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Top-down and bottom-up modulation of pain-induced oscillations

Identifieur interne : 000027 ( Pmc/Checkpoint ); précédent : 000026; suivant : 000028

Top-down and bottom-up modulation of pain-induced oscillations

Auteurs : Michael Hauck [Allemagne] ; Claudia Domnick [Allemagne] ; Jürgen Lorenz [Allemagne] ; Christian Gerloff [Allemagne] ; Andreas K. Engel [Allemagne]

Source :

RBID : PMC:4488623

Abstract

Attention is an important factor that is able to strongly modulate the experience of pain. In order to differentiate cortical mechanisms underlying subject-driven (i.e., top-down) and stimulus-driven (bottom-up) modes of attentional pain modulation, we recorded electric brain activity in healthy volunteers during painful laser stimulation while spatial attention and stimulus intensity were systematically varied. The subjects’ task was to evaluate the pain intensity at the attended finger, while ignoring laser stimuli delivered to the other finger. Top-down (attention) and bottom up (intensity) influences differed in their effects on oscillatory response components. Attention towards pain induced a decrease in alpha and an increase in gamma band power, localized in the insula. Pain intensity modulated delta, alpha, beta and gamma band power. Source localization revealed stimulus driven modulation in the cingulate gyrus (CG) and somatosensory areas for gamma power changes. Our results indicate that bottom-up and top-down modes of processing exert different effects on pain-induced slow and fast oscillatory activities. Future studies may examine pain-induced oscillations using this paradigm to test for altered attentional pain control in patients with chronic pain.


Url:
DOI: 10.3389/fnhum.2015.00375
PubMed: 26190991
PubMed Central: 4488623


Affiliations:


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PMC:4488623

Le document en format XML

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<p>Attention is an important factor that is able to strongly modulate the experience of pain. In order to differentiate cortical mechanisms underlying subject-driven (i.e., top-down) and stimulus-driven (bottom-up) modes of attentional pain modulation, we recorded electric brain activity in healthy volunteers during painful laser stimulation while spatial attention and stimulus intensity were systematically varied. The subjects’ task was to evaluate the pain intensity at the attended finger, while ignoring laser stimuli delivered to the other finger. Top-down (attention) and bottom up (intensity) influences differed in their effects on oscillatory response components. Attention towards pain induced a decrease in alpha and an increase in gamma band power, localized in the insula. Pain intensity modulated delta, alpha, beta and gamma band power. Source localization revealed stimulus driven modulation in the cingulate gyrus (CG) and somatosensory areas for gamma power changes. Our results indicate that bottom-up and top-down modes of processing exert different effects on pain-induced slow and fast oscillatory activities. Future studies may examine pain-induced oscillations using this paradigm to test for altered attentional pain control in patients with chronic pain.</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">26190991</article-id>
<article-id pub-id-type="pmc">4488623</article-id>
<article-id pub-id-type="doi">10.3389/fnhum.2015.00375</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Neuroscience</subject>
<subj-group>
<subject>Original Research</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Top-down and bottom-up modulation of pain-induced oscillations</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Hauck</surname>
<given-names>Michael</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="author-notes" rid="fn001">
<sup>*</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/210846"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Domnick</surname>
<given-names>Claudia</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Lorenz</surname>
<given-names>Jürgen</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Gerloff</surname>
<given-names>Christian</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/21012"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Engel</surname>
<given-names>Andreas K.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/3693"></uri>
</contrib>
</contrib-group>
<aff id="aff1">
<sup>1</sup>
<institution>Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf</institution>
<country>Hamburg, Germany</country>
</aff>
<aff id="aff2">
<sup>2</sup>
<institution>Department of Neurology, University Medical Center Hamburg-Eppendorf</institution>
<country>Hamburg, Germany</country>
</aff>
<aff id="aff3">
<sup>3</sup>
<institution>Faculty of Life Science, Laboratory of Human Biology and Physiology, Applied Science University</institution>
<country>Hamburg, Germany</country>
</aff>
<author-notes>
<fn fn-type="edited-by">
<p>Edited by: Klaus Gramann, Berlin Institute of Technology, Germany</p>
</fn>
<fn fn-type="edited-by">
<p>Reviewed by: Markus Bauer, University of Nottingham, UK; Massimiliano Valeriani, Ospedale Pediatrico Bambino Gesú, Italy</p>
</fn>
<corresp id="fn001">*Correspondence: Michael Hauck, Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf, Martinistrasse 52, 20246 Hamburg, Germany
<email xlink:type="simple">hauck@uke.de</email>
</corresp>
</author-notes>
<pub-date pub-type="epub">
<day>02</day>
<month>7</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="collection">
<year>2015</year>
</pub-date>
<volume>9</volume>
<elocation-id>375</elocation-id>
<history>
<date date-type="received">
<day>13</day>
<month>4</month>
<year>2015</year>
</date>
<date date-type="accepted">
<day>15</day>
<month>6</month>
<year>2015</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright © 2015 Hauck, Domnick, Lorenz, Gerloff and Engel.</copyright-statement>
<copyright-year>2015</copyright-year>
<copyright-holder>Hauck, Domnick, Lorenz, Gerloff and Engel</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 Creative Commons Attribution License (CC BY). The use, distribution and 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>Attention is an important factor that is able to strongly modulate the experience of pain. In order to differentiate cortical mechanisms underlying subject-driven (i.e., top-down) and stimulus-driven (bottom-up) modes of attentional pain modulation, we recorded electric brain activity in healthy volunteers during painful laser stimulation while spatial attention and stimulus intensity were systematically varied. The subjects’ task was to evaluate the pain intensity at the attended finger, while ignoring laser stimuli delivered to the other finger. Top-down (attention) and bottom up (intensity) influences differed in their effects on oscillatory response components. Attention towards pain induced a decrease in alpha and an increase in gamma band power, localized in the insula. Pain intensity modulated delta, alpha, beta and gamma band power. Source localization revealed stimulus driven modulation in the cingulate gyrus (CG) and somatosensory areas for gamma power changes. Our results indicate that bottom-up and top-down modes of processing exert different effects on pain-induced slow and fast oscillatory activities. Future studies may examine pain-induced oscillations using this paradigm to test for altered attentional pain control in patients with chronic pain.</p>
</abstract>
<kwd-group>
<kwd>pain</kwd>
<kwd>EEG</kwd>
<kwd>gamma band</kwd>
<kwd>attention</kwd>
<kwd>functional imaging</kwd>
</kwd-group>
<funding-group>
<award-group>
<funding-source id="cn001">UKE Junior Research</funding-source>
<award-id rid="cn001">FFM F-161-1</award-id>
<award-id rid="cn001">SFB 936/Z1</award-id>
</award-group>
</funding-group>
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<fig-count count="4"></fig-count>
<table-count count="0"></table-count>
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</article-meta>
</front>
</pmc>
<affiliations>
<list>
<country>
<li>Allemagne</li>
</country>
</list>
<tree>
<country name="Allemagne">
<noRegion>
<name sortKey="Hauck, Michael" sort="Hauck, Michael" uniqKey="Hauck M" first="Michael" last="Hauck">Michael Hauck</name>
</noRegion>
<name sortKey="Domnick, Claudia" sort="Domnick, Claudia" uniqKey="Domnick C" first="Claudia" last="Domnick">Claudia Domnick</name>
<name sortKey="Engel, Andreas K" sort="Engel, Andreas K" uniqKey="Engel A" first="Andreas K." last="Engel">Andreas K. Engel</name>
<name sortKey="Gerloff, Christian" sort="Gerloff, Christian" uniqKey="Gerloff C" first="Christian" last="Gerloff">Christian Gerloff</name>
<name sortKey="Hauck, Michael" sort="Hauck, Michael" uniqKey="Hauck M" first="Michael" last="Hauck">Michael Hauck</name>
<name sortKey="Lorenz, Jurgen" sort="Lorenz, Jurgen" uniqKey="Lorenz J" first="Jürgen" last="Lorenz">Jürgen Lorenz</name>
</country>
</tree>
</affiliations>
</record>

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