Cognitive modulation of pain-related brain responses depends on behavioral strategy

Abstract Interactions of pain and cognition have been studied in humans and animals previously, but the relationship between such behavioral interactions and brain activity is unknown. We aimed to show using functional MRI (fMRI) how a cognitively demanding task (Stroop) modulates pain‐related brain activations and conversely, how pain modulates attention‐related activity. Reaction time data indicated two types of pain responders: subjects in the A group had a faster Stroop reaction time when pain was concomitant to the attention task, while those in the P group had a slower Stroop performance during painful stimulation. fMRI data obtained during Stroop performance with and without noxious stimulation were subjected to region of interest analyses. We first tested whether brain activity during painful median nerve stimulation was modulated by cognitive load. We next tested whether brain activity during the high conflict cognitive task was modulated by pain. Pain‐related activity in three regions, primary (S1), and secondary (S2) somatosensory cortices, and anterior insula, was attenuated by cognitive engagement, but this effect was specific to the A group. Pain‐related activations in the caudal and rostral anterior cingulate cortex (ACC) and ventroposterior thalamus were not modulated by cognitive load. None of the areas showing attention‐related responses, including bilateral dorsolateral prefrontal and posterior parietal cortices, were modulated by pain. These findings suggest that cortical regions associated with pain can be modulated by cognitive strategies. Furthermore, the distinction of behavioral subgroups may relate to cognitive coping strategies taken by patients with chronic pain.

[1]  Heidi Johansen-Berg,et al.  Attention to touch modulates activity in both primary and secondary somatosensory areas , 2000, NeuroImage.

[2]  Geert Crombez,et al.  Attentional functioning in fibromyalgia, rheumatoid arthritis, and musculoskeletal pain patients. , 2002, Arthritis and rheumatism.

[3]  M. Bushnell,et al.  Task-related responses of monkey medullary dorsal horn neurons. , 1987, Journal of neurophysiology.

[4]  H Burton,et al.  Neuronal activity in the second somatosensory cortex of monkeys (Macaca mulatta) during active touch of gratings. , 1993, Journal of neurophysiology.

[5]  M. Bushnell,et al.  Cortical representation of the sensory dimension of pain. , 2001, Journal of neurophysiology.

[6]  S. Stone-Elander,et al.  Pain-related cerebral activation is altered by a distracting cognitive task , 2000, Pain.

[7]  A. Craig,et al.  Pain mechanisms: labeled lines versus convergence in central processing. , 2003, Annual review of neuroscience.

[8]  Alan C. Evans,et al.  A General Statistical Analysis for fMRI Data , 2000, NeuroImage.

[9]  Karl J. Friston,et al.  Cortical and subcortical localization of response to pain in man using positron emission tomography , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[10]  Stephen M. Smith,et al.  Temporal Autocorrelation in Univariate Linear Modeling of FMRI Data , 2001, NeuroImage.

[11]  R. Dubner,et al.  The effect of behavioral state on the sensory processing of nociceptive and non-nociceptive information. , 1988, Progress in brain research.

[12]  P. Spinhoven,et al.  Cognitive Change following Cognitive Behavioural Therapy for Non-Cardiac Chest Pain , 1999, Psychotherapy and Psychosomatics.

[13]  T. Dalgleish,et al.  The emotional Stroop task and psychopathology. , 1996, Psychological bulletin.

[14]  M. Zeegers,et al.  The modified Stroop paradigm as a measure of selective attention towards pain‐related stimuli among chronic pain patients: a meta‐analysis , 2002, European journal of pain.

[15]  E. Niebur,et al.  Growth patterns in the developing brain detected by using continuum mechanical tensor maps , 2022 .

[16]  A. K. Jones,et al.  Pain mechanisms and their disorders. , 2003, British medical bulletin.

[17]  G. Pagnoni,et al.  Does Anticipation of Pain Affect Cortical Nociceptive Systems? , 2002, The Journal of Neuroscience.

[18]  S S Hsiao,et al.  Effects of selective attention on spatial form processing in monkey primary and secondary somatosensory cortex. , 1993, Journal of neurophysiology.

[19]  D. Hoffman,et al.  Neuronal activity in medullary dorsal horn of awake monkeys trained in a thermal discrimination task. III. Task-related responses and their functional role. , 1981, Journal of neurophysiology.

[20]  Roger Zimmermann,et al.  Attentional modulation of human pain processing in the secondary somatosensory cortex: a magnetoencephalographic study , 2002, Neuroscience Letters.

