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Processing of emotional information in the human subthalamic nucleus

Identifieur interne : 002253 ( Main/Corpus ); précédent : 002252; suivant : 002254

Processing of emotional information in the human subthalamic nucleus

Auteurs : Anne Buot ; Marie-Laure Welter ; Carine Karachi ; Jean-Baptiste Pochon ; Eric Bardinet ; Jérôme Yelnik ; Luc Mallet

Source :

RBID : ISTEX:D33A19A1065CD121E47DA16D3E5717A75D4D6573

Abstract

Background The subthalamic nucleus (STN) is an efficient target for treating patients with Parkinson's disease as well as patients with obsessive–compulsive disorder (OCD) using high frequency stimulation (HFS). In both Parkinson's disease and OCD patients, STN-HFS can trigger abnormal behaviours, such as hypomania and impulsivity. Methods To investigate if this structure processes emotional information, and whether it depends on motor demands, we recorded subthalamic local field potentials in 16 patients with Parkinson's disease using deep brain stimulation electrodes. Recordings were made with and without dopaminergic treatment while patients performed an emotional categorisation paradigm in which the response varied according to stimulus valence (pleasant, unpleasant and neutral) and to the instruction given (motor, non-motor and passive). Results Pleasant, unpleasant and neutral stimuli evoked an event related potential (ERP). Without dopamine medication, ERP amplitudes were significantly larger for unpleasant compared with neutral pictures, whatever the response triggered by the stimuli; and the magnitude of this effect was maximal in the ventral part of the STN. No significant difference in ERP amplitude was observed for pleasant pictures. With dopamine medication, ERP amplitudes were significantly increased for pleasant compared with neutral pictures whatever the response triggered by the stimuli, while ERP amplitudes to unpleasant pictures were not modified. Conclusions These results demonstrate that the ventral part of the STN processes the emotional valence of stimuli independently of the motor context and that dopamine enhances processing of pleasant information. These findings confirm the specific involvement of the STN in emotional processes in human, which may underlie the behavioural changes observed in patients with deep brain stimulation.

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DOI: 10.1136/jnnp-2011-302158

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ISTEX:D33A19A1065CD121E47DA16D3E5717A75D4D6573

