Cerebral responses and role of the prefrontal cortex in conditioned pain modulation: an fMRI study in healthy subjects
•The mechanisms underlying conditioned pain modulation are multifaceted.•During cold, application-specific cerebral activations were found in precuneus and left insula.•Conditioned suppression of insula test-pain response was related to hypoalgesia.•The insular changes are predicted by early prefron...
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| Published in | Behavioural brain research Vol. 281; pp. 187 - 198 |
|---|---|
| Main Authors | , , , , , , , , , |
| Format | Journal Article Web Resource |
| Language | English |
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Netherlands
Elsevier B.V
15.03.2015
Elsevier Elsevier Science |
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| Abstract | •The mechanisms underlying conditioned pain modulation are multifaceted.•During cold, application-specific cerebral activations were found in precuneus and left insula.•Conditioned suppression of insula test-pain response was related to hypoalgesia.•The insular changes are predicted by early prefrontal response to cold conditioning.•Smaller early prefrontal response predicts heterotopic noxious hyperalgesia.
The mechanisms underlying conditioned pain modulation (CPM) are multifaceted. We searched for a link between individual differences in prefrontal cortex activity during multi-trial heterotopic noxious cold conditioning and modulation of the cerebral response to phasic heat pain.
In 24 healthy female subjects, we conditioned laser heat stimuli to the left hand by applying alternatively ice-cold or lukewarm compresses to the right foot. We compared pain ratings with cerebral fMRI BOLD responses. We also analyzed the relation between CPM and BOLD changes produced by the heterotopic cold conditioning itself, as well as the impact of anxiety and habituation of cold-pain ratings.
Specific cerebral activation was identified in precuneus and left posterior insula/SII, respectively, during early and sustained phases of cold application. During cold conditioning, laser pain decreased (n=7), increased (n=10) or stayed unchanged (n=7). At the individual level, the psychophysical effect was directly proportional to the cold-induced modulation of the laser-induced BOLD response in left posterior insula/SII. The latter correlated with the BOLD response recorded 80s earlier during the initial 10-s phase of cold application in anterior cingulate, orbitofrontal and lateral prefrontal cortices.
High anxiety and habituation of cold pain were associated with greater laser heat-induced pain during heterotopic cold stimulation. The habituation was also linked to the early cold-induced orbitofrontal responses.
We conclude that individual differences in conditioned pain modulation are related to different levels of prefrontal cortical activation by the early part of the conditioning stimulus, possibly due to different levels in trait anxiety. |
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| AbstractList | The mechanisms underlying conditioned pain modulation (CPM) are multifaceted. We searched for a link between individual differences in prefrontal cortex activity during multi-trial heterotopic noxious cold conditioning and modulation of the cerebral response to phasic heat pain. In 24 healthy female subjects, we conditioned laser heat stimuli to the left hand by applying alternatively ice-cold or lukewarm compresses to the right foot. We compared pain ratings with cerebral fMRI BOLD responses. We also analyzed the relation between CPM and BOLD changes produced by the heterotopic cold conditioning itself, as well as the impact of anxiety and habituation of cold-pain ratings. Specific cerebral activation was identified in precuneus and left posterior insula/SII, respectively, during early and sustained phases of cold application. During cold conditioning, laser pain decreased (n=7), increased (n=10) or stayed unchanged (n=7). At the individual level, the psychophysical effect was directly proportional to the cold-induced modulation of the laser-induced BOLD response in left posterior insula/SII. The latter correlated with the BOLD response recorded 80s earlier during the initial 10-s phase of cold application in anterior cingulate, orbitofrontal and lateral prefrontal cortices. High anxiety and habituation of cold pain were associated with greater laser heat-induced pain during heterotopic cold stimulation. The habituation was also linked to the early cold-induced orbitofrontal responses. We conclude that individual differences in conditioned pain modulation are related to different levels of prefrontal cortical activation by the early part of the conditioning stimulus, possibly due to different levels in trait anxiety. The mechanisms underlying conditioned pain modulation (CPM) are multifaceted. We searched for a link between individual differences in prefrontal cortex activity during multi-trial heterotopic noxious cold conditioning and modulation of the cerebral response to phasic heat pain. In 24 healthy female subjects, we conditioned laser heat stimuli to the left hand by applying alternatively ice-cold or lukewarm compresses to the right foot. We compared pain ratings with cerebral fMRI BOLD responses. We also analyzed the relation between CPM and BOLD changes produced by the heterotopic cold conditioning itself, as well as the impact of anxiety and habituation of cold-pain ratings. Specific cerebral activation was identified in precuneus and left posterior insula/SII, respectively, during early and sustained phases of cold application. During cold conditioning, laser pain decreased (n=7), increased (n=10) or stayed unchanged (n=7). At the individual level, the psychophysical effect was directly proportional to the cold-induced modulation of the laser-induced BOLD response in left posterior insula/SII. The latter correlated with the BOLD response recorded 80s earlier during the initial 10-s phase of cold application in anterior cingulate, orbitofrontal and lateral prefrontal cortices. High anxiety and habituation of cold pain were associated with greater laser heat-induced pain during heterotopic cold stimulation. The habituation was also linked to the early cold-induced orbitofrontal responses. We conclude that individual differences in conditioned pain modulation are related to different levels of prefrontal cortical activation by the early part of the conditioning stimulus, possibly due to different levels in trait anxiety.The mechanisms underlying conditioned pain modulation (CPM) are multifaceted. We searched for a link between individual differences in prefrontal cortex activity during multi-trial heterotopic noxious cold conditioning and modulation of the cerebral response to phasic heat pain. In 24 healthy female subjects, we conditioned laser heat stimuli to the left hand by applying alternatively ice-cold or lukewarm compresses to the right foot. We compared pain ratings with cerebral fMRI BOLD responses. We also analyzed the relation between CPM and BOLD changes produced by the heterotopic cold conditioning itself, as well as the impact of anxiety and habituation of cold-pain ratings. Specific cerebral activation was identified in precuneus and left posterior insula/SII, respectively, during early and sustained phases of cold application. During cold conditioning, laser pain decreased (n=7), increased (n=10) or stayed unchanged (n=7). At the individual level, the psychophysical effect was directly proportional to the cold-induced modulation of the laser-induced BOLD response in left posterior insula/SII. The latter correlated with the BOLD response recorded 80s earlier during the initial 10-s phase of cold application in anterior cingulate, orbitofrontal and lateral prefrontal cortices. High anxiety and habituation of cold pain were associated with greater laser heat-induced pain during heterotopic cold stimulation. The habituation was also linked to the early cold-induced orbitofrontal responses. We conclude that individual differences in conditioned pain modulation are related to different levels of prefrontal cortical activation by the early part of the conditioning stimulus, possibly due to different levels in trait anxiety. •The mechanisms underlying conditioned pain modulation are multifaceted.•During cold, application-specific cerebral activations were found in precuneus and left insula.•Conditioned suppression of insula test-pain response was related to hypoalgesia.•The insular changes are predicted by early prefrontal response to cold conditioning.