Advanced Parkinson's disease effect on goal-directed and habitual processes involved in visuomotor associative learning
Identifieur interne : 000541 ( Pmc/Checkpoint ); précédent : 000540; suivant : 000542Advanced Parkinson's disease effect on goal-directed and habitual processes involved in visuomotor associative learning
Auteurs : Fadila Hadj-Bouziane [France] ; Isabelle Benatru [France] ; Andrea Brovelli [France] ; Hélène Klinger [France] ; Stéphane Thobois [France] ; Emmanuel Broussolle [France] ; Driss Boussaoud [France] ; Martine Meunier [France]Source :
- Frontiers in Human Neuroscience [ 1662-5161 ] ; 2013.
Abstract
The present behavioral study re-addresses the question of habit learning in Parkinson's disease (PD). Patients were early onset, non-demented, dopa-responsive, candidates for surgical treatment, similar to those we found earlier as suffering greater dopamine depletion in the putamen than in the caudate nucleus. The task was the same conditional associative learning task as that used previously in monkeys and healthy humans to unveil the striatum involvement in habit learning. Sixteen patients and 20 age- and education-matched healthy control subjects learned sets of 3 visuo-motor associations between complex patterns and joystick displacements during two testing sessions separated by a few hours. We distinguished errors preceding vs. following the first correct response to compare patients' performance during the earliest phase of learning dominated by goal-directed actions with that observed later on, when responses start to become habitual. The disease significantly retarded both learning phases, especially in patients under 60 years of age. However, only the late phase deficit was disease severity-dependent and persisted on the second testing session. These findings provide the first corroboration in Parkinson patients of two ideas well-established in the animal literature. The first is the idea that associating visual stimuli to motor acts is a form of habit learning that engages the striatum. It is confirmed here by the global impairment in visuo-motor learning induced by PD. The second idea is that goal-directed behaviors are predominantly caudate-dependent whereas habitual responses are primarily putamen-dependent. At the advanced PD stages tested here, dopamine depletion is greater in the putamen than in the caudate nucleus. Accordingly, the late phase of learning corresponding to the emergence of habitual responses was more vulnerable to the disease than the early phase dominated by goal-directed actions.
Url:
DOI: 10.3389/fnhum.2012.00351
PubMed: 23386815
PubMed Central: 3560419
Affiliations:
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<front><div type="abstract" xml:lang="en"><p>The present behavioral study re-addresses the question of habit learning in Parkinson's disease (PD). Patients were early onset, non-demented, dopa-responsive, candidates for surgical treatment, similar to those we found earlier as suffering greater dopamine depletion in the putamen than in the caudate nucleus. The task was the same conditional associative learning task as that used previously in monkeys and healthy humans to unveil the striatum involvement in habit learning. Sixteen patients and 20 age- and education-matched healthy control subjects learned sets of 3 visuo-motor associations between complex patterns and joystick displacements during two testing sessions separated by a few hours. We distinguished errors preceding vs. following the first correct response to compare patients' performance during the earliest phase of learning dominated by goal-directed actions with that observed later on, when responses start to become habitual. The disease significantly retarded both learning phases, especially in patients under 60 years of age. However, only the late phase deficit was disease severity-dependent and persisted on the second testing session. These findings provide the first corroboration in Parkinson patients of two ideas well-established in the animal literature. The first is the idea that associating visual stimuli to motor acts is a form of habit learning that engages the striatum. It is confirmed here by the global impairment in visuo-motor learning induced by PD. The second idea is that goal-directed behaviors are predominantly caudate-dependent whereas habitual responses are primarily putamen-dependent. At the advanced PD stages tested here, dopamine depletion is greater in the putamen than in the caudate nucleus. Accordingly, the late phase of learning corresponding to the emergence of habitual responses was more vulnerable to the disease than the early phase dominated by goal-directed actions.</p>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Front Hum Neurosci</journal-id>
<journal-id journal-id-type="iso-abbrev">Front Hum Neurosci</journal-id>
