Anticipation and violated expectation of pain are influenced by trait rumination: An fMRI study

Gyongyi Kokonyei, Attila Galambos, Andrea Edit Edes, Natalia Kocsel, Edina Szabo, Dorottya Pap, Lajos R. Kozak, Gyorgy Bagdy, G. Juhász

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

Rumination – as a stable tendency to focus repetitively on feelings related to distress – represents a transdiagnostic risk factor. Theories suggest altered emotional information processing as the key mechanism of rumination. However, studies on the anticipation processes in relation to rumination are scarce, even though expectation in this process is demonstrated to influence the processing of emotional stimuli. In addition, no published study has investigated violated expectation in relation to rumination yet. In the present study we examined the neural correlates of pain anticipation and perception using a fear conditioning paradigm with pain as the unconditioned stimulus in healthy subjects (N = 30). Rumination was assessed with the 10-item Ruminative Response Scale (RRS). Widespread brain activation – extending to temporal, parietal, and occipital lobes along with activation in the cingulate cortex, insula, and putamen – showed a positive correlation with rumination, supporting our hypothesis that trait rumination influences anticipatory processes. Interestingly, with violated expectation (when an unexpected, non-painful stimulus follows a pain cue compared to when an expected, painful stimulus follows the same pain cue) a negative association between rumination and activation was found in the posterior cingulate cortex, which is responsible for change detection in the environment and subsequent behavioral modification. Our results suggest that rumination is associated with increased neural response to pain perception and pain anticipation, and may deteriorate the identification of an unexpected omission of aversive stimuli. Therefore, targeting rumination in cognitive behavioral therapy of chronic pain could have a beneficial effect.

Original languageEnglish
JournalCognitive, Affective and Behavioral Neuroscience
DOIs
Publication statusAccepted/In press - Jan 1 2018

Fingerprint

Magnetic Resonance Imaging
Pain
Pain Perception
Gyrus Cinguli
Cues
Occipital Lobe
Parietal Lobe
Putamen
Cognitive Therapy
Temporal Lobe
Automatic Data Processing
Chronic Pain
Fear
Healthy Volunteers
Emotions
Brain

Keywords

  • Conditioning
  • Expectation
  • fMRI
  • Pain anticipation
  • Rumination
  • Violation

ASJC Scopus subject areas

  • Cognitive Neuroscience
  • Behavioral Neuroscience

Cite this

Anticipation and violated expectation of pain are influenced by trait rumination : An fMRI study. / Kokonyei, Gyongyi; Galambos, Attila; Edes, Andrea Edit; Kocsel, Natalia; Szabo, Edina; Pap, Dorottya; Kozak, Lajos R.; Bagdy, Gyorgy; Juhász, G.

In: Cognitive, Affective and Behavioral Neuroscience, 01.01.2018.

Research output: Contribution to journalArticle

Kokonyei, Gyongyi ; Galambos, Attila ; Edes, Andrea Edit ; Kocsel, Natalia ; Szabo, Edina ; Pap, Dorottya ; Kozak, Lajos R. ; Bagdy, Gyorgy ; Juhász, G. / Anticipation and violated expectation of pain are influenced by trait rumination : An fMRI study. In: Cognitive, Affective and Behavioral Neuroscience. 2018.
@article{7b1da647b9914b5bbd2aef99b8338e82,
title = "Anticipation and violated expectation of pain are influenced by trait rumination: An fMRI study",
abstract = "Rumination – as a stable tendency to focus repetitively on feelings related to distress – represents a transdiagnostic risk factor. Theories suggest altered emotional information processing as the key mechanism of rumination. However, studies on the anticipation processes in relation to rumination are scarce, even though expectation in this process is demonstrated to influence the processing of emotional stimuli. In addition, no published study has investigated violated expectation in relation to rumination yet. In the present study we examined the neural correlates of pain anticipation and perception using a fear conditioning paradigm with pain as the unconditioned stimulus in healthy subjects (N = 30). Rumination was assessed with the 10-item Ruminative Response Scale (RRS). Widespread brain activation – extending to temporal, parietal, and occipital lobes along with activation in the cingulate cortex, insula, and putamen – showed a positive correlation with rumination, supporting our hypothesis that trait rumination influences anticipatory processes. Interestingly, with violated expectation (when an unexpected, non-painful stimulus follows a pain cue compared to when an expected, painful stimulus follows the same pain cue) a negative association between rumination and activation was found in the posterior cingulate cortex, which is responsible for change detection in the environment and subsequent behavioral modification. Our results suggest that rumination is associated with increased neural response to pain perception and pain anticipation, and may deteriorate the identification of an unexpected omission of aversive stimuli. Therefore, targeting rumination in cognitive behavioral therapy of chronic pain could have a beneficial effect.",
keywords = "Conditioning, Expectation, fMRI, Pain anticipation, Rumination, Violation",
author = "Gyongyi Kokonyei and Attila Galambos and Edes, {Andrea Edit} and Natalia Kocsel and Edina Szabo and Dorottya Pap and Kozak, {Lajos R.} and Gyorgy Bagdy and G. Juh{\'a}sz",
year = "2018",
month = "1",
day = "1",
doi = "10.3758/s13415-018-0644-y",
language = "English",
journal = "Cognitive, Affective and Behavioral Neuroscience",
issn = "1530-7026",
publisher = "Springer New York",

