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Asymmetric right/left encoding of emotions in the human subthalamic nucleus

Identifieur interne : 001607 ( Ncbi/Merge ); précédent : 001606; suivant : 001608

Asymmetric right/left encoding of emotions in the human subthalamic nucleus

Auteurs : Renana Eitan [Israël] ; Reuben R. Shamir [Israël] ; Eduard Linetsky [Israël] ; Ovadya Rosenbluh [Israël] ; Shay Moshel [Israël] ; Tamir Ben-Hur [Israël] ; Hagai Bergman [Israël] ; Zvi Israel [Israël]

Source :

RBID : PMC:3810611

Abstract

Emotional processing is lateralized to the non-dominant brain hemisphere. However, there is no clear spatial model for lateralization of emotional domains in the basal ganglia. The subthalamic nucleus (STN), an input structure in the basal ganglia network, plays a major role in the pathophysiology of Parkinson's disease (PD). This role is probably not limited only to the motor deficits of PD, but may also span the emotional and cognitive deficits commonly observed in PD patients. Beta oscillations (12–30 Hz), the electrophysiological signature of PD, are restricted to the dorsolateral part of the STN that corresponds to the anatomically defined sensorimotor STN. The more medial, more anterior and more ventral parts of the STN are thought to correspond to the anatomically defined limbic and associative territories of the STN. Surprisingly, little is known about the electrophysiological properties of the non-motor domains of the STN, nor about electrophysiological differences between right and left STNs. In this study, microelectrodes were utilized to record the STN spontaneous spiking activity and responses to vocal non-verbal emotional stimuli during deep brain stimulation (DBS) surgeries in human PD patients. The oscillation properties of the STN neurons were used to map the dorsal oscillatory and the ventral non-oscillatory regions of the STN. Emotive auditory stimulation evoked activity in the ventral non-oscillatory region of the right STN. These responses were not observed in the left ventral STN or in the dorsal regions of either the right or left STN. Therefore, our results suggest that the ventral non-oscillatory regions are asymmetrically associated with non-motor functions, with the right ventral STN associated with emotional processing. These results suggest that DBS of the right ventral STN may be associated with beneficial or adverse emotional effects observed in PD patients and may relieve mental symptoms in other neurological and psychiatric diseases.


