Altered prefrontal correlates of monetary anticipation and outcome in chronic pain

Abstract Chronic pain may alter both affect- and value-related behaviors, which represents a potentially treatable aspect of chronic pain experience. Current understanding of how chronic pain influences the function of brain reward systems, however, is limited. Using a monetary incentive delay task and functional magnetic resonance imaging (fMRI), we measured neural correlates of reward anticipation and outcomes in female participants with the chronic pain condition of fibromyalgia (N = 17) and age-matched, pain-free, female controls (N = 15). We hypothesized that patients would demonstrate lower positive arousal, as well as altered reward anticipation and outcome activity within corticostriatal circuits implicated in reward processing. Patients demonstrated lower arousal ratings as compared with controls, but no group differences were observed for valence, positive arousal, or negative arousal ratings. Group fMRI analyses were conducted to determine predetermined region of interest, nucleus accumbens (NAcc) and medial prefrontal cortex (mPFC), responses to potential gains, potential losses, reward outcomes, and punishment outcomes. Compared with controls, patients demonstrated similar, although slightly reduced, NAcc activity during gain anticipation. Conversely, patients demonstrated dramatically reduced mPFC activity during gain anticipation—possibly related to lower estimated reward probabilities. Further, patients demonstrated normal mPFC activity to reward outcomes, but dramatically heightened mPFC activity to no-loss (nonpunishment) outcomes. In parallel to NAcc and mPFC responses, patients demonstrated slightly reduced activity during reward anticipation in other brain regions, which included the ventral tegmental area, anterior cingulate cortex, and anterior insular cortex. Together, these results implicate altered corticostriatal processing of monetary rewards in chronic pain.

[1]  M. Lorr,et al.  Manual for the Profile of Mood States , 1971 .

[2]  W. Schultz,et al.  Neuronal activity in monkey ventral striatum related to the expectation of reward , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  Robert C. Coghill,et al.  Distinct brain mechanisms support spatial vs temporal filtering of nociceptive information , 2014, PAIN®.

[4]  Brian Knutson,et al.  Ventral Striatal Activation During Reward Anticipation Correlates with Impulsivity in Alcoholics , 2009, Biological Psychiatry.

[5]  R Turner,et al.  Optimized EPI for fMRI studies of the orbitofrontal cortex , 2003, NeuroImage.

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

[7]  Herta Flor,et al.  Structural plasticity and reorganisation in chronic pain , 2016, Nature Reviews Neuroscience.

[8]  C. Carver,et al.  Behavioral inhibition, behavioral activation, and affective responses to impending reward and punishment: The BIS/BAS Scales , 1994 .

[9]  M. Roesch,et al.  Neuronal Activity Related to Reward Value and Motivation in Primate Frontal Cortex , 2004, Science.

[10]  J. Grafman,et al.  Structured event complexes in the medial prefrontal cortex support counterfactual representations for future planning , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[11]  G. Glover,et al.  Prefrontal cortical regulation of brainwide circuit dynamics and reward-related behavior , 2016, Science.

[12]  S. Huettel,et al.  Activation in the VTA and Nucleus Accumbens Increases in Anticipation of Both Gains and Losses , 2009, Front. Behav. Neurosci..

[13]  S. Quartz,et al.  Human Insula Activation Reflects Risk Prediction Errors As Well As Risk , 2008, The Journal of Neuroscience.

[14]  Brian Knutson,et al.  Neural valuation of environmental resources , 2015, NeuroImage.

[15]  M. Baliki,et al.  Predicting Value of Pain and Analgesia: Nucleus Accumbens Response to Noxious Stimuli Changes in the Presence of Chronic Pain , 2010, Neuron.

[16]  C. Spielberger,et al.  Manual for the State-Trait Anxiety Inventory , 1970 .

[17]  S. Langenecker,et al.  NEURAL REACTIVITY TO REWARD AS A PREDICTOR OF COGNITIVE BEHAVIORAL THERAPY RESPONSE IN ANXIETY AND DEPRESSION , 2016, Depression and anxiety.

[18]  W. Schultz,et al.  Discrete Coding of Reward Probability and Uncertainty by Dopamine Neurons , 2003, Science.

[19]  J. Gläscher,et al.  Dissociable Systems for Gain- and Loss-Related Value Predictions and Errors of Prediction in the Human Brain , 2006, The Journal of Neuroscience.

[20]  T. Wager,et al.  Orbitofrontal cortex mediates pain inhibition by monetary reward , 2017, Social cognitive and affective neuroscience.

[21]  S. Mackey,et al.  Neuroimaging of Pain: Human Evidence and Clinical Relevance of Central Nervous System Processes and Modulation. , 2018, Anesthesiology.

[22]  H. Fields Understanding How Opioids Contribute to Reward and Analgesia , 2007, Regional Anesthesia & Pain Medicine.

