Effect of spinal anesthesia-induced deafferentation on pain processing in healthy male volunteers: A task-related fMRI study

BackgroundSpinal anesthesia causes short-term deafferentation and alters the crosstalk among brain regions involved in pain perception and pain modulation. In the current study, we examined the effect of spinal anesthesia on pain response to noxious thermal stimuli in non-deafferented skin areas usi...

Full description

Bibliographic Details
Main Authors: Elske Sitsen, Najmeh Khalili-Mahani, Mischa de Rover, Albert Dahan, Marieke Niesters
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-11-01
Series:Frontiers in Pain Research
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpain.2022.1001148/full
_version_ 1811211401511829504
author Elske Sitsen
Najmeh Khalili-Mahani
Mischa de Rover
Mischa de Rover
Albert Dahan
Marieke Niesters
author_facet Elske Sitsen
Najmeh Khalili-Mahani
Mischa de Rover
Mischa de Rover
Albert Dahan
Marieke Niesters
author_sort Elske Sitsen
collection DOAJ
description BackgroundSpinal anesthesia causes short-term deafferentation and alters the crosstalk among brain regions involved in pain perception and pain modulation. In the current study, we examined the effect of spinal anesthesia on pain response to noxious thermal stimuli in non-deafferented skin areas using a functional magnetic resonance imaging (fMRI) paradigm.MethodsTwenty-two healthy subjects participated in the study. We performed a task-based fMRI study using a randomized crossover design. Subjects were scanned under two conditions (spinal anesthesia or control) at two-time points: before and after spinal anesthesia. Spinal anesthesia resulted in sensory loss up to dermatome Th6. Calibrated heat-pain stimuli were administered to the right forearm (C8-Th1) using a box-car design (blocks of 10s on/25s off) during MRI scanning. Pain perception was measured using a visual analogue scale (1–100) at the beginning and the end of each session. Generalized estimating equations were used to examine the effect of intervention by time by order on pain scores. Similarly, higher-level effects were tested with appropriate general linear models (accounting for within-subject variations in session and time) to examine: (1) Differences in BOLD response to pain stimulus under spinal anesthesia versus control; and (2) Effects of spinal anesthesia on pain-related modulation of the cerebral activation.ResultsComplete fMRI data was available for eighteen participants. Spinal anesthesia was associated with moderate pain score increase. Significant differences in brain response to noxious thermal stimuli were present in comparison of spinal versus control condition (post—pre). Spinal condition was associated with higher BOLD signal in the bilateral inferior parietal lobule and lower BOLD signal in bilateral postcentral and precentral gyrus. Within the angular regions, we observed a positive correlation between pain scores and BOLD signal. These observations were independent from order effect (whether the spinal anesthesia was administered in the first or the second visit). However, we did observe order effect on brain regions including medial prefrontal regions, possibly related to anticipation of the experience of spinal anesthesia.ConclusionsThe loss of sensory and motor activity caused by spinal anesthesia has a significant impact on brain regions involved in the sensorimotor and cognitive processing of noxious heat pain stimuli. Our results indicate that the anticipation or experience of a strong somatosensory response to the spinal intervention might confound and contribute to increased sensitivity to cognitive pain processing. Future studies must account for individual differences in subjective experience of pain sensation within the experimental context.
first_indexed 2024-04-12T05:13:45Z
format Article
id doaj.art-4c0930ff70c941c68c978f4dd6eeb0ba
institution Directory Open Access Journal
issn 2673-561X
language English
last_indexed 2024-04-12T05:13:45Z
publishDate 2022-11-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Pain Research
spelling doaj.art-4c0930ff70c941c68c978f4dd6eeb0ba2022-12-22T03:46:42ZengFrontiers Media S.A.Frontiers in Pain Research2673-561X2022-11-01310.3389/fpain.2022.10011481001148Effect of spinal anesthesia-induced deafferentation on pain processing in healthy male volunteers: A task-related fMRI studyElske Sitsen0Najmeh Khalili-Mahani1Mischa de Rover2Mischa de Rover3Albert Dahan4Marieke Niesters5Department of Anesthesiology, Leiden University Medical Center, Leiden, NetherlandsMcGill Centre for Integrative Neuroscience, Montreal Neurological Institute, McGill University, Montreal, QC, CanadaDepartment of Clinical Psychology, Institute of Psychology, Leiden University, Leiden, NetherlandsLeiden Institute of Brain and Cognition, Leiden, NetherlandsDepartment of Anesthesiology, Leiden University Medical Center, Leiden, NetherlandsDepartment of Anesthesiology, Leiden University Medical Center, Leiden, NetherlandsBackgroundSpinal anesthesia