<journal-id journal-id-type="publisher-id">Front. Hum. Neurosci.</journal-id>
<journal-title-group><journal-title>Frontiers in Human Neuroscience</journal-title>
</journal-title-group>
<issn pub-type="epub">1662-5161</issn>
<publisher><publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">23386815</article-id>
<article-id pub-id-type="pmc">3560419</article-id>
<article-id pub-id-type="doi">10.3389/fnhum.2012.00351</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Neuroscience</subject>
<subj-group><subject>Original Research Article</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>Advanced Parkinson's disease effect on goal-directed and habitual processes involved in visuomotor associative learning</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Hadj-Bouziane</surname>
<given-names>Fadila</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
<xref ref-type="author-notes" rid="fn001"><sup>*</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Benatru</surname>
<given-names>Isabelle</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Brovelli</surname>
<given-names>Andrea</given-names>
</name>
<xref ref-type="aff" rid="aff5"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Klinger</surname>
<given-names>Hélène</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
<xref ref-type="aff" rid="aff6"><sup>6</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Thobois</surname>
<given-names>Stéphane</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
<xref ref-type="aff" rid="aff6"><sup>6</sup>
</xref>
<xref ref-type="aff" rid="aff7"><sup>7</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Broussolle</surname>
<given-names>Emmanuel</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
<xref ref-type="aff" rid="aff6"><sup>6</sup>
</xref>
<xref ref-type="aff" rid="aff7"><sup>7</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Boussaoud</surname>
<given-names>Driss</given-names>
</name>
<xref ref-type="aff" rid="aff8"><sup>8</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Meunier</surname>
<given-names>Martine</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1"><sup>1</sup>
<institution>INSERM U1028, Lyon Neuroscience Research Center, IMPACT Team</institution>
<country>Lyon, France</country>
</aff>
<aff id="aff2"><sup>2</sup>
<institution>CNRS UMR5292, Lyon Neuroscience Research Center, IMPACT Team</institution>
<country>Lyon, France</country>
</aff>
<aff id="aff3"><sup>3</sup>
<institution>University Lyon 1</institution>
<country>Lyon, France</country>
</aff>
<aff id="aff4"><sup>4</sup>
<institution>Service de Neurologie, CHU Poitiers</institution>
<country>Poitiers, France</country>
</aff>
<aff id="aff5"><sup>5</sup>
<institution>Institut de Neurosciences de la Timone (INT), UMR 7289 CNRS and Aix-Marseille Université, Campus Santé Timone</institution>
<country>Marseille, France</country>
</aff>
<aff id="aff6"><sup>6</sup>
<institution>Hospices Civils de Lyon, Hôpital Neurologique Pierre Wertheimer, Service de Neurologie C</institution>
<country>Lyon, France</country>
</aff>
<aff id="aff7"><sup>7</sup>
<institution>Centre de Neurosciences Cognitives, CNRS UMR 5229</institution>
<country>Bron, France</country>
</aff>
<aff id="aff8"><sup>8</sup>
<institution>Institut de Neuroscience des Systémes, UMR 1106, INSERM, Aix-Marseille Université</institution>
<country>Marseille, France</country>
</aff>
<author-notes><fn fn-type="edited-by"><p>Edited by: John J. Foxe, Albert Einstein College of Medicine, USA</p>
</fn>
<fn fn-type="edited-by"><p>Reviewed by: Rosalyn J. Moran, University College London, UK; Adam C. Snyder, University of Pittsburgh, USA</p>
</fn>
<corresp id="fn001">*Correspondence: Fadila Hadj-Bouziane, INSERM U1028, 16 Avenue du Doyen Lépine, 69500 Bron cedex, France. e-mail: <email xlink:type="simple">fadila.hadj-bouziane@inserm.fr</email>
</corresp>
</author-notes>
<pub-date pub-type="epub"><day>16</day>
<month>1</month>
<year>2013</year>
</pub-date>
<pub-date pub-type="collection"><year>2012</year>
</pub-date>
<volume>6</volume>
<elocation-id>351</elocation-id>
<history><date date-type="received"><day>02</day>
<month>8</month>
<year>2012</year>
</date>
<date date-type="accepted"><day>18</day>
<month>12</month>
<year>2012</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2013 Hadj-Bouziane, Benatru, Brovelli, Klinger, Thobois, Broussolle, Boussaoud and Meunier.</copyright-statement>
<copyright-year>2013</copyright-year>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/3.0/"><license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and subject to any copyright notices concerning any third-party graphics etc.</license-p>
</license>
</permissions>