[23]  Brian Knutson,et al.  A region of mesial prefrontal cortex tracks monetarily rewarding outcomes: characterization with rapid event-related fMRI , 2003, NeuroImage.

[24]  L. Becerra,et al.  Alterations in brain structure and functional connectivity in prescription opioid-dependent patients. , 2010, Brain : a journal of neurology.

[25]  D. Borsook,et al.  Neuroscience and Biobehavioral Reviews Reward Deficiency and Anti-reward in Pain Chronification , 2022 .

[26]  Samuel M. McClure,et al.  Separate Neural Systems Value Immediate and Delayed Monetary Rewards , 2004, Science.

[27]  R. Coghill,et al.  Opioid-independent mechanisms supporting offset analgesia and temporal sharpening of nociceptive information , 2012, PAIN.

[28]  M. Walker,et al.  Sleep Deprivation Amplifies Reactivity of Brain Reward Networks, Biasing the Appraisal of Positive Emotional Experiences , 2011, The Journal of Neuroscience.

[29]  F. Wolfe,et al.  Fibromyalgia Criteria and Severity Scales for Clinical and Epidemiological Studies: A Modification of the ACR Preliminary Diagnostic Criteria for Fibromyalgia , 2011, The Journal of Rheumatology.

[30]  M. Laubach,et al.  Reward-related activity in the medial prefrontal cortex is driven by consumption , 2013, Front. Neurosci..

[31]  Brian Knutson,et al.  Linking nucleus accumbens dopamine and blood oxygenation , 2007, Psychopharmacology.

[32]  D. Watson,et al.  Development and validation of brief measures of positive and negative affect: the PANAS scales. , 1988, Journal of personality and social psychology.

[33]  S. Haber,et al.  The Reward Circuit: Linking Primate Anatomy and Human Imaging , 2010, Neuropsychopharmacology.

[34]  M. Ernst,et al.  Longitudinal study of striatal activation to reward and loss anticipation from mid-adolescence into late adolescence/early adulthood , 2014, Brain and Cognition.

[35]  Samuel M. McClure,et al.  Distinct Midbrain and Habenula Pathways Are Involved in Processing Aversive Events in Humans , 2015, The Journal of Neuroscience.

[36]  H. Beck,et al.  Function and developmental origin of a mesocortical inhibitory circuit , 2015, Nature Neuroscience.

[37]  Brian Knutson,et al.  Reward Processing After Catecholamine Depletion in Unmedicated, Remitted Subjects with Major Depressive Disorder , 2009, Biological Psychiatry.

[38]  Jeffrey C. Cooper,et al.  Functional magnetic resonance imaging of reward prediction , 2005, Current opinion in neurology.

[39]  T. Westfall,et al.  ALTERATIONS IN THE , 1985 .

[40]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[41]  K. Berridge,et al.  What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? , 1998, Brain Research Reviews.

[42]  Brian Knutson,et al.  Affective traits link to reliable neural markers of incentive anticipation , 2014, NeuroImage.

[43]  C. Cleeland,et al.  Validity of the Brief Pain Inventory for Use in Documenting the Outcomes of Patients With Noncancer Pain , 2004, The Clinical journal of pain.

[44]  A. Dahan,et al.  Offset Analgesia in Neuropathic Pain Patients and Effect of Treatment with Morphine and Ketamine , 2011, Anesthesiology.

[45]  Brian Knutson,et al.  Anticipation of Increasing Monetary Reward Selectively Recruits Nucleus Accumbens , 2001, The Journal of Neuroscience.

[46]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[47]  Alain Dagher,et al.  Fibromyalgia patients show an abnormal dopamine response to pain , 2007, The European journal of neuroscience.

[48]  Luke J. Chang,et al.  Large-Scale Meta-Analysis of Human Medial Frontal Cortex Reveals Tripartite Functional Organization , 2016, The Journal of Neuroscience.

[49]  Russell A. Poldrack,et al.  Large-scale automated synthesis of human functional neuroimaging data , 2011, Nature Methods.

[50]  John J Sunderland,et al.  Reduced presynaptic dopamine activity in fibromyalgia syndrome demonstrated with positron emission tomography: a pilot study. , 2007, The journal of pain : official journal of the American Pain Society.

[51]  Yuan Bo Peng,et al.  Integrative Neuroscience Review Article the Anterior Cingulate Cortex and Pain Processing , 2022 .

[52]  David Borsook,et al.  Signal valence in the nucleus accumbens to pain onset and offset , 2008, European journal of pain.

[53]  G. Glover,et al.  Spiral‐in/out BOLD fMRI for increased SNR and reduced susceptibility artifacts , 2001, Magnetic resonance in medicine.

[54]  Brian Knutson,et al.  Spatial smoothing systematically biases the localization of reward-related brain activity , 2013, NeuroImage.

[55]  P. Dayan,et al.  Cortical substrates for exploratory decisions in humans , 2006, Nature.