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<div type="abstract">Background The subthalamic nucleus (STN) is an efficient target for treating patients with Parkinson's disease as well as patients with obsessive–compulsive disorder (OCD) using high frequency stimulation (HFS). In both Parkinson's disease and OCD patients, STN-HFS can trigger abnormal behaviours, such as hypomania and impulsivity. Methods To investigate if this structure processes emotional information, and whether it depends on motor demands, we recorded subthalamic local field potentials in 16 patients with Parkinson's disease using deep brain stimulation electrodes. Recordings were made with and without dopaminergic treatment while patients performed an emotional categorisation paradigm in which the response varied according to stimulus valence (pleasant, unpleasant and neutral) and to the instruction given (motor, non-motor and passive). Results Pleasant, unpleasant and neutral stimuli evoked an event related potential (ERP). Without dopamine medication, ERP amplitudes were significantly larger for unpleasant compared with neutral pictures, whatever the response triggered by the stimuli; and the magnitude of this effect was maximal in the ventral part of the STN. No significant difference in ERP amplitude was observed for pleasant pictures. With dopamine medication, ERP amplitudes were significantly increased for pleasant compared with neutral pictures whatever the response triggered by the stimuli, while ERP amplitudes to unpleasant pictures were not modified. Conclusions These results demonstrate that the ventral part of the STN processes the emotional valence of stimuli independently of the motor context and that dopamine enhances processing of pleasant information. These findings confirm the specific involvement of the STN in emotional processes in human, which may underlie the behavioural changes observed in patients with deep brain stimulation.</div>
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<abstract>Background The subthalamic nucleus (STN) is an efficient target for treating patients with Parkinson's disease as well as patients with obsessive–compulsive disorder (OCD) using high frequency stimulation (HFS). In both Parkinson's disease and OCD patients, STN-HFS can trigger abnormal behaviours, such as hypomania and impulsivity. Methods To investigate if this structure processes emotional information, and whether it depends on motor demands, we recorded subthalamic local field potentials in 16 patients with Parkinson's disease using deep brain stimulation electrodes. Recordings were made with and without dopaminergic treatment while patients performed an emotional categorisation paradigm in which the response varied according to stimulus valence (pleasant, unpleasant and neutral) and to the instruction given (motor, non-motor and passive). Results Pleasant, unpleasant and neutral stimuli evoked an event related potential (ERP). Without dopamine medication, ERP amplitudes were significantly larger for unpleasant compared with neutral pictures, whatever the response triggered by the stimuli; and the magnitude of this effect was maximal in the ventral part of the STN. No significant difference in ERP amplitude was observed for pleasant pictures. With dopamine medication, ERP amplitudes were significantly increased for pleasant compared with neutral pictures whatever the response triggered by the stimuli, while ERP amplitudes to unpleasant pictures were not modified. Conclusions These results demonstrate that the ventral part of the STN processes the emotional valence of stimuli independently of the motor context and that dopamine enhances processing of pleasant information. These findings confirm the specific involvement of the STN in emotional processes in human, which may underlie the behavioural changes observed in patients with deep brain stimulation.</abstract>
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<forename type="first">Jean-Baptiste</forename>
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<forename type="first">Eric</forename>
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<forename type="first">Luc</forename>
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<p>Background The subthalamic nucleus (STN) is an efficient target for treating patients with Parkinson's disease as well as patients with obsessive–compulsive disorder (OCD) using high frequency stimulation (HFS). In both Parkinson's disease and OCD patients, STN-HFS can trigger abnormal behaviours, such as hypomania and impulsivity. Methods To investigate if this structure processes emotional information, and whether it depends on motor demands, we recorded subthalamic local field potentials in 16 patients with Parkinson's disease using deep brain stimulation electrodes. Recordings were made with and without dopaminergic treatment while patients performed an emotional categorisation paradigm in which the response varied according to stimulus valence (pleasant, unpleasant and neutral) and to the instruction given (motor, non-motor and passive). Results Pleasant, unpleasant and neutral stimuli evoked an event related potential (ERP). Without dopamine medication, ERP amplitudes were significantly larger for unpleasant compared with neutral pictures, whatever the response triggered by the stimuli; and the magnitude of this effect was maximal in the ventral part of the STN. No significant difference in ERP amplitude was observed for pleasant pictures. With dopamine medication, ERP amplitudes were significantly increased for pleasant compared with neutral pictures whatever the response triggered by the stimuli, while ERP amplitudes to unpleasant pictures were not modified. Conclusions These results demonstrate that the ventral part of the STN processes the emotional valence of stimuli independently of the motor context and that dopamine enhances processing of pleasant information. These findings confirm the specific involvement of the STN in emotional processes in human, which may underlie the behavioural changes observed in patients with deep brain stimulation.</p>
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<name>
<surname>Buot</surname>
<given-names>Anne</given-names>
</name>
<xref ref-type="aff" rid="af1">1</xref>
<xref ref-type="aff" rid="af2">2</xref>
<xref ref-type="aff" rid="af3">3</xref>
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<name>
<surname>Welter</surname>
<given-names>Marie-Laure</given-names>
</name>
<xref ref-type="aff" rid="af1">1</xref>
<xref ref-type="aff" rid="af2">2</xref>
<xref ref-type="aff" rid="af3">3</xref>
<xref ref-type="aff" rid="af4">4</xref>
<xref ref-type="aff" rid="af7">7</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Karachi</surname>
<given-names>Carine</given-names>
</name>
<xref ref-type="aff" rid="af1">1</xref>
<xref ref-type="aff" rid="af2">2</xref>
<xref ref-type="aff" rid="af3">3</xref>
<xref ref-type="aff" rid="af5">5</xref>
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<surname>Pochon</surname>
<given-names>Jean-Baptiste</given-names>
</name>
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<xref ref-type="aff" rid="af2">2</xref>
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<given-names>Eric</given-names>
</name>
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<given-names>Jérôme</given-names>
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<given-names>Luc</given-names>
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Centre de Recherche de l'Institut du Cerveau et de la Moelle épinière (CRICM), Université Pierre et Marie Curie-Paris 6, Paris, France</aff>
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Inserm, Paris, France</aff>
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<label>3</label>
CNRS, Paris, France</aff>
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<label>4</label>
Groupe Hospitalier Pitié-Salpêtrière, AP-HP, Fédération des maladies du système nerveux, Paris, France</aff>
<aff id="af5">
<label>5</label>
Groupe Hospitalier Pitié-Salpêtrière, AP-HP, Service de neurochirurgie, Paris, France</aff>
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Centre de Neuroimagerie de Recherche (CENIR), Groupe Hospitalier Pitié-Salpêtrière, Paris, France</aff>
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Centre d'Investigation Clinique, Groupe Hospitalier Pitié-Salpêtrière, AP-HP, Paris, France</aff>
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<label>Correspondence to</label>
A Buot, Centre de Recherche de l'Institut du Cerveau et de la Moelle épinière (CRICM), UPMC-Inserm UMR_S 975-CNRS UMR 7225, CHU Pitié-Salpêtrière, 47, Bd de L'Hôpital, 75651 Paris cedex 13, France;
<email>anne.buot@gmail.com</email>
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<p>The subthalamic nucleus (STN) is an efficient target for treating patients with Parkinson's disease as well as patients with obsessive–compulsive disorder (OCD) using high frequency stimulation (HFS). In both Parkinson's disease and OCD patients, STN-HFS can trigger abnormal behaviours, such as hypomania and impulsivity.</p>
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<sec>
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<p>To investigate if this structure processes emotional information, and whether it depends on motor demands, we recorded subthalamic local field potentials in 16 patients with Parkinson's disease using deep brain stimulation electrodes. Recordings were made with and without dopaminergic treatment while patients performed an emotional categorisation paradigm in which the response varied according to stimulus valence (pleasant, unpleasant and neutral) and to the instruction given (motor, non-motor and passive).</p>
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<p>Pleasant, unpleasant and neutral stimuli evoked an event related potential (ERP). Without dopamine medication, ERP amplitudes were significantly larger for unpleasant compared with neutral pictures, whatever the response triggered by the stimuli; and the magnitude of this effect was maximal in the ventral part of the STN. No significant difference in ERP amplitude was observed for pleasant pictures. With dopamine medication, ERP amplitudes were significantly increased for pleasant compared with neutral pictures whatever the response triggered by the stimuli, while ERP amplitudes to unpleasant pictures were not modified.</p>
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<p>These results demonstrate that the ventral part of the STN processes the emotional valence of stimuli independently of the motor context and that dopamine enhances processing of pleasant information. These findings confirm the specific involvement of the STN in emotional processes in human, which may underlie the behavioural changes observed in patients with deep brain stimulation.</p>
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