[21]  N. Costes,et al.  Haemodynamic brain responses to acute pain in humans: sensory and attentional networks. , 1999, Brain : a journal of neurology.

[22]  Ronald Melzack,et al.  From the gate to the neuromatrix , 1999, Pain.

[23]  M. L. Wood,et al.  Functional MRI of pain- and attention-related activations in the human cingulate cortex. , 1997, Journal of neurophysiology.

[24]  Karl J. Friston,et al.  Cerebral responses to pain in patients with atypical facial pain measured by positron emission tomography. , 1994, Journal of neurology, neurosurgery, and psychiatry.

[25]  D. Zurakowski,et al.  Physical therapy and cognitive-behavioral treatment for complex regional pain syndromes. , 2002, The Journal of pediatrics.

[26]  Leslie G. Ungerleider,et al.  Increased Activity in Human Visual Cortex during Directed Attention in the Absence of Visual Stimulation , 1999, Neuron.

[27]  F. Mauguière,et al.  Representation of pain and somatic sensation in the human insula: a study of responses to direct electrical cortical stimulation. , 2002, Cerebral cortex.

[28]  R. Kerns,et al.  Cognitive-behavioral therapy for chronic low back pain in older persons: a preliminary study. , 2003, Pain medicine.

[29]  R. Dowman Attentional set effects on spinal and supraspinal responses to pain. , 2001, Psychophysiology.

[30]  J. Baron,et al.  Overcoming Stroop interference: the effects of practice on distractor potency. , 1980, Journal of experimental psychology. Human perception and performance.

[31]  J. Ridley Studies of Interference in Serial Verbal Reactions , 2001 .

[32]  T. Jessell PAIN , 1982, The Lancet.

[33]  R. Koeppe,et al.  Comparison of human cerebral activation pattern during cutaneous warmth, heat pain, and deep cold pain. , 1996, Journal of neurophysiology.

[34]  Alan C. Evans,et al.  Multiple representations of pain in human cerebral cortex. , 1991, Science.

[35]  M. Catherine Bushnell,et al.  Effects of odors on pain perception: deciphering the roles of emotion and attention , 2003, Pain.

[36]  Ryouhei Ishii,et al.  Parallel distributed processing neuroimaging in the Stroop task using spatially filtered magnetoencephalography analysis , 2002, Neuroscience Letters.

[37]  D. Zald,et al.  Cognitive Impairment in Musculoskeletal Pain Patients , 1991, International journal of psychiatry in medicine.

[38]  H Hämäläinen,et al.  Activation of somatosensory cortical areas varies with attentional state: an fMRI study , 2002, Behavioural Brain Research.

[39]  M. L. Wood,et al.  fMRI of human somatosensory and cingulate cortex during painful electrical nerve stimulation , 1995, Neuroreport.

[40]  M. Bushnell,et al.  Pain perception: is there a role for primary somatosensory cortex? , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[41]  G. Lohmann,et al.  Color-Word Matching Stroop Task: Separating Interference and Response Conflict , 2001, NeuroImage.

[42]  J. Downar,et al.  A cortical network sensitive to stimulus salience in a neutral behavioral context across multiple sensory modalities. , 2002, Journal of neurophysiology.

[43]  Leslie G. Ungerleider,et al.  Mechanisms of directed attention in the human extrastriate cortex as revealed by functional MRI. , 1998, Science.

[44]  Leslie G. Ungerleider,et al.  Attentional control of the processing of neural and emotional stimuli. , 2002, Brain research. Cognitive brain research.

[45]  B. Dick,et al.  The disruptive effect of chronic pain on mismatch negativity , 2003, Clinical Neurophysiology.

[46]  R Dubner,et al.  Activity of trigeminothalamic neurons in medullary dorsal horn of awake monkeys trained in a thermal discrimination task. , 1984, Journal of neurophysiology.

[47]  H. Fields,et al.  Post-operative pain: effect of extent of injury and attention , 1982, Brain Research.

[48]  Jonathan Downar,et al.  Neural correlates of the prolonged salience of painful stimulation , 2003, NeuroImage.

[49]  R. Peyron,et al.  Functional imaging of brain responses to pain. A review and meta-analysis (2000) , 2000, Neurophysiologie Clinique/Clinical Neurophysiology.

[50]  S. Clare,et al.  Imaging how attention modulates pain in humans using functional MRI. , 2002, Brain : a journal of neurology.

[51]  M. Bushnell,et al.  Pain affect encoded in human anterior cingulate but not somatosensory cortex. , 1997, Science.

