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 inNeuroImage (Orlando, Fla.) Vol. 107; pp. 10 - 22
Main Authors Rubio, Amandine, Van Oudenhove, Lukas, Pellissier, Sonia, Ly, Huynh Giao, Dupont, Patrick, Lafaye de Micheaux, Hugo, Tack, Jan, Dantzer, Cécile, Delon-Martin, Chantal, Bonaz, Bruno
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 15.02.2015
Elsevier Limited
Elsevier
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Online AccessGet full text
ISSN1053-8119
1095-9572
1095-9572
DOI10.1016/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.
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
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/25479021$$D View this record in MEDLINE/PubMed
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IEDL.DBID 7X7
ISSN 1053-8119
1095-9572
IngestDate Sun Sep 28 07:53:33 EDT 2025
Sun Sep 28 01:00:53 EDT 2025
Sun Sep 28 06:19:08 EDT 2025
Sat Sep 27 18:54:53 EDT 2025
Wed Aug 13 05:59:11 EDT 2025
Sat Aug 23 13:05:46 EDT 2025
Fri Mar 21 18:56:19 EDT 2025
Tue Jul 01 03:01:40 EDT 2025
Thu Apr 24 22:56:43 EDT 2025
Tue Aug 26 16:31:52 EDT 2025
IsPeerReviewed true
IsScholarly true
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
License Copyright © 2014 Elsevier Inc. All rights reserved.
Distributed under a Creative Commons Attribution 4.0 International License: http://creativecommons.org/licenses/by/4.0
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Snippet The human brain responds both before and during the application of aversive stimuli. Anticipation allows the organism to prepare its nociceptive system to...
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SubjectTerms Activation
Adult
Amygdala
Anterior cingulate cortex
Anticipation
Anticipation, Psychological - physiology
Anticipatory
Anxiety
Anxiety - psychology
Arousal
Autonomic nervous system
Autonomic Nervous System - physiology
Brain
Brain - physiology
Brain mapping
Cerebellum
Chronic illnesses
Cognitive science
Cortex (cingulate)
Cortex (motor)
Cortex (somatosensory)
Cortexes
Cues
Data processing
Deactivation
Digestive system
Discomfort
Distension
Electrocardiography
Female
fMRI
Functional magnetic resonance imaging
Gyrus Cinguli - physiology
Healthy Volunteers
Heart rate
Heart Rate - physiology
HRV
Humans
Inflammatory bowel diseases
Information processing
Intestine
Irritable bowel syndrome
Magnetic Resonance Imaging
Male
Medical imaging
Nerve Net - physiology
Nervous system
Neuroscience
Nociception - physiology
Pain
Pain - physiopathology
Pain perception
Physical Stimulation
Prefrontal cortex
Rectal distension
Rectum
Rectum - innervation
Rectum - physiology
Supplementary motor area
Surveys
Task forces
Thalamus
Uncertainty
Young Adult
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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Volume 107
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