[56]  I. Tracey,et al.  The importance of context: When relative relief renders pain pleasant , 2013, PAIN®.

[57]  A. Beck,et al.  Psychometric properties of the Beck Depression Inventory: Twenty-five years of evaluation , 1988 .

[58]  Brandon Galarita,et al.  Chronic , 2020, Definitions.

[59]  M E Robinson,et al.  Negative affect and the experience of chronic pain. , 1992, Journal of psychosomatic research.

[60]  R. Coghill,et al.  Differential effects of experimental central sensitization on the time-course and magnitude of offset analgesia , 2012, PAIN.

[61]  E. Navratilova,et al.  Brain Circuits Encoding Reward from Pain Relief , 2015, Trends in Neurosciences.

[62]  S. Haber,et al.  Primate cingulostriatal projection: Limbic striatal versus sensorimotor striatal input , 1994, The Journal of comparative neurology.

[63]  C. Libedinsky,et al.  Sleep Deprivation Alters Valuation Signals in the Ventromedial Prefrontal Cortex , 2011, Front. Behav. Neurosci..

[64]  Thomas J. Schnitzer,et al.  Corticostriatal functional connectivity predicts transition to chronic back pain , 2012, Nature Neuroscience.

[65]  Frank Van Overwalle,et al.  Counterfactual thinking: an fMRI study on changing the past for a better future. , 2013, Social cognitive and affective neuroscience.

[66]  L. McWilliams,et al.  Mood and anxiety disorders associated with chronic pain: an examination in a nationally representative sample , 2003, Pain.

[67]  M. Farah,et al.  Progress and challenges in probing the human brain , 2015, Nature.

[68]  Robert C. Coghill,et al.  Offset analgesia: A temporal contrast mechanism for nociceptive information , 2008, Pain.

[69]  Dante R. Chialvo,et al.  Chronic pain patients are impaired on an emotional decision-making task , 2004, Pain.

[70]  A. Dale,et al.  Dorsal anterior cingulate cortex: A role in reward-based decision making , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[71]  Brian Knutson,et al.  Dissociation of reward anticipation and outcome with event-related fMRI , 2001, Neuroreport.

[72]  T. Robbins,et al.  Reduction in ventral striatal activity when anticipating a reward in depression and schizophrenia: a replicated cross-diagnostic finding , 2015, Front. Psychol..

[73]  Elie Karam,et al.  Common chronic pain conditions in developed and developing countries: gender and age differences and comorbidity with depression-anxiety disorders. , 2008, The journal of pain : official journal of the American Pain Society.

[74]  Daniel J Buysse,et al.  The Patient-Reported Outcomes Measurement Information System (PROMIS) developed and tested its first wave of adult self-reported health outcome item banks: 2005-2008. , 2010, Journal of clinical epidemiology.

[75]  I. Tracey,et al.  A common neurobiology for pain and pleasure , 2008, Nature Reviews Neuroscience.

[76]  S. Morley,et al.  A confirmatory factor analysis of the Beck Depression Inventory in chronic pain , 2002, PAIN.

[77]  Evgeny J. Chumin,et al.  Differential dopamine function in fibromyalgia , 2015, Brain Imaging and Behavior.

[78]  P. Glimcher,et al.  The neural correlates of subjective value during intertemporal choice , 2007, Nature Neuroscience.

[79]  J. Fallon Collateralization of monoamine neurons: mesotelencephalic dopamine projections to caudate, septum, and frontal cortex , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[80]  B. Lim,et al.  Decreased motivation during chronic pain requires long-term depression in the nucleus accumbens , 2014, Science.

[81]  Matthew T. Kaufman,et al.  Distributed Neural Representation of Expected Value , 2005, The Journal of Neuroscience.

[82]  Altered Dopamine Responses to Monetary Rewards in Female Fibromyalgia Patients with and without Depression: A [11C]Raclopride Bolus-plus-Infusion PET Study , 2017, Psychotherapy and Psychosomatics.

[83]  Brian Knutson,et al.  Neural Responses to Monetary Incentives in Major Depression , 2008, Biological Psychiatry.

[84]  Yuan Bo Peng,et al.  The biopsychosocial approach to chronic pain: scientific advances and future directions. , 2007, Psychological bulletin.

[85]  近間 正典 Insular Cortical Projections to Functional Regions of the Striatum Correlate with Cortical Cytoarchitectonic Organization in the Primate , 1998 .

[86]  Brian Knutson,et al.  Anticipatory affect: neural correlates and consequences for choice , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[87]  Vitaly Napadow,et al.  Disrupted Brain Circuitry for Pain‐Related Reward/Punishment in Fibromyalgia , 2014, Arthritis & rheumatology.

[88]  K. Deisseroth,et al.  Input-specific control of reward and aversion in the ventral tegmental area , 2012, Nature.

[89]  L. Swanson,et al.  The projections of the ventral tegmental area and adