Inhibitory control and error monitoring by human subthalamic neurons
Identifieur interne : 001504 ( Ncbi/Merge ); précédent : 001503; suivant : 001505Inhibitory control and error monitoring by human subthalamic neurons
Auteurs : J. Bastin [France] ; M. Polosan [France] ; D. Benis [France] ; L. Goetz [France] ; M. Bhattacharjee [France] ; B. Piallat [France] ; A. Krainik [France] ; T. Bougerol [France] ; S. Chabardès [France] ; O. David [France]Source :
- Translational Psychiatry [ 2158-3188 ] ; 2014.
Abstract
The subthalamic nucleus (STN) has been shown to be implicated in the control of voluntary action, especially during tasks involving conflicting choice alternatives or rapid response suppression. However, the precise role of the STN during nonmotor functions remains controversial. First, we tested whether functionally distinct neuronal populations support different executive control functions (such as inhibitory control or error monitoring) even within a single subterritory of the STN. We used microelectrode recordings during deep brain stimulation surgery to study extracellular activity of the putative associative-limbic part of the STN while patients with severe obsessive-compulsive disorder performed a stop-signal task. Second, 2–4 days after the surgery, local field potential recordings of STN were used to test the hypothesis that STN oscillations may also reflect executive control signals. Extracellular recordings revealed three functionally distinct neuronal populations: the first one fired selectively before and during motor responses, the second one selectively increased their firing rate during successful inhibitory control, and the last one fired selectively during error monitoring. Furthermore, we found that beta band activity (15–35 Hz) rapidly increased during correct and incorrect behavioral stopping. Taken together, our results provide critical electrophysiological support for the hypothesized role of the STN in the integration of motor and cognitive-executive control functions.
Url:
DOI: 10.1038/tp.2014.73
PubMed: 25203170
PubMed Central: 4203004
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<front><div type="abstract" xml:lang="en"><p>The subthalamic nucleus (STN) has been shown to be implicated in the control of voluntary action, especially during tasks involving conflicting choice alternatives or rapid response suppression. However, the precise role of the STN during nonmotor functions remains controversial. First, we tested whether functionally distinct neuronal populations support different executive control functions (such as inhibitory control or error monitoring) even within a single subterritory of the STN. We used microelectrode recordings during deep brain stimulation surgery to study extracellular activity of the putative associative-limbic part of the STN while patients with severe obsessive-compulsive disorder performed a stop-signal task. Second, 2–4 days after the surgery, local field potential recordings of STN were used to test the hypothesis that STN oscillations may also reflect executive control signals. Extracellular recordings revealed three functionally distinct neuronal populations: the first one fired selectively before and during motor responses, the second one selectively increased their firing rate during successful inhibitory control, and the last one fired selectively during error monitoring. Furthermore, we found that beta band activity (15–35 Hz) rapidly increased during correct and incorrect behavioral stopping. Taken together, our results provide critical electrophysiological support for the hypothesized role of the STN in the integration of motor and cognitive-executive control functions.</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">Transl Psychiatry</journal-id>
<journal-id journal-id-type="iso-abbrev">Transl Psychiatry</journal-id>
<journal-title-group><journal-title>Translational Psychiatry</journal-title>
</journal-title-group>
<issn pub-type="epub">2158-3188</issn>
<publisher><publisher-name>Nature Publishing Group</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">25203170</article-id>
<article-id pub-id-type="pmc">4203004</article-id>
<article-id pub-id-type="pii">tp201473</article-id>
<article-id pub-id-type="doi">10.1038/tp.2014.73</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Original Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Inhibitory control and error monitoring by human subthalamic neurons</article-title>