<abstract><p>The present behavioral study re-addresses the question of habit learning in Parkinson's disease (PD). Patients were early onset, non-demented, dopa-responsive, candidates for surgical treatment, similar to those we found earlier as suffering greater dopamine depletion in the putamen than in the caudate nucleus. The task was the same conditional associative learning task as that used previously in monkeys and healthy humans to unveil the striatum involvement in habit learning. Sixteen patients and 20 age- and education-matched healthy control subjects learned sets of 3 visuo-motor associations between complex patterns and joystick displacements during two testing sessions separated by a few hours. We distinguished errors preceding vs. following the first correct response to compare patients' performance during the earliest phase of learning dominated by goal-directed actions with that observed later on, when responses start to become habitual. The disease significantly retarded both learning phases, especially in patients under 60 years of age. However, only the late phase deficit was disease severity-dependent and persisted on the second testing session. These findings provide the first corroboration in Parkinson patients of two ideas well-established in the animal literature. The first is the idea that associating visual stimuli to motor acts is a form of habit learning that engages the striatum. It is confirmed here by the global impairment in visuo-motor learning induced by PD. The second idea is that goal-directed behaviors are predominantly caudate-dependent whereas habitual responses are primarily putamen-dependent. At the advanced PD stages tested here, dopamine depletion is greater in the putamen than in the caudate nucleus. Accordingly, the late phase of learning corresponding to the emergence of habitual responses was more vulnerable to the disease than the early phase dominated by goal-directed actions.</p>
</abstract>
<kwd-group><kwd>feedback-based learning</kwd>
<kwd>striatum</kwd>
<kwd>habits</kwd>
<kwd>goal-directed actions</kwd>
<kwd>Parkinson's disease</kwd>
</kwd-group>
<counts><fig-count count="4"></fig-count>
<table-count count="3"></table-count>
<equation-count count="0"></equation-count>
<ref-count count="90"></ref-count>
<page-count count="11"></page-count>
<word-count count="9177"></word-count>
</counts>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>France</li>
</country>
</list>
<tree><country name="France"><noRegion><name sortKey="Hadj Bouziane, Fadila" sort="Hadj Bouziane, Fadila" uniqKey="Hadj Bouziane F" first="Fadila" last="Hadj-Bouziane">Fadila Hadj-Bouziane</name>
</noRegion>
<name sortKey="Benatru, Isabelle" sort="Benatru, Isabelle" uniqKey="Benatru I" first="Isabelle" last="Benatru">Isabelle Benatru</name>
<name sortKey="Boussaoud, Driss" sort="Boussaoud, Driss" uniqKey="Boussaoud D" first="Driss" last="Boussaoud">Driss Boussaoud</name>
<name sortKey="Broussolle, Emmanuel" sort="Broussolle, Emmanuel" uniqKey="Broussolle E" first="Emmanuel" last="Broussolle">Emmanuel Broussolle</name>
<name sortKey="Broussolle, Emmanuel" sort="Broussolle, Emmanuel" uniqKey="Broussolle E" first="Emmanuel" last="Broussolle">Emmanuel Broussolle</name>
<name sortKey="Broussolle, Emmanuel" sort="Broussolle, Emmanuel" uniqKey="Broussolle E" first="Emmanuel" last="Broussolle">Emmanuel Broussolle</name>
<name sortKey="Brovelli, Andrea" sort="Brovelli, Andrea" uniqKey="Brovelli A" first="Andrea" last="Brovelli">Andrea Brovelli</name>
<name sortKey="Hadj Bouziane, Fadila" sort="Hadj Bouziane, Fadila" uniqKey="Hadj Bouziane F" first="Fadila" last="Hadj-Bouziane">Fadila Hadj-Bouziane</name>
<name sortKey="Hadj Bouziane, Fadila" sort="Hadj Bouziane, Fadila" uniqKey="Hadj Bouziane F" first="Fadila" last="Hadj-Bouziane">Fadila Hadj-Bouziane</name>
<name sortKey="Klinger, Helene" sort="Klinger, Helene" uniqKey="Klinger H" first="Hélène" last="Klinger">Hélène Klinger</name>
<name sortKey="Klinger, Helene" sort="Klinger, Helene" uniqKey="Klinger H" first="Hélène" last="Klinger">Hélène Klinger</name>
<name sortKey="Meunier, Martine" sort="Meunier, Martine" uniqKey="Meunier M" first="Martine" last="Meunier">Martine Meunier</name>
<name sortKey="Meunier, Martine" sort="Meunier, Martine" uniqKey="Meunier M" first="Martine" last="Meunier">Martine Meunier</name>
<name sortKey="Meunier, Martine" sort="Meunier, Martine" uniqKey="Meunier M" first="Martine" last="Meunier">Martine Meunier</name>
<name sortKey="Thobois, Stephane" sort="Thobois, Stephane" uniqKey="Thobois S" first="Stéphane" last="Thobois">Stéphane Thobois</name>
<name sortKey="Thobois, Stephane" sort="Thobois, Stephane" uniqKey="Thobois S" first="Stéphane" last="Thobois">Stéphane Thobois</name>
<name sortKey="Thobois, Stephane" sort="Thobois, Stephane" uniqKey="Thobois S" first="Stéphane" last="Thobois">Stéphane Thobois</name>
</country>
</tree>
</affiliations>
</record>
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