•Smaller early prefrontal response predicts heterotopic noxious hyperalgesia. The mechanisms underlying conditioned pain modulation (CPM) are multifaceted. We searched for a link between individual differences in prefrontal cortex activity during multi-trial heterotopic noxious cold conditioning and modulation of the cerebral response to phasic heat pain. In 24 healthy female subjects, we conditioned laser heat stimuli to the left hand by applying alternatively ice-cold or lukewarm compresses to the right foot. We compared pain ratings with cerebral fMRI BOLD responses. We also analyzed the relation between CPM and BOLD changes produced by the heterotopic cold conditioning itself, as well as the impact of anxiety and habituation of cold-pain ratings. Specific cerebral activation was identified in precuneus and left posterior insula/SII, respectively, during early and sustained phases of cold application. During cold conditioning, laser pain decreased (n=7), increased (n=10) or stayed unchanged (n=7). At the individual level, the psychophysical effect was directly proportional to the cold-induced modulation of the laser-induced BOLD response in left posterior insula/SII. The latter correlated with the BOLD response recorded 80s earlier during the initial 10-s phase of cold application in anterior cingulate, orbitofrontal and lateral prefrontal cortices. High anxiety and habituation of cold pain were associated with greater laser heat-induced pain during heterotopic cold stimulation. The habituation was also linked to the early cold-induced orbitofrontal responses. We conclude that individual differences in conditioned pain modulation are related to different levels of prefrontal cortical activation by the early part of the conditioning stimulus, possibly due to different levels in trait anxiety. The mechanisms underlying conditioned pain modulation (CPM) are multifaceted. We searched for a link between individual differences in prefrontal cortex activity during multi-trial heterotopic noxious cold conditioning and modulation of the cerebral response to phasic heat pain. In 24 healthy female subjects, we conditioned laser heat stimuli to the left hand by applying alternatively ice-cold or lukewarm compresses to the right foot. We compared pain ratings with cerebral fMRI BOLD responses. We also analyzed the relation between CPM and BOLD changes produced by the heterotopic cold conditioning itself, as well as the impact of anxiety and habituation of cold-pain ratings. Specific cerebral activation was identified in precuneus and left posterior insula/SII, respectively, during early and sustained phases of cold application. During cold conditioning, laser pain decreased ( n = 7), increased ( n = 10) or stayed unchanged ( n = 7). At the individual level, the psychophysical effect was directly proportional to the cold-induced modulation of the laser-induced BOLD response in left posterior insula/SII. The latter correlated with the BOLD response recorded 80 s earlier during the initial 10-s phase of cold application in anterior cingulate, orbitofrontal and lateral prefrontal cortices. High anxiety and habituation of cold pain were associated with greater laser heat-induced pain during heterotopic cold stimulation. The habituation was also linked to the early cold-induced orbitofrontal responses. We conclude that individual differences in conditioned pain modulation are related to different levels of prefrontal cortical activation by the early part of the conditioning stimulus, possibly due to different levels in trait anxiety. |
| Author | Noirhomme, Quentin Renshaw, Perry F. Guy, Nathalie Laureys, Steven Viganò, Alessandro Bogdanov, Volodymyr B. Phillips, Christophe Dallel, Radhouane Schoenen, Jean Bogdanova, Olena V. |
| AuthorAffiliation | b Headache Research Unit, Department of Neurology, CHR Citadelle, University of Liège, Liège, Belgium e Coma Science Group, Department of Neurology, University and University Hospital of Liège, Liège, Belgium a INRA, Nutrition et Neurobiologie Intégrée and Bordeaux Segalen University, UMR 1286, 146 rue Léo-Saignat, Bordeaux Cedex, 33076, France c SAMILAL- Dept. Anatomy, Histology, Forensic Medicine, Orthopaedics - La Sapienza, University of Rome; Dept. of Neurology and Psychiatry - La Sapienza, University of Rome h Department of electrical engineering and computer science, University of Liège, Liège, Belgium f University of Utah, Salt Lake City, USA d Cyclotron Research Centre, University of Liège, Liège, Belgium g Clermont Université, Université d’Auvergne, BP 10448, F-63000 Clermont-Ferrand; Inserm, UMR1107, Trigeminal pain and Migraine F-63000 Clermont-Ferrand; CHU, Clermont-Ferrand |