causes short-term deafferentation and alters the crosstalk among brain regions involved in pain perception and pain modulation. In the current study, we examined the effect of spinal anesthesia on pain response to noxious thermal stimuli in non-deafferented skin areas using a functional magnetic resonance imaging (fMRI) paradigm.MethodsTwenty-two healthy subjects participated in the study. We performed a task-based fMRI study using a randomized crossover design. Subjects were scanned under two conditions (spinal anesthesia or control) at two-time points: before and after spinal anesthesia. Spinal anesthesia resulted in sensory loss up to dermatome Th6. Calibrated heat-pain stimuli were administered to the right forearm (C8-Th1) using a box-car design (blocks of 10s on/25s off) during MRI scanning. Pain perception was measured using a visual analogue scale (1–100) at the beginning and the end of each session. Generalized estimating equations were used to examine the effect of intervention by time by order on pain scores. Similarly, higher-level effects were tested with appropriate general linear models (accounting for within-subject variations in session and time) to examine: (1) Differences in BOLD response to pain stimulus under spinal anesthesia versus control; and (2) Effects of spinal anesthesia on pain-related modulation of the cerebral activation.ResultsComplete fMRI data was available for eighteen participants. Spinal anesthesia was associated with moderate pain score increase. Significant differences in brain response to noxious thermal stimuli were present in comparison of spinal versus control condition (post—pre). Spinal condition was associated with higher BOLD signal in the bilateral inferior parietal lobule and lower BOLD signal in bilateral postcentral and precentral gyrus. Within the angular regions, we observed a positive correlation between pain scores and BOLD signal. These observations were independent from order effect (whether the spinal anesthesia was administered in the first or the second visit). However, we did observe order effect on brain regions including medial prefrontal regions, possibly related to anticipation of the experience of spinal anesthesia.ConclusionsThe loss of sensory and motor activity caused by spinal anesthesia has a significant impact on brain regions involved in the sensorimotor and cognitive processing of noxious heat pain stimuli. Our results indicate that the anticipation or experience of a strong somatosensory response to the spinal intervention might confound and contribute to increased sensitivity to cognitive pain processing. Future studies must account for individual differences in subjective experience of pain sensation within the experimental context.https://www.frontiersin.org/articles/10.3389/fpain.2022.1001148/fulldeafferentationpainspinal anesthesiatask-related fMRIsensorimotor cortexinferior parietal lobule
spellingShingle Elske Sitsen
Najmeh Khalili-Mahani
Mischa de Rover
Mischa de Rover
Albert Dahan
Marieke Niesters
Effect of spinal anesthesia-induced deafferentation on pain processing in healthy male volunteers: A task-related fMRI study
Frontiers in Pain Research
deafferentation
pain
spinal anesthesia
task-related fMRI
sensorimotor cortex
inferior parietal lobule
title Effect of spinal anesthesia-induced deafferentation on pain processing in healthy male volunteers: A task-related fMRI study
title_full Effect of spinal anesthesia-induced deafferentation on pain processing in healthy male volunteers: A task-related fMRI study
title_fullStr Effect of spinal anesthesia-induced deafferentation on pain processing in healthy male volunteers: A task-related fMRI study
title_full_unstemmed Effect of spinal anesthesia-induced deafferentation on pain processing in healthy male volunteers: A task-related fMRI study
title_short Effect of spinal anesthesia-induced deafferentation on pain processing in healthy male volunteers: A task-related fMRI study
title_sort effect of spinal anesthesia induced deafferentation on pain processing in healthy male volunteers a task related fmri study
topic deafferentation
pain
spinal anesthesia
task-related fMRI
sensorimotor cortex
inferior parietal lobule
url https://www.frontiersin.org/articles/10.3389/fpain.2022.1001148/full
work_keys_str_mv AT elskesitsen effectofspinalanesthesiainduceddeafferentationonpainprocessinginhealthymalevolunteersataskrelatedfmristudy
AT najmehkhalilimahani effectofspinalanesthesiainduceddeafferentationonpainprocessinginhealthymalevolunteersataskrelatedfmristudy
AT mischaderover effectofspinalanesthesiainduceddeafferentationonpainprocessinginhealthymalevolunteersataskrelatedfmristudy
AT mischaderover effectofspinalanesthesiainduceddeafferentationonpainprocessinginhealthymalevolunteersataskrelatedfmristudy
AT albertdahan effectofspinalanesthesiainduceddeafferentationonpainprocessinginhealthymalevolunteersataskrelatedfmristudy
AT mariekeniesters effectofspinalanesthesiainduceddeafferentationonpainprocessinginhealthymalevolunteersataskrelatedfmristudy