Active pain coping is associated with the response in real-time fMRI neurofeedback during pain

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Abstract

Real-time functional magnetic resonance imaging (rt-fMRI) neurofeedback is used as a tool to gain voluntary control of activity in various brain regions. Little emphasis has been put on the influence of cognitive and personality traits on neurofeedback efficacy and baseline activity. Here, we assessed the effect of individual pain coping on rt-fMRI neurofeedback during heat-induced pain. Twenty-eight healthy subjects completed the Coping Strategies Questionnaire (CSQ) prior to scanning. The first part of the fMRI experiment identified target regions using painful heat stimulation. Then, subjects were asked to down-regulate the pain target brain region during four neurofeedback runs with painful heat stimulation. Functional MRI analysis included correlation analysis between fMRI activation and pain ratings as well as CSQ ratings. At the behavioral level, the active pain coping (first principal component of CSQ) was correlated with pain ratings during neurofeedback. Concerning neuroimaging, pain sensitive regions were negatively correlated with pain coping. During neurofeedback, the pain coping was positively correlated with activation in the anterior cingulate cortex, prefrontal cortex, hippocampus and visual cortex. Thermode temperature was negatively correlated with anterior insula and dorsolateral prefrontal cortex activation. In conclusion, self-reported pain coping mechanisms and pain sensitivity are a source of variance during rt-fMRI neurofeedback possibly explaining variations in regulation success. In particular, active coping seems to be associated with successful pain regulation.

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Most cited references 43

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Functional imaging of brain responses to pain. A review and meta-analysis (2000).

R Peyron, L García-Larrea, B Laurent (2000)

Brain responses to pain, assessed through positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) are reviewed. Functional activation of brain regions are thought to be reflected by increases in the regional cerebral blood flow (rCBF) in PET studies, and in the blood oxygen level dependent (BOLD) signal in fMRI. rCBF increases to noxious stimuli are almost constantly observed in second somatic (SII) and insular regions, and in the anterior cingulate cortex (ACC), and with slightly less consistency in the contralateral thalamus and the primary somatic area (SI). Activation of the lateral thalamus, SI, SII and insula are thought to be related to the sensory-discriminative aspects of pain processing. SI is activated in roughly half of the studies, and the probability of obtaining SI activation appears related to the total amount of body surface stimulated (spatial summation) and probably also by temporal summation and attention to the stimulus. In a number of studies, the thalamic response was bilateral, probably reflecting generalised arousal in reaction to pain. ACC does not seem to be involved in coding stimulus intensity or location but appears to participate in both the affective and attentional concomitants of pain sensation, as well as in response selection. ACC subdivisions activated by painful stimuli partially overlap those activated in orienting and target detection tasks, but are distinct from those activated in tests involving sustained attention (Stroop, etc.). In addition to ACC, increased blood flow in the posterior parietal and prefrontal cortices is thought to reflect attentional and memory networks activated by noxious stimulation. Less noted but frequent activation concerns motor-related areas such as the striatum, cerebellum and supplementary motor area, as well as regions involved in pain control such as the periaqueductal grey. In patients, chronic spontaneous pain is associated with decreased resting rCBF in contralateral thalamus, which may be reverted by analgesic procedures. Abnormal pain evoked by innocuous stimuli (allodynia) has been associated with amplification of the thalamic, insular and SII responses, concomitant to a paradoxical CBF decrease in ACC. It is argued that imaging studies of allodynia should be encouraged in order to understand central reorganisations leading to abnormal cortical pain processing. A number of brain areas activated by acute pain, particularly the thalamus and anterior cingulate, also show increases in rCBF during analgesic procedures. Taken together, these data suggest that hemodynamic responses to pain reflect simultaneously the sensory, cognitive and affective dimensions of pain, and that the same structure may both respond to pain and participate in pain control. The precise biochemical nature of these mechanisms remains to be investigated.

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Pain catastrophizing and neural responses to pain among persons with fibromyalgia.

R Gracely, M Geisser, T. Giesecke … (2004)

Pain catastrophizing, or characterizations of pain as awful, horrible and unbearable, is increasingly being recognized as an important factor in the experience of pain. The purpose of this investigation was to examine the association between catastrophizing, as measured by the Coping Strategies Questionnaire Catastrophizing Subscale, and brain responses to blunt pressure assessed by functional MRI among 29 subjects with fibromyalgia. Since catastrophizing has been suggested to augment pain perception through enhanced attention to painful stimuli, and heightened emotional responses to pain, we hypothesized that catastrophizing would be positively associated with activation in structures believed to be involved in these aspects of pain processing. As catastrophizing is also strongly associated with depression, the influence of depressive symptomatology was statistically removed. Residual scores of catastrophizing controlling for depressive symptomatology were significantly associated with increased activity in the ipsilateral claustrum (r = 0.51, P < 0.05), cerebellum (r = 0.43, P < 0.05), dorsolateral prefrontal cortex (r = 0.47, P < 0.05), and parietal cortex (r = 0.41, P < 0.05), and in the contralateral dorsal anterior cingulate gyrus (ACC; r = 0.43, P < 0.05), dorsolateral prefrontal cortex (r = 0.41, P < 0.05), medial frontal cortex (r = 0.40, P < 0.05) and lentiform nuclei (r = 0.40, P < 0.05). Analysis of subjects classified as high or low catastrophizers, based on a median split of residual catastrophizing scores, showed that both groups displayed significant increases in ipsilateral secondary somatosensory cortex (SII), although the magnitude of activation was twice as large among high catastrophizers. Both groups also had significant activations in contralateral insula, SII, primary somatosensory cortex (SI), inferior parietal lobule and thalamus. High catastrophizers displayed unique activation in the contralateral anterior ACC, and the contralateral and ipsilateral lentiform. Both groups also displayed significant ipsilateral activation in SI, anterior and posterior cerebellum, posterior cingulate gyrus, and superior and inferior frontal gyrus. These findings suggest that pain catastrophizing, independent of the influence of depression, is significantly associated with increased activity in brain areas related to anticipation of pain (medial frontal cortex, cerebellum), attention to pain (dorsal ACC, dorsolateral prefrontal cortex), emotional aspects of pain (claustrum, closely connected to amygdala) and motor control. These results support the hypothesis that catastrophizing influences pain perception through altering attention and anticipation, and heightening emotional responses to pain. Activation associated with catastrophizing in motor areas of the brain may reflect expressive responses to pain that are associated with greater pain catastrophizing.