[52]  M. Bushnell,et al.  Attentional influences on noxious and innocuous cutaneous heat detection in humans and monkeys , 1985 .

[53]  M. Norris,et al.  Active and passive coping strategies in chronic pain patients , 1996, Pain.

[54]  N. Cohen,et al.  The relative involvement of anterior cingulate and prefrontal cortex in attentional control depends on nature of conflict. , 2001, Brain research. Cognitive brain research.

[55]  Richard F. Martin,et al.  Nociceptive responses of trigeminal neurons in SII-7b cortex of awake monkeys , 1989, Brain Research.

[56]  A. Kamanlı,et al.  Auditory P300 event related potentials and serotonin reuptake inhibitor treatment in patients with fibromyalgia , 2003, Annals of the rheumatic diseases.

[57]  J. Downar,et al.  The Effect of Task Relevance on the Cortical Response to Changes in Visual and Auditory Stimuli: An Event-Related fMRI Study , 2001, NeuroImage.

[58]  C. L. Kwan,et al.  Functional MRI study of thalamic and cortical activations evoked by cutaneous heat, cold, and tactile stimuli. , 1998, Journal of neurophysiology.

[59]  E. Chudler,et al.  Somatosensory, multisensory, and task-related neurons in cortical area 7b (PF) of unanesthetized monkeys. , 1994, Journal of neurophysiology.

[60]  R. Gruen,et al.  CognitiveBehavioural Therapy for the Management of Sickle Cell Disease Pain: Identification and Assessment of Costs , 2001, Ethnicity & health.

[61]  S Minoshima,et al.  Temporal and spatial dynamics of human forebrain activity during heat pain: analysis by positron emission tomography. , 2001, Journal of neurophysiology.

[62]  G. Werner,et al.  Symmetry and connectivity in the map of the body surface in somatosensory area II of primates. , 1969, Journal of neurophysiology.

[63]  Colin M. Macleod,et al.  Interdimensional interference in the Stroop effect: uncovering the cognitive and neural anatomy of attention , 2000, Trends in Cognitive Sciences.

[64]  Mark W. Woolrich,et al.  Attention to touch modulates activity in both primary and secondary somatosensory areas. , 2000 .

[65]  Behavioral Specializations of SI and SII Cortex: A Comparative Examination of the Neural Logic of Touch in Rats, Cats, and Other Mammals , 1994, Experimental Neurology.

[66]  M. Bushnell,et al.  Effects of attention on the intensity and unpleasantness of thermal pain , 1989, Pain.

[67]  George Bush,et al.  The emotional counting stroop paradigm: a functional magnetic resonance imaging probe of the anterior cingulate affective division , 1998, Biological Psychiatry.

[68]  Colin M. Macleod Half a century of research on the Stroop effect: an integrative review. , 1991, Psychological bulletin.

[69]  W. Richter,et al.  Distraction Modulates Anterior Cingulate Gyrus Activations during the Cold Pressor Test , 2001, NeuroImage.

[70]  G. Crombez,et al.  Attention and somatic awareness in chronic pain , 1997, PAIN.

[71]  K. Mccaul,et al.  Attention, distraction, and cold-pressor pain. , 1982, Journal of Personality and Social Psychology.

[72]  Ravi S. Menon,et al.  Imaging Attentional Modulation of Pain in the Periaqueductal Gray in Humans , 2002, The Journal of Neuroscience.

[73]  El-Mehdi Meftah,et al.  Effects of a cross-modal manipulation of attention on somatosensory cortical neuronal responses to tactile stimuli in the monkey. , 2002, Journal of neurophysiology.

[74]  Leslie G. Ungerleider,et al.  Neuroimaging Studies of Attention: From Modulation of Sensory Processing to Top-Down Control , 2003, The Journal of Neuroscience.

[75]  Fumio Goto,et al.  Fluvoxamine modulates pain sensation and affective processing of pain in human brain , 2003, Neuroreport.

[76]  Frederik Barkhof,et al.  A paced visual serial addition test for fMRI , 2003, Journal of the Neurological Sciences.

[77]  C. Eccleston The attentional control of pain: methodological and theoretical concerns , 1995, Pain.

[78]  S. Rauch,et al.  The counting stroop: An interference task specialized for functional neuroimaging—validation study with functional MRI , 1998, Human brain mapping.

[79]  B R Rosen,et al.  The Multi-Source Interference Task: validation study with fMRI in individual subjects , 2003, Molecular Psychiatry.

[80]  Alan C. Evans,et al.  Functional imaging of an illusion of pain , 1996, Nature.