Url:
DOI: 10.3389/fnsys.2013.00069
PubMed: 24194703
PubMed Central: 3810611

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PMC:3810611

Le document en format XML

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<p>Emotional processing is lateralized to the non-dominant brain hemisphere. However, there is no clear spatial model for lateralization of emotional domains in the basal ganglia. The subthalamic nucleus (STN), an input structure in the basal ganglia network, plays a major role in the pathophysiology of Parkinson's disease (PD). This role is probably not limited only to the motor deficits of PD, but may also span the emotional and cognitive deficits commonly observed in PD patients. Beta oscillations (12–30 Hz), the electrophysiological signature of PD, are restricted to the dorsolateral part of the STN that corresponds to the anatomically defined sensorimotor STN. The more medial, more anterior and more ventral parts of the STN are thought to correspond to the anatomically defined limbic and associative territories of the STN. Surprisingly, little is known about the electrophysiological properties of the non-motor domains of the STN, nor about electrophysiological differences between right and left STNs. In this study, microelectrodes were utilized to record the STN spontaneous spiking activity and responses to vocal non-verbal emotional stimuli during deep brain stimulation (DBS) surgeries in human PD patients. The oscillation properties of the STN neurons were used to map the dorsal oscillatory and the ventral non-oscillatory regions of the STN. Emotive auditory stimulation evoked activity in the ventral non-oscillatory region of the right STN. These responses were not observed in the left ventral STN or in the dorsal regions of either the right or left STN. Therefore, our results suggest that the ventral non-oscillatory regions are asymmetrically associated with non-motor functions, with the right ventral STN associated with emotional processing. These results suggest that DBS of the right ventral STN may be associated with beneficial or adverse emotional effects observed in PD patients and may relieve mental symptoms in other neurological and psychiatric diseases.</p>
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</TEI>
<pmc article-type="research-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">Front Syst Neurosci</journal-id>
<journal-id journal-id-type="iso-abbrev">Front Syst Neurosci</journal-id>
<journal-id journal-id-type="publisher-id">Front. Syst. Neurosci.</journal-id>
<journal-title-group>
<journal-title>Frontiers in Systems Neuroscience</journal-title>
</journal-title-group>
<issn pub-type="epub">1662-5137</issn>
<publisher>
<publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">24194703</article-id>
<article-id pub-id-type="pmc">3810611</article-id>
<article-id pub-id-type="doi">10.3389/fnsys.2013.00069</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>Asymmetric right/left encoding of emotions in the human subthalamic nucleus</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Eitan</surname>
<given-names>Renana</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn003">
<sup></sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Shamir</surname>
<given-names>Reuben R.</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
<xref ref-type="aff" rid="aff4">
<sup>4</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
</xref>
<xref ref-type="author-notes" rid="fn003">
<sup></sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Linetsky</surname>
<given-names>Eduard</given-names>
</name>
<xref ref-type="aff" rid="aff5">
<sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Rosenbluh</surname>
<given-names>Ovadya</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Moshel</surname>
<given-names>Shay</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
<xref ref-type="aff" rid="aff4">
<sup>4</sup>
</xref>
<xref ref-type="aff" rid="aff6">
<sup>6</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Ben-Hur</surname>
<given-names>Tamir</given-names>
</name>
<xref ref-type="aff" rid="aff5">
<sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Bergman</surname>
<given-names>Hagai</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Israel</surname>
<given-names>Zvi</given-names>
</name>
<xref ref-type="aff" rid="aff4">
<sup>4</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1">
<sup>1</sup>
<institution>Department of Psychiatry, Hadassah-Hebrew University Medical Center</institution>
<country>Jerusalem, Israel</country>
</aff>
<aff id="aff2">
<sup>2</sup>
<institution>Department of Medical Neurobiology (Physiology), Institute of Medical Research – Israel-Canada, The Hebrew University-Hadassah Medical School</institution>
<country>Jerusalem, Israel</country>
</aff>
<aff id="aff3">
<sup>3</sup>
<institution>The Edmond and Lily Safra Center for Brain Research, The Hebrew University</institution>
<country>Jerusalem, Israel</country>
</aff>
<aff id="aff4">
<sup>4</sup>
<institution>Department of Neurosurgery, Center for Functional and Restorative Neurosurgery, Hadassah-Hebrew University Medical Center</institution>
<country>Jerusalem, Israel</country>
</aff>
<aff id="aff5">
<sup>5</sup>
<institution>Department of Neurology, Hadassah–Hebrew University Medical Center</institution>
<country>Jerusalem, Israel</country>
</aff>
<aff id="aff6">
<sup>6</sup>
<institution>The Jerusalem Mental Health Center, Kfar-Shaul Etanim</institution>
<country>Jerusalem, Israel</country>
</aff>
<author-notes>
<fn fn-type="edited-by">
<p>Edited by: Izhar Bar-Gad, Bar-Ilan University, Israel</p>
</fn>
<fn fn-type="edited-by">