<alt-title alt-title-type="running">Executive control by human subthalamic nucleus</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Bastin</surname>
<given-names>J</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="aff" rid="aff2">2</xref>
<xref ref-type="corresp" rid="caf1">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Polosan</surname>
<given-names>M</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="aff" rid="aff2">2</xref>
<xref ref-type="aff" rid="aff3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Benis</surname>
<given-names>D</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="aff" rid="aff2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Goetz</surname>
<given-names>L</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="aff" rid="aff2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Bhattacharjee</surname>
<given-names>M</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="aff" rid="aff2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Piallat</surname>
<given-names>B</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="aff" rid="aff2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Krainik</surname>
<given-names>A</given-names>
</name>
<xref ref-type="aff" rid="aff2">2</xref>
<xref ref-type="aff" rid="aff4">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Bougerol</surname>
<given-names>T</given-names>
</name>
<xref ref-type="aff" rid="aff3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Chabardès</surname>
<given-names>S</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="aff" rid="aff2">2</xref>
<xref ref-type="aff" rid="aff5">5</xref>
</contrib>
<contrib contrib-type="author"><name><surname>David</surname>
<given-names>O</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="aff" rid="aff2">2</xref>
</contrib>
<aff id="aff1"><label>1</label>
<institution>Fonctions Cérébrales et Neuromodulation, Université Joseph Fourier</institution>
, Grenoble,<country>France</country>
</aff>
<aff id="aff2"><label>2</label>
<institution>Grenoble Institut des Neurosciences, INSERM, U836</institution>
, Grenoble,<country>France</country>
</aff>
<aff id="aff3"><label>3</label>
<institution>Clinique de Psychiatrie, Pôle Neurologie Psychiatrie, Centre Hospitalier Universitaire</institution>
, Grenoble,<country>France</country>
</aff>
<aff id="aff4"><label>4</label>
<institution>Clinique de Neuroradiologie, Pôle Imagerie, Centre Hospitalier Universitaire</institution>
, Grenoble,<country>France</country>
</aff>
<aff id="aff5"><label>5</label>
<institution>Clinique de Neurochirurgie, Pôle Tête et Cou, Centre Hospitalier Universitaire</institution>
, Grenoble,<country>France</country>
</aff>
</contrib-group>
<author-notes><corresp id="caf1"><label>*</label>
<institution>Institut des Neurosciences de Grenoble, Bâtiment Edmond J. Safra des Neurosciences, Chemin Fortuné Ferrini</institution>
, Université Joseph Fourier, Site Santé La Tronche, BP 170, 38042 Grenoble Cedex 9, <country>France</country>
. E-mail: <email>julien.bastin@ujf-grenoble.fr</email>
</corresp>
</author-notes>
<pub-date pub-type="ppub"><month>09</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="epub"><day>09</day>
<month>09</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>1</day>
<month>9</month>
<year>2014</year>
</pub-date>
<volume>4</volume>
<issue>9</issue>
<fpage>e439</fpage>
<lpage></lpage>
<history><date date-type="received"><day>27</day>
<month>08</month>
<year>2013</year>
</date>
<date date-type="rev-recd"><day>30</day>
<month>06</month>
<year>2014</year>
</date>
<date date-type="accepted"><day>14</day>
<month>07</month>
<year>2014</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2014 Macmillan Publishers Limited</copyright-statement>
<copyright-year>2014</copyright-year>
<copyright-holder>Macmillan Publishers Limited</copyright-holder>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by-nc-sa/3.0/"><pmc-comment>author-paid</pmc-comment>
<license-p>This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 3.0 Unported License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by-nc-sa/3.0/">http://creativecommons.org/licenses/by-nc-sa/3.0/</ext-link>
</license-p>
</license>
</permissions>