}

TY - JOUR

T1 - Anticipation and violated expectation of pain are influenced by trait rumination

T2 - An fMRI study

AU - Kokonyei, Gyongyi

AU - Galambos, Attila

AU - Edes, Andrea Edit

AU - Kocsel, Natalia

AU - Szabo, Edina

AU - Pap, Dorottya

AU - Kozak, Lajos R.

AU - Bagdy, Gyorgy

AU - Juhász, G.

PY - 2018/1/1

Y1 - 2018/1/1

N2 - Rumination – as a stable tendency to focus repetitively on feelings related to distress – represents a transdiagnostic risk factor. Theories suggest altered emotional information processing as the key mechanism of rumination. However, studies on the anticipation processes in relation to rumination are scarce, even though expectation in this process is demonstrated to influence the processing of emotional stimuli. In addition, no published study has investigated violated expectation in relation to rumination yet. In the present study we examined the neural correlates of pain anticipation and perception using a fear conditioning paradigm with pain as the unconditioned stimulus in healthy subjects (N = 30). Rumination was assessed with the 10-item Ruminative Response Scale (RRS). Widespread brain activation – extending to temporal, parietal, and occipital lobes along with activation in the cingulate cortex, insula, and putamen – showed a positive correlation with rumination, supporting our hypothesis that trait rumination influences anticipatory processes. Interestingly, with violated expectation (when an unexpected, non-painful stimulus follows a pain cue compared to when an expected, painful stimulus follows the same pain cue) a negative association between rumination and activation was found in the posterior cingulate cortex, which is responsible for change detection in the environment and subsequent behavioral modification. Our results suggest that rumination is associated with increased neural response to pain perception and pain anticipation, and may deteriorate the identification of an unexpected omission of aversive stimuli. Therefore, targeting rumination in cognitive behavioral therapy of chronic pain could have a beneficial effect.

AB - Rumination – as a stable tendency to focus repetitively on feelings related to distress – represents a transdiagnostic risk factor. Theories suggest altered emotional information processing as the key mechanism of rumination. However, studies on the anticipation processes in relation to rumination are scarce, even though expectation in this process is demonstrated to influence the processing of emotional stimuli. In addition, no published study has investigated violated expectation in relation to rumination yet. In the present study we examined the neural correlates of pain anticipation and perception using a fear conditioning paradigm with pain as the unconditioned stimulus in healthy subjects (N = 30). Rumination was assessed with the 10-item Ruminative Response Scale (RRS). Widespread brain activation – extending to temporal, parietal, and occipital lobes along with activation in the cingulate cortex, insula, and putamen – showed a positive correlation with rumination, supporting our hypothesis that trait rumination influences anticipatory processes. Interestingly, with violated expectation (when an unexpected, non-painful stimulus follows a pain cue compared to when an expected, painful stimulus follows the same pain cue) a negative association between rumination and activation was found in the posterior cingulate cortex, which is responsible for change detection in the environment and subsequent behavioral modification. Our results suggest that rumination is associated with increased neural response to pain perception and pain anticipation, and may deteriorate the identification of an unexpected omission of aversive stimuli. Therefore, targeting rumination in cognitive behavioral therapy of chronic pain could have a beneficial effect.

KW - Conditioning

KW - Expectation

KW - fMRI

KW - Pain anticipation

KW - Rumination

KW - Violation

UR - http://www.scopus.com/inward/record.url?scp=85053830548&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85053830548&partnerID=8YFLogxK

U2 - 10.3758/s13415-018-0644-y

DO - 10.3758/s13415-018-0644-y

M3 - Article

C2 - 30251186

AN - SCOPUS:85053830548

JO - Cognitive, Affective and Behavioral Neuroscience

JF - Cognitive, Affective and Behavioral Neuroscience

SN - 1530-7026

ER -