<p>Reviewed by: Andrea A. Kühn, Charité, University-Medicine Berlin, Germany; Paul Krack, Grenoble Institute of Neuroscience - Inserm U.836-UJF-CEA-CHU, France</p>
</fn>
<corresp id="fn001">*Correspondence: Reuben R. Shamir, Department of Medical Neurobiology (Physiology) and Department of Neurosurgery, The Hebrew University-Hadassah Medical School, Ein-Karem Campus, PO Box 12272, 91120 Jerusalem, Israel e-mail:
<email xlink:type="simple">shamir.ruby@gmail.com</email>
</corresp>
<fn fn-type="other" id="fn002">
<p>This article was submitted to the journal Frontiers in Systems Neuroscience.</p>
</fn>
<fn fn-type="present-address" id="fn003">
<p>†These authors have contributed equally to this work.</p>
</fn>
</author-notes>
<pub-date pub-type="epub">
<day>29</day>
<month>10</month>
<year>2013</year>
</pub-date>
<pub-date pub-type="collection">
<year>2013</year>
</pub-date>
<volume>7</volume>
<elocation-id>69</elocation-id>
<history>
<date date-type="received">
<day>15</day>
<month>7</month>
<year>2013</year>
</date>
<date date-type="accepted">
<day>04</day>
<month>10</month>
<year>2013</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright © 2013 Eitan, Shamir, Linetsky, Rosenbluh, Moshel, Ben-Hur, Bergman and Israel.</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 (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</license-p>
</license>
</permissions>
<abstract>
<p>Emotional processing is lateralized to the non-dominant brain hemisphere. However, there is no clear spatial model for lateralization of emotional domains in the basal ganglia. The subthalamic nucleus (STN), an input structure in the basal ganglia network, plays a major role in the pathophysiology of Parkinson's disease (PD). This role is probably not limited only to the motor deficits of PD, but may also span the emotional and cognitive deficits commonly observed in PD patients. Beta oscillations (12–30 Hz), the electrophysiological signature of PD, are restricted to the dorsolateral part of the STN that corresponds to the anatomically defined sensorimotor STN. The more medial, more anterior and more ventral parts of the STN are thought to correspond to the anatomically defined limbic and associative territories of the STN. Surprisingly, little is known about the electrophysiological properties of the non-motor domains of the STN, nor about electrophysiological differences between right and left STNs. In this study, microelectrodes were utilized to record the STN spontaneous spiking activity and responses to vocal non-verbal emotional stimuli during deep brain stimulation (DBS) surgeries in human PD patients. The oscillation properties of the STN neurons were used to map the dorsal oscillatory and the ventral non-oscillatory regions of the STN. Emotive auditory stimulation evoked activity in the ventral non-oscillatory region of the right STN. These responses were not observed in the left ventral STN or in the dorsal regions of either the right or left STN. Therefore, our results suggest that the ventral non-oscillatory regions are asymmetrically associated with non-motor functions, with the right ventral STN associated with emotional processing. These results suggest that DBS of the right ventral STN may be associated with beneficial or adverse emotional effects observed in PD patients and may relieve mental symptoms in other neurological and psychiatric diseases.</p>
</abstract>
<kwd-group>
<kwd>Parkinson's disease</kwd>
<kwd>deep brain stimulation (DBS)</kwd>
<kwd>emotions</kwd>
<kwd>subthalamic nucleus</kwd>
<kwd>spikes</kwd>
</kwd-group>
<counts>
<fig-count count="6"></fig-count>
<table-count count="2"></table-count>
<equation-count count="0"></equation-count>
<ref-count count="73"></ref-count>
<page-count count="11"></page-count>
<word-count count="8503"></word-count>
</counts>
</article-meta>
</front>
</pmc>
<affiliations>
<list>
<country>
<li>Israël</li>
</country>
</list>
<tree>
<country name="Israël">
<noRegion>
<name sortKey="Eitan, Renana" sort="Eitan, Renana" uniqKey="Eitan R" first="Renana" last="Eitan">Renana Eitan</name>
</noRegion>
<name sortKey="Ben Hur, Tamir" sort="Ben Hur, Tamir" uniqKey="Ben Hur T" first="Tamir" last="Ben-Hur">Tamir Ben-Hur</name>
<name sortKey="Bergman, Hagai" sort="Bergman, Hagai" uniqKey="Bergman H" first="Hagai" last="Bergman">Hagai Bergman</name>
<name sortKey="Bergman, Hagai" sort="Bergman, Hagai" uniqKey="Bergman H" first="Hagai" last="Bergman">Hagai Bergman</name>
<name sortKey="Israel, Zvi" sort="Israel, Zvi" uniqKey="Israel Z" first="Zvi" last="Israel">Zvi Israel</name>
<name sortKey="Linetsky, Eduard" sort="Linetsky, Eduard" uniqKey="Linetsky E" first="Eduard" last="Linetsky">Eduard Linetsky</name>
<name sortKey="Moshel, Shay" sort="Moshel, Shay" uniqKey="Moshel S" first="Shay" last="Moshel">Shay Moshel</name>
<name sortKey="Moshel, Shay" sort="Moshel, Shay" uniqKey="Moshel S" first="Shay" last="Moshel">Shay Moshel</name>
<name sortKey="Moshel, Shay" sort="Moshel, Shay" uniqKey="Moshel S" first="Shay" last="Moshel">Shay Moshel</name>
<name sortKey="Moshel, Shay" sort="Moshel, Shay" uniqKey="Moshel S" first="Shay" last="Moshel">Shay Moshel</name>
<name sortKey="Rosenbluh, Ovadya" sort="Rosenbluh, Ovadya" uniqKey="Rosenbluh O" first="Ovadya" last="Rosenbluh">Ovadya Rosenbluh</name>
<name sortKey="Shamir, Reuben R" sort="Shamir, Reuben R" uniqKey="Shamir R" first="Reuben R." last="Shamir">Reuben R. Shamir</name>
<name sortKey="Shamir, Reuben R" sort="Shamir, Reuben R" uniqKey="Shamir R" first="Reuben R." last="Shamir">Reuben R. Shamir</name>
<name sortKey="Shamir, Reuben R" sort="Shamir, Reuben R" uniqKey="Shamir R" first="Reuben R." last="Shamir">Reuben R. Shamir</name>
</country>
</tree>
</affiliations>
</record>

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