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

Peyron, R.; Laurent, B.; García-Larrea, L.

doi:10.1016/s0987-7053(00)00227-6

Cited by 2,171Pain Mechanisms and TreatmentsPain Management and Placebo EffectPain Management and Treatment

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

Peyron, R., Laurent, B., García-Larrea, L.·2000·Neurophysiologie Clinique/Clinical Neurophysiology

DOI 10.1016/s0987-7053(00)00227-6

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Abstract

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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Coactivation of the ACC and anterior insula in imaging experiments is strongly linked to emotional processing and interoceptive awareness.
“Coactivation of the ACC and anterior insula in imaging experiments is strongly linked to emotional processing and introceptive awareness (28, 35, 36).”
From Threatening a rubber hand that you feel is yours elicits a cortical anxiety response. (2007) · cites this paper as [36]
The contrast painful vs non-painful indicated the involvement of large portions of the pain matrix.
“This contrast indicated the involvement of large portions of the pain matrix [29], [30].”
From What are you feeling? Using functional magnetic resonance imaging to assess the modulation of sensory and affective responses during empathy for pain (2007) · cites this paper as [30]

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Cortical Localization of Human Sustained Attention: Detection with Functional MR Using a Visual Vigilance Paradigm
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Thalamic Relay Site for Cold Perception in Humans
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Attention modulates somatosensory cerebral blood flow response to vibrotactile stimulation as measured by positron emission tomography
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Persistent pain inhibits contralateral somatosensory cortical activity in humans
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Anticipation causes increased blood flow to the anterior cingulate cortex
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Functional localization of pain perception in the human brain studied by PET
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Diffusion tensor microscopy of the intervertebral disc anulus fibrosus
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Inhibition of the human primary motor area by painful heat stimulation of the skin
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Human taste cortical areas studied with functional magnetic resonance imaging: evidence of functional lateralization related to handedness
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Stimulation of Human Thalamus for Pain Relief: Possible Modulatory Circuits Revealed by Positron Emission Tomography
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Characterizing the Relationship between BOLD Contrast and Regional Cerebral Blood Flow Measurements by Varying the Stimulus Presentation Rate
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Reversal, by treatment with an aldose reductase inhibitor, of impaired axonal transport and motor nerve conduction velocity in experimental diabetes mellitus
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Spinal afferent processing
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Proceedings of the 8th World Congress on Pain
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Functional imaging of human right hemispheric activation for exploratory movements
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Analgesia produced by injection of lidocaine into the anterior cingulum bundle of the rat
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Affective and attentive neural networks in humans
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Monkey insular cortex neurons respond to baroreceptive and somatosensory convergent inputs
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Attention-induced neuronal activity in the monkey somatosensory cortex revealed by pupillometrics
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Central processing of rectal pain: a functional MR imaging study.
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The Question of How the Dorsal Horn Encodes Sensory Information
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Identifying global anatomical differences: Deformation-based morphometry
(1998) · doi:10.1002/(sici)1097-0193(1998)6:5/6
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Bush (1998) · doi:10.1002/(sici)1097-0193(1998)6:4

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Dissociable intrinsic connectivity networks for salience processing and executive control
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Empathy for Pain Involves the Affective but not Sensory Components of Pain
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Conflict monitoring and anterior cingulate cortex: an update
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Human brain mechanisms of pain perception and regulation in health and disease
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Both of Us Disgusted in My Insula
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The integration of negative affect, pain and cognitive control in the cingulate cortex
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The valuation system: A coordinate-based meta-analysis of BOLD fMRI experiments examining neural correlates of subjective value
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Meta-analytic evidence for common and distinct neural networks associated with directly experienced pain and empathy for pain
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Coordinate‐based activation likelihood estimation meta‐analysis of neuroimaging data: A random‐effects approach based on empirical estimates of spatial uncertainty
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Placebo-Induced Changes in fMRI in the Anticipation and Experience of Pain
Wager, T. D., Rilling, J. K., Smith, E. E., Sokolik, A., Casey, K. L., Davidson, R. J., Kosslyn, S. M., Rose, R. M., & Cohen, J. D. (2004) · Science · doi:10.1126/science.1093065 · Cited by 1,992 · see citing works
Social Cognitive Neuroscience: A Review of Core Processes
Lieberman, M. D. (2007) · Annual Review of Psychology · doi:10.1146/annurev.psych.58.110405.085654 · Cited by 2,010 · see citing works
The neural basis of error detection: Conflict monitoring and the error-related negativity
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“Thereafter, the SN shows involvement not only in cognitively demanding tasks such as attentional and responseselection paradigms (Menon et al. 2001; Ridderinkhof et al. 2004) but also responds to uncertainty and emotional salience (Peyron et al. 2000; Grinband et al. 2006).”
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Self-citation

Authors: Peyron, R., Laurent, B., & García-Larrea, L.
Affiliations: Centre d'Exploration et de Recherche Médicale par Emission de Positons (FR)
Corresponding author: Peyron, R.
ORCID: Peyron, R.
Laurent, B.
Venue: Neurophysiologie Clinique/Clinical Neurophysiology
Publisher: Elsevier BV
Published: 2000-10
Volume: 30
Issue: 5
Pages: 263-288
ISSN: 0987-7053 (ISSN-L)
DOI: 10.1016/s0987-7053(00)00227-6
OpenAlex: W2025577666
Cited by: 2,171
References: 165
Citations by year: 2026: 27 · 2025: 43 · 2024: 34 · 2023: 50 · 2022: 60 · 2021: 76 · 2020: 95 · 2019: 77 · 2018: 82 · 2017: 94 · 2016: 91 · 2015: 114 · 2014: 84 · 2013: 132 · 2012: 105
FWCI: 19.57
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neurophysiologie Clinique (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Physiology › Pain Mechanisms and Treatments
Life Sciences › Neuroscience › Cognitive Neuroscience › Pain Management and Placebo Effect
Health Sciences › Medicine › Anesthesiology and Pain Medicine › Pain Management and Treatment
Keywords: pain processing, brain activation, regional cerebral blood flow, anterior cingulate cortex, thalamus, insula, spatial summation, temporal summation, allodynia, chronic pain, analgesia, pain management, central sensitization
MeSH terms: Analgesia, Attention, Brain, Brain Mapping, Cerebral Cortex, Cerebrovascular Circulation, Cognition, Emotions, Gyrus Cinguli, Humans, Hyperesthesia, Magnetic Resonance Imaging, Oxygen, Pain, Pain Measurement, Parietal Lobe, Receptors, Opioid, Somatosensory Cortex, Subtraction Technique, Thalamus, Tomography, Emission-Computed, Prefrontal Cortex

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

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