Uncertainty in anticipation of uncomfortable rectal distension is modulated by the autonomic nervous system — A fMRI study in healthy volunteers
The human brain responds both before and during the application of aversive stimuli. Anticipation allows the organism to prepare its nociceptive system to respond adequately to the subsequent stimulus. The context in which an uncomfortable stimulus is experienced may also influence neural processing...
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Published in | NeuroImage (Orlando, Fla.) Vol. 107; pp. 10 - 22 |
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Main Authors | , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
Elsevier Inc
15.02.2015
Elsevier Limited Elsevier |
Subjects | |
Online Access | Get full text |
ISSN | 1053-8119 1095-9572 1095-9572 |
DOI | 10.1016/j.neuroimage.2014.11.043 |
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Abstract | The human brain responds both before and during the application of aversive stimuli. Anticipation allows the organism to prepare its nociceptive system to respond adequately to the subsequent stimulus. The context in which an uncomfortable stimulus is experienced may also influence neural processing. Uncertainty of occurrence, timing and intensity of an aversive event may lead to increased anticipatory anxiety, fear, physiological arousal and sensory perception.
We aimed to identify, in healthy volunteers, the effects of uncertainty in the anticipation of uncomfortable rectal distension, and the impact of the autonomic nervous system (ANS) activity and anxiety-related psychological variables on neural mechanisms of anticipation of rectal distension using fMRI.
Barostat-controlled uncomfortable rectal distensions were preceded by cued uncertain or certain anticipation in 15 healthy volunteers in a fMRI protocol at 3T. Electrocardiographic data were concurrently registered by MR scanner. The low frequency (LF)-component of the heart rate variability (HRV) time-series was extracted and inserted as a regressor in the fMRI model (‘LF-HRV model’). The impact of ANS activity was analyzed by comparing the fMRI signal in the ‘standard model’ and in the ‘LF-HRV model’ across the different anticipation and distension conditions. The scores of the psychological questionnaires and the rating of perceived anticipatory anxiety were included as covariates in the fMRI data analysis.
Our experiments led to the following key findings: 1) the subgenual anterior cingulate cortex (sgACC) is the only activation site that relates to uncertainty in healthy volunteers and is directly correlated to individual questionnaire score for pain-related anxiety; 2) uncertain anticipation of rectal distension involved several relevant brain regions, namely activation of sgACC and medial prefrontal cortex and deactivation of amygdala, insula, thalamus, secondary somatosensory cortex, supplementary motor area and cerebellum; 3) most of the brain activity during anticipation, but not distension, is associated with activity of the central autonomic network.
This approach could be applied to study the ANS impact on brain activity in various pathological conditions, namely in patients with chronic digestive conditions characterized by visceral discomfort and ANS imbalance such as irritable bowel syndrome or inflammatory bowel diseases.
•sgACC is the only activation site that relates to uncertainty, in healthy subjects.•sgACC activation during uncertainty is correlated to individual pain-related anxiety.•Uncertain anticipation involves activation of sgACC-MPFC and amygdala deactivation.•Brain activity during anticipation reflects central autonomic network activity. |
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AbstractList | The human brain responds both before and during the application of aversive stimuli. Anticipation allows the organism to prepare its nociceptive system to respond adequately to the subsequent stimulus. The context in which an uncomfortable stimulus is experienced may also influence neural processing. Uncertainty of occurrence, timing and intensity of an aversive event may lead to increased anticipatory anxiety, fear, physiological arousal and sensory perception. We aimed to identify, in healthy volunteers, the effects of uncertainty in the anticipation of uncomfortable rectal distension, and the impact of the autonomic nervous system (ANS) activity and anxiety-related psychological variables on neural mechanisms of anticipation of rectal distension using fMRI. Barostat-controlled uncomfortable rectal distensions were preceded by cued uncertain or certain anticipation in 15 healthy volunteers in a fMRI protocol at 3T. Electrocardiographic data were concurrently registered by MR scanner. The low frequency (LF)-component of the heart rate variability (HRV) time-series was extracted and inserted as a regressor in the fMRI model ('LF-HRV model'). The impact of ANS activity was analyzed by comparing the fMRI signal in the 'standard model' and in the 'LF-HRV model' across the different anticipation and distension conditions. The scores of the psychological questionnaires and the rating of perceived anticipatory anxiety were included as covariates in the fMRI data analysis. Our experiments led to the following key findings: 1) the subgenual anterior cingulate cortex (sgACC) is the only activation site that relates to uncertainty in healthy volunteers and is directly correlated to individual questionnaire score for pain-related anxiety; 2) uncertain anticipation of