| AuthorAffiliation_xml | – name: a INRA, Nutrition et Neurobiologie Intégrée and Bordeaux Segalen University, UMR 1286, 146 rue Léo-Saignat, Bordeaux Cedex, 33076, France – name: e Coma Science Group, Department of Neurology, University and University Hospital of Liège, Liège, Belgium – name: h Department of electrical engineering and computer science, University of Liège, Liège, Belgium – name: d Cyclotron Research Centre, University of Liège, Liège, Belgium – name: b Headache Research Unit, Department of Neurology, CHR Citadelle, University of Liège, Liège, Belgium – name: g Clermont Université, Université d’Auvergne, BP 10448, F-63000 Clermont-Ferrand; Inserm, UMR1107, Trigeminal pain and Migraine F-63000 Clermont-Ferrand; CHU, Clermont-Ferrand – name: c SAMILAL- Dept. Anatomy, Histology, Forensic Medicine, Orthopaedics - La Sapienza, University of Rome; Dept. of Neurology and Psychiatry - La Sapienza, University of Rome – name: f University of Utah, Salt Lake City, USA |
| Author_xml | – sequence: 1 givenname: Volodymyr B. surname: Bogdanov fullname: Bogdanov, Volodymyr B. email: vlabogd@yahoo.com organization: INRA, Nutrition et Neurobiologie Intégrée and Bordeaux Segalen University, UMR 1286, 146 rue Léo-Saignat, Bordeaux Cedex, 33076, France – sequence: 2 givenname: Alessandro surname: Viganò fullname: Viganò, Alessandro organization: Headache Research Unit, Department of Neurology, CHR Citadelle, University of Liège, Liège, Belgium – sequence: 3 givenname: Quentin surname: Noirhomme fullname: Noirhomme, Quentin organization: Cyclotron Research Centre, University of Liège, Liège, Belgium – sequence: 4 givenname: Olena V. surname: Bogdanova fullname: Bogdanova, Olena V. organization: University of Utah, Salt Lake City, USA – sequence: 5 givenname: Nathalie surname: Guy fullname: Guy, Nathalie organization: Clermont Université, Université d’Auvergne, BP 10448, F-63000 Clermont-Ferrand; Inserm, UMR1107, Trigeminal pain and Migraine F-63000 Clermont-Ferrand; CHU, Clermont-Ferrand – sequence: 6 givenname: Steven surname: Laureys fullname: Laureys, Steven organization: Cyclotron Research Centre, University of Liège, Liège, Belgium – sequence: 7 givenname: Perry F. surname: Renshaw fullname: Renshaw, Perry F. organization: University of Utah, Salt Lake City, USA – sequence: 8 givenname: Radhouane surname: Dallel fullname: Dallel, Radhouane organization: Clermont Université, Université d’Auvergne, BP 10448, F-63000 Clermont-Ferrand; Inserm, UMR1107, Trigeminal pain and Migraine F-63000 Clermont-Ferrand; CHU, Clermont-Ferrand – sequence: 9 givenname: Christophe surname: Phillips fullname: Phillips, Christophe organization: Cyclotron Research Centre, University of Liège, Liège, Belgium – sequence: 10 givenname: Jean surname: Schoenen fullname: Schoenen, Jean organization: Headache Research Unit, Department of Neurology, CHR Citadelle, University of Liège, Liège, Belgium |
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| Snippet | •The mechanisms underlying conditioned pain modulation are multifaceted.•During cold, application-specific cerebral activations were found in precuneus and... The mechanisms underlying conditioned pain modulation (CPM) are multifaceted. We searched for a link between individual differences in prefrontal cortex... |
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| SubjectTerms | Adult Brain imaging Brain Mapping - methods Cerebral Cortex - physiopathology Cold Temperature Conditioned pain modulation Conditioning (Psychology) Female Healthy Volunteers Hot Temperature Human health sciences Humans Individuality Life Sciences Magnetic Resonance Imaging Middle Aged Neurologie Neurology Neurons and Cognition Pain - physiopathology Pain - psychology Pain Measurement - methods Pain Threshold Prefrontal cortex Prefrontal Cortex - physiopathology Sciences de la santé humaine Young Adult |
| Title | Cerebral responses and role of the prefrontal cortex in conditioned pain modulation: an fMRI study in healthy subjects |
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