<abstract><p>The subthalamic nucleus (STN) has been shown to be implicated in the control of voluntary action, especially during tasks involving conflicting choice alternatives or rapid response suppression. However, the precise role of the STN during nonmotor functions remains controversial. First, we tested whether functionally distinct neuronal populations support different executive control functions (such as inhibitory control or error monitoring) even within a single subterritory of the STN. We used microelectrode recordings during deep brain stimulation surgery to study extracellular activity of the putative associative-limbic part of the STN while patients with severe obsessive-compulsive disorder performed a stop-signal task. Second, 2–4 days after the surgery, local field potential recordings of STN were used to test the hypothesis that STN oscillations may also reflect executive control signals. Extracellular recordings revealed three functionally distinct neuronal populations: the first one fired selectively before and during motor responses, the second one selectively increased their firing rate during successful inhibitory control, and the last one fired selectively during error monitoring. Furthermore, we found that beta band activity (15–35 Hz) rapidly increased during correct and incorrect behavioral stopping. Taken together, our results provide critical electrophysiological support for the hypothesized role of the STN in the integration of motor and cognitive-executive control functions.</p>
</abstract>
</article-meta>
</front>
<floats-group><fig id="fig1"><label>Figure 1</label>
<caption><p>(<bold>a</bold>
) Localization of DBS electrodes contacts on axial and coronal MRI sections of a patient. (<bold>b</bold>
) Microelectrode STN recording and mean waveform (black)±s.d. (gray) of the isolated spike cluster. (<bold>c</bold>
) Stop-signal task. Participants were instructed to respond as fast as they can to the GO cue and to withhold their response when a stop signal occurs. Task difficulty during STOP trials was adjusted by shortening or lengthening the delay between GO and STOP cues (stop-signal delay, SSD) after unsuccessful or successful STOP trials. After each trial, positive and negative feedback was presented for 1 s (see Materials and Methods). CD, caudate nucleus; DBS, deep brain stimulation; GP, globus pallidus; MRI, magnetic resonance imaging; RN, red nucleus; SN, substantia nigra; STN, subthalamic nucleus.</p>
</caption>
<graphic xlink:href="tp201473f1"></graphic>
</fig>
<fig id="fig2"><label>Figure 2</label>
<caption><p>Selective response of STN neurons during stopping, shown as rastergrams (black dots), SDF (continuous lines) and PSTH across trial types (SS, US, LMGO). (<bold>a</bold>
) Representative SS unit. In rastergrams, green dots indicate the onset of GO cue and blue dots indicate the time of incorrect button press. Trials are sorted according to their stop-signal delay (SS and US trials) or motor reaction time (GO trials). Time origin indicates stop cue during SS and US trials and simulated stop cue during LMGO trials. Vertical dashed red line indicates SSRT during this SST experiment. (<bold>b</bold>
) Normalized population activity of all recorded SS units (<italic>n</italic>
=10). Error bars indicate s.e.m. LMGO, latency-matched GO; PSTH, peri-stimulus spike histogram; SDF, spike density function; SS, successful stop trial; SSRT, stop-signal reaction time; SST, stop-signal task; STN, subthalamic nucleus; US, unsuccessful stop trial.</p>
</caption>
<graphic xlink:href="tp201473f2"></graphic>
</fig>
<fig id="fig3"><label>Figure 3</label>
<caption><p>Selective response of STN neurons during error monitoring, shown as rastergrams (black dots), SDF (continuous lines) and PSTH across trial types (US, fast GO trials and SS). (<bold>a</bold>
) Representative US unit. In rastergrams, green dots indicate the onset of GO cue and red dots indicate time of stop cue. Time origin indicates button presses (BP) during US and fast GO trials and stop cue during SS trials. (<bold>b</bold>
) Population activity of all recorded US units (<italic>n</italic>
=12). The conventions are as in <xref ref-type="fig" rid="fig5">Figure 5</xref>
. PSTH, peri-stimulus spike histogram; SDF, spike density function; SS, successful stop trial; STN, subthalamic nucleus; US, unsuccessful stop trial.</p>
</caption>
<graphic xlink:href="tp201473f3"></graphic>
</fig>
<fig id="fig4"><label>Figure 4</label>
