9</issue>
<elocation-id>e0137185</elocation-id>
<history><date date-type="received"><day>30</day>
<month>5</month>
<year>2015</year>
</date>
<date date-type="accepted"><day>13</day>
<month>8</month>
<year>2015</year>
</date>
</history>
<permissions><copyright-year>2015</copyright-year>
<copyright-holder>Pelosi et al</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>
, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:type="simple" xlink:href="pone.0137185.pdf"></self-uri>
<abstract><p>Grooming behaviour is the most common innate behaviour in animals. In rodents, it consists of sequences of movements organized in four phases, executed symmetrically on both sides of the animal and creating a syntactic chain of behavioural events. The grooming syntax can be altered by stress and novelty, as well as by several mutations and brain lesions. Grooming behaviour is known to be affected by alterations of the dopamine system, including dopamine receptor modulation, dopamine alteration in genetically modified animals, and after brain lesion. While a lot is known about the initiation and syntactic modifications of this refined sequence of movements, effects of unilateral lesion of dopamine neurons are unclear particularly regarding the symmetry of syntactic chains. In the present work we studied grooming in mice unilaterally lesioned in the medial forebrain bundle by 6-hydroxydopamine. We found a reduction in completion of grooming bouts, associated with reduction in number of transitions between grooming phases. The data also revealed the development of asymmetry in grooming behaviour, with reduced tendency to groom the contralateral side to the lesion. Symmetry was recovered following treatment with L-DOPA. Thus, the present work shows that unilateral lesion of dopamine neurons reduces self-grooming behaviour by affecting duration and numbers of events. It produces premature discontinuation of grooming chains but the sequence syntax remains correct. This deficient grooming could be considered as an intrinsic symptom of Parkinson’s disease in animal models and could present some similarities with abnormalities of motor movement sequencing seen in patients. Our study also suggests grooming analysis as an additional method to screen parkinsonism in animal models.</p>
</abstract>
<funding-group><funding-statement>Funding was provided by Inserm (<ext-link ext-link-type="uri" xlink:href="http://www.inserm.fr">http://www.inserm.fr</ext-link>
), the Université Pierre et Marie Curie (UPMC, Paris 6) (UPMC, <ext-link ext-link-type="uri" xlink:href="http://www.upmc.fr">http://www.upmc.fr</ext-link>
), the Agence Nationale de la Recherche (<ext-link ext-link-type="uri" xlink:href="http://www.agence-nationale-recherche.fr">http://www.agence-nationale-recherche.fr</ext-link>
) (ANR09-MNPS-014) and the European Research Council (ERC, <ext-link ext-link-type="uri" xlink:href="http://erc.europa.eu">http://erc.europa.eu</ext-link>
) advanced investigator grant to JA Girault. Equipment at the IFM was also supported by DIM NeRF from Région Ile-de-France and by the FRC/Rotary “Espoir en tête”. The Girault & Hervé group is affiliated with the Paris School of Neuroscience (ENP) and the Bio-Psy laboratory of excellence.</funding-statement>
</funding-group>
<counts><fig-count count="5"></fig-count>
<table-count count="0"></table-count>
<page-count count="15"></page-count>
</counts>
<custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name>
<meta-value>All excel files and videos examples are available from the Harvard Dataverse (<ext-link ext-link-type="uri" xlink:href="http://dx.doi.org/10.7910/DVN/1UK7K1">http://dx.doi.org/10.7910/DVN/1UK7K1</ext-link>
).</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
<notes><title>Data Availability</title>
<p>All excel files and videos examples are available from the Harvard Dataverse (<ext-link ext-link-type="uri" xlink:href="http://dx.doi.org/10.7910/DVN/1UK7K1">http://dx.doi.org/10.7910/DVN/1UK7K1</ext-link>
).</p>
</notes>
</front>
</pmc>
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