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Control over brain activation and pain learned by using real-time functional MRI.

R Christopher deCharms, Fumiko Maeda, Gary H Glover … (2005)

If an individual can learn to directly control activation of localized regions within the brain, this approach might provide control over the neurophysiological mechanisms that mediate behavior and cognition and could potentially provide a different route for treating disease. Control over the endogenous pain modulatory system is a particularly important target because it could enable a unique mechanism for clinical control over pain. Here, we found that by using real-time functional MRI (rtfMRI) to guide training, subjects were able to learn to control activation in the rostral anterior cingulate cortex (rACC), a region putatively involved in pain perception and regulation. When subjects deliberately induced increases or decreases in rACC fMRI activation, there was a corresponding change in the perception of pain caused by an applied noxious thermal stimulus. Control experiments demonstrated that this effect was not observed after similar training conducted without rtfMRI information, or using rtfMRI information derived from a different brain region, or sham rtfMRI information derived previously from a different subject. Chronic pain patients were also trained to control activation in rACC and reported decreases in the ongoing level of chronic pain after training. These findings show that individuals can gain voluntary control over activation in a specific brain region given appropriate training, that voluntary control over activation in rACC leads to control over pain perception, and that these effects were powerful enough to impact severe, chronic clinical pain.

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Author and article information

Contributors

Kirsten Emmert: +41 78 78 452 89 , emmert.kirsten@gmail.com

Journal

Journal ID (nlm-ta): Brain Imaging Behav

Journal ID (iso-abbrev): Brain Imaging Behav

Title: Brain Imaging and Behavior

Publisher: Springer US (New York )

ISSN (Print): 1931-7557

ISSN (Electronic): 1931-7565

Publication date (Electronic): 12 April 2016

Publication date PMC-release: 12 April 2016

Publication date (Print): 2017

Volume: 11

Issue: 3

Pages: 712-721

Affiliations

[1 ]ISNI 0000 0001 0721 9812, GRID grid.150338.c, , Department of Radiology and Medical Informatics, CIBM, University Hospital Geneva, Gabrielle-Perret-Gentil 4, ; 1205 Geneva, Switzerland

[2 ]ISNI 0000000121839049, GRID grid.5333.6, Medical Image Processing Laboratory, Institute of Bioengineering, , Ecole Polytechnique Fédérale de Lausanne (EPFL), ; Lausanne, Switzerland

[3 ]GRID grid.410607.4, Department of Neurology, , University Medical Center of the Johannes Gutenberg-University Mainz, ; Mainz, Germany

[4 ]GRID grid.410607.4, Institute of Neuroradiology, , University Medical Center of the Johannes Gutenberg-University Mainz, ; Mainz, Germany

[5 ]Affidea Centre de Diagnostic Radiologique de Carouge CDRC, Geneva, Switzerland

[6 ]ISNI 0000 0001 2322 4988, GRID grid.8591.5, , Faculty of Medicine of the University of Geneva, ; Geneva, Switzerland

[7 ]ISNI 0000 0004 1936 9457, GRID grid.8993.b, Department of Surgical Sciences, Radiology, , Uppsala University, ; Uppsala, Sweden

[8 ]ISNI 0000 0000 9428 7911, GRID grid.7708.8, Department of Neuroradiology, , University Hospital Freiburg, ; Freiburg im Breisgau, Germany

Article

Publisher ID: 9547

DOI: 10.1007/s11682-016-9547-0

PMC ID: 5486591

PubMed ID: 27071949

SO-VID: 2f157a89-1cb8-47c2-8ffb-91044f1069f0

License:

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

History

Funding

Funded by: Swiss National Science Foundation

Award ID: 320030_147126/1

Award ID: PP00P2-146318

Award Recipient : Kirsten Emmert

Funded by: Stiftung Rheinland-Pfalz

Award ID: Project 936

Award Recipient : Markus Breimhorst

Custom metadata

ScienceOpen disciplines: Radiology & Imaging

Keywords: real-time fmri,neurofeedback,fmri,pain,pain coping,csq

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ScienceOpen disciplines: Radiology & Imaging

Keywords: real-time fmri, neurofeedback, fmri, pain, pain coping, csq

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Active pain coping is associated with the response in real-time fMRI neurofeedback during pain

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Abstract

Electronic supplementary material

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Probing cerebral hemodynamics with BOLD fMRI

Most cited references 43

Functional imaging of brain responses to pain. A review and meta-analysis (2000).

Pain catastrophizing and neural responses to pain among persons with fibromyalgia.

Control over brain activation and pain learned by using real-time functional MRI.

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Cited by 14

Most referenced authors 511