<caption><p>Selective response of STN neurons during motor responses, shown as rastergrams (black dots), SDF (continuous lines) and PSTH across trial types (US, GO and SS trials). (<bold>a</bold>
) Representative GO unit. Time origin indicates button presses (BP) during US and fast GO trials and stop cue during SS trials. (<bold>b</bold>
) Population activity of all recorded GO units (<italic>n</italic>
=10). The conventions are as in <xref ref-type="fig" rid="fig5">Figure 5</xref>
. PSTH, peri-stimulus spike histogram; SDF, spike density function; SS, successful stop trial; STN, subthalamic nucleus; US, unsuccessful stop trial.</p>
</caption>
<graphic xlink:href="tp201473f4"></graphic>
</fig>
<fig id="fig5"><label>Figure 5</label>
<caption><p>Subthalamic task-related LFP activity. (<bold>a</bold>
) Trial-averaged time-frequency charts of a STN bipolar recording in a representative patient. Time origin indicates stop cue during SS and US trials and button press during GO trials. (<bold>b</bold>
) Single-trial beta band power of a STN bipolar recording time-locked to stop cue during SS and US trials and to virtual stop cue during GO trials. (<bold>c</bold>
) Grand average beta power time series (<italic>n</italic>
=7 patients, 14 recorded STNs). (<bold>d</bold>
) Beta band maximal power amplitude in the 500-ms period after stop (or virtual stop) cue. Vertical dashed orange line indicates the average latency at which the difference between SS and LMGO trials reached significance. Vertical dashed red line indicates SSRT. Stars indicate significant differences between trial types (<italic>post hoc</italic>
Tukey, <italic>P</italic>
<0.05). LFP, local field potential; LMGO, latency-matched GO; SS, successful stop trial; SSRT, stop-signal reaction time; STN, subthalamic nucleus; US, unsuccessful stop trial.</p>
</caption>
<graphic xlink:href="tp201473f5"></graphic>
</fig>
</floats-group>
</pmc>
<affiliations><list><country><li>France</li>
</country>
</list>
<tree><country name="France"><noRegion><name sortKey="Bastin, J" sort="Bastin, J" uniqKey="Bastin J" first="J" last="Bastin">J. Bastin</name>
</noRegion>
<name sortKey="Bastin, J" sort="Bastin, J" uniqKey="Bastin J" first="J" last="Bastin">J. Bastin</name>
<name sortKey="Benis, D" sort="Benis, D" uniqKey="Benis D" first="D" last="Benis">D. Benis</name>
<name sortKey="Benis, D" sort="Benis, D" uniqKey="Benis D" first="D" last="Benis">D. Benis</name>
<name sortKey="Bhattacharjee, M" sort="Bhattacharjee, M" uniqKey="Bhattacharjee M" first="M" last="Bhattacharjee">M. Bhattacharjee</name>
<name sortKey="Bhattacharjee, M" sort="Bhattacharjee, M" uniqKey="Bhattacharjee M" first="M" last="Bhattacharjee">M. Bhattacharjee</name>
<name sortKey="Bougerol, T" sort="Bougerol, T" uniqKey="Bougerol T" first="T" last="Bougerol">T. Bougerol</name>
<name sortKey="Chabardes, S" sort="Chabardes, S" uniqKey="Chabardes S" first="S" last="Chabardès">S. Chabardès</name>
<name sortKey="Chabardes, S" sort="Chabardes, S" uniqKey="Chabardes S" first="S" last="Chabardès">S. Chabardès</name>
<name sortKey="Chabardes, S" sort="Chabardes, S" uniqKey="Chabardes S" first="S" last="Chabardès">S. Chabardès</name>
<name sortKey="David, O" sort="David, O" uniqKey="David O" first="O" last="David">O. David</name>
<name sortKey="David, O" sort="David, O" uniqKey="David O" first="O" last="David">O. David</name>
<name sortKey="Goetz, L" sort="Goetz, L" uniqKey="Goetz L" first="L" last="Goetz">L. Goetz</name>
<name sortKey="Goetz, L" sort="Goetz, L" uniqKey="Goetz L" first="L" last="Goetz">L. Goetz</name>
<name sortKey="Krainik, A" sort="Krainik, A" uniqKey="Krainik A" first="A" last="Krainik">A. Krainik</name>
<name sortKey="Krainik, A" sort="Krainik, A" uniqKey="Krainik A" first="A" last="Krainik">A. Krainik</name>
<name sortKey="Piallat, B" sort="Piallat, B" uniqKey="Piallat B" first="B" last="Piallat">B. Piallat</name>
<name sortKey="Piallat, B" sort="Piallat, B" uniqKey="Piallat B" first="B" last="Piallat">B. Piallat</name>
<name sortKey="Polosan, M" sort="Polosan, M" uniqKey="Polosan M" first="M" last="Polosan">M. Polosan</name>
<name sortKey="Polosan, M" sort="Polosan, M" uniqKey="Polosan M" first="M" last="Polosan">M. Polosan</name>
<name sortKey="Polosan, M" sort="Polosan, M" uniqKey="Polosan M" first="M" last="Polosan">M. Polosan</name>
</country>
</tree>
</affiliations>
</record>
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