rectal distension involved several relevant brain regions, namely activation of sgACC and medial prefrontal cortex and deactivation of amygdala, insula, thalamus, secondary somatosensory cortex, supplementary motor area and cerebellum; 3) most of the brain activity during anticipation, but not distension, is associated with activity of the central autonomic network. This approach could be applied to study the ANS impact on brain activity in various pathological conditions, namely in patients with chronic digestive conditions characterized by visceral discomfort and ANS imbalance such as irritable bowel syndrome or inflammatory bowel diseases. The human brain responds both before and during the application of aversive stimuli. Anticipation allows the organism to prepare its nociceptive system to respond adequately to the subsequent stimulus. The context in which an uncomfortable stimulus is experienced may also influence neural processing. Uncertainty of occurrence, timing and intensity of an aversive event may lead to increased anticipatory anxiety, fear, physiological arousal and sensory perception. We aimed to identify, in healthy volunteers, the effects of uncertainty in the anticipation of uncomfortable rectal distension, and the impact of the autonomic nervous system (ANS) activity and anxiety-related psychological variables on neural mechanisms of anticipation of rectal distension using fMRI. Barostat-controlled uncomfortable rectal distensions were preceded by cued uncertain or certain anticipation in 15 healthy volunteers in a fMRI protocol at 3T. Electrocardiographic data were concurrently registered by MR scanner. The low frequency (LF)-component of the heart rate variability (HRV) time-series was extracted and inserted as a regressor in the fMRI model ('LF-HRV model'). The impact of ANS activity was analyzed by comparing the fMRI signal in the 'standard model' and in the 'LF-HRV model' across the different anticipation and distension conditions. The scores of the psychological questionnaires and the rating of perceived anticipatory anxiety were included as covariates in the fMRI data analysis. Our experiments led to the following key findings: 1) the subgenual anterior cingulate cortex (sgACC) is the only activation site that relates to uncertainty in healthy volunteers and is directly correlated to individual questionnaire score for pain-related anxiety; 2) uncertain anticipation of rectal distension involved several relevant brain regions, namely activation of sgACC and medial prefrontal cortex and deactivation of amygdala, insula, thalamus, secondary somatosensory cortex, supplementary motor area and cerebellum; 3) most of the brain activity during anticipation, but not distension, is associated with activity of the central autonomic network. This approach could be applied to study the ANS impact on brain activity in various pathological conditions, namely in patients with chronic digestive conditions characterized by visceral discomfort and ANS imbalance such as irritable bowel syndrome or inflammatory bowel diseases.The human brain responds both before and during the application of aversive stimuli. Anticipation allows the organism to prepare its nociceptive system to respond adequately to the subsequent stimulus. The context in which an uncomfortable stimulus is experienced may also influence neural processing. Uncertainty of occurrence, timing and intensity of an aversive event may lead to increased anticipatory anxiety, fear, physiological arousal and sensory perception. We aimed to identify, in healthy volunteers, the effects of uncertainty in the anticipation of uncomfortable rectal distension, and the impact of the autonomic nervous system (ANS) activity and anxiety-related psychological variables on neural mechanisms of anticipation of rectal distension using fMRI. Barostat-controlled uncomfortable rectal distensions were preceded by cued uncertain or certain anticipation in 15 healthy volunteers in a fMRI protocol at 3T. Electrocardiographic data were concurrently registered by MR scanner. The low frequency (LF)-component of the heart rate variability (HRV) time-series was extracted and inserted as a regressor in the fMRI model ('LF-HRV model'). The impact of ANS activity was analyzed by comparing the fMRI signal in the 'standard model' and in the 'LF-HRV model' across the different anticipation and distension conditions. The scores of the psychological questionnaires and the rating of perceived anticipatory anxiety were included as covariates in the fMRI data analysis. Our experiments led to the following key findings: 1) the subgenual anterior cingulate cortex (sgACC) is the only activation site that relates to uncertainty in healthy volunteers and is directly correlated to individual questionnaire score for pain-related anxiety; 2) uncertain anticipation of rectal distension involved several relevant brain regions, namely activation of sgACC and medial prefrontal cortex and deactivation of amygdala, insula, thalamus, secondary somatosensory cortex, supplementary motor area and cerebellum; 3) most of the brain activity during anticipation, but not distension, is associated with activity of the central autonomic network. This approach could be applied to study the ANS impact on brain activity in various pathological conditions, namely in patients with chronic digestive conditions characterized by visceral discomfort and ANS imbalance such as irritable bowel syndrome or inflammatory bowel diseases. The human brain responds both before and during the application of aversive stimuli. Anticipation allows the organism to prepare its nociceptive system to respond adequately to the subsequent stimulus. The context in which an uncomfortable stimulus is experienced may also influence neural processing. Uncertainty of occurrence, timing and intensity of an aversive event may lead to increased anticipatory anxiety, fear, physiological arousal and sensory perception. We aimed to identify, in healthy volunteers, the effects of uncertainty in the anticipation of uncomfortable rectal distension, and the impact of the autonomic nervous system (ANS) activity and anxiety-related psychological variables on neural mechanisms of anticipation of rectal distension using fMRI. Barostat-controlled uncomfortable rectal distensions were preceded by cued uncertain or certain anticipation in 15 healthy volunteers in a fMRI protocol at 3T. Electrocardiographic data were concurrently registered by MR scanner. The low frequency (LF)-component of the heart rate variability (HRV) time-series was extracted and inserted as a regressor in the fMRI model (‘LF-HRV model’). The impact of ANS activity was analyzed by comparing the fMRI signal in the ‘standard model’ and in the ‘LF-HRV model’ across the different anticipation and distension conditions. The scores of the psychological questionnaires and the rating of perceived anticipatory anxiety were included as covariates in the fMRI data analysis. Our experiments led to the following key findings: 1) the subgenual anterior cingulate cortex (sgACC) is the only activation site that relates to uncertainty in healthy volunteers and is directly correlated to individual questionnaire score for pain-related anxiety; 2) uncertain anticipation of rectal distension involved several relevant brain regions, namely activation of sgACC and medial prefrontal cortex and deactivation of amygdala, insula, thalamus, secondary somatosensory cortex, supplementary motor area and cerebellum; 3) most of the brain activity during anticipation, but not distension, is associated with activity of the central autonomic network. This approach could be applied to study the ANS impact on brain activity in various pathological conditions, namely in patients with chronic digestive conditions characterized by visceral discomfort and ANS imbalance such as irritable bowel syndrome or inflammatory bowel diseases. •sgACC is the only activation site that relates to uncertainty, in healthy subjects.•sgACC activation during uncertainty is correlated to individual pain-related anxiety.•Uncertain anticipation involves activation of sgACC-MPFC and amygdala deactivation.•Brain activity during anticipation reflects central autonomic network activity. |
Author | Ly, Huynh Giao Van Oudenhove, Lukas Dantzer, Cécile Rubio, Amandine Pellissier, Sonia Lafaye de Micheaux, Hugo Dupont, Patrick Delon-Martin, Chantal Tack, Jan Bonaz, Bruno |
Author_xml | – sequence: 1 givenname: Amandine surname: Rubio fullname: Rubio, Amandine email: arubio@chu-grenoble.fr organization: INSERM, U836, F-38000 Grenoble, France – sequence: 2 givenname: Lukas surname: Van Oudenhove fullname: Van Oudenhove, Lukas organization: University Psychiatric Centre, Liaison Psychiatry, University Hospital Gasthuisberg, B-3000 Leuven, Belgium – sequence: 3 givenname: Sonia surname: Pellissier fullname: Pellissier, Sonia organization: INSERM, U836, F-38000 Grenoble, France – sequence: 4 givenname: Huynh Giao surname: Ly fullname: Ly, Huynh Giao organization: Department of Clinical and Experimental Medicine, Translational Research Center for Gastrointestinal Diseases, University of Leuven, B-3000 Leuven, Belgium – sequence: 5 givenname: Patrick surname: Dupont fullname: Dupont, Patrick organization: University Psychiatric Centre, Liaison Psychiatry, University Hospital Gasthuisberg, B-3000 Leuven, Belgium – sequence: 6 givenname: Hugo surname: Lafaye de Micheaux fullname: Lafaye de Micheaux, Hugo organization: INSERM, U836, F-38000 Grenoble, France – sequence: 7 givenname: Jan surname: Tack fullname: Tack, Jan organization: Department of Clinical and Experimental Medicine, Translational Research Center for Gastrointestinal Diseases, University of Leuven, B-3000 Leuven, Belgium – sequence: 8 givenname: Cécile surname: Dantzer fullname: Dantzer, Cécile organization: Univ. Savoie, F-73000 Chambery, France – sequence: 9 givenname: Chantal surname: Delon-Martin fullname: Delon-Martin, Chantal organization: INSERM, U836, F-38000 Grenoble, France – sequence: 10 givenname: Bruno surname: Bonaz fullname: Bonaz, Bruno organization: INSERM, U836, F-38000 Grenoble, France |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25479021$$D View this record in MEDLINE/PubMed https://hal.science/hal-01987074$$DView record in HAL |
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Copyright | 2014 Elsevier Inc. Copyright © 2014 Elsevier Inc. All rights reserved. Copyright Elsevier Limited Feb 15, 2015 Distributed under a Creative Commons Attribution 4.0 International License |
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Keywords | Rectal distension ACC Discomfort Anterior cingulate cortex ANS SMA vmPFC sgACC Anticipation HRV INS CAN HF-HRV fMRI Autonomic nervous system PAG LF-HRV Anxiety S2 |
Language | English |
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Title | Uncertainty in anticipation of uncomfortable rectal distension is modulated by the autonomic nervous system — A fMRI study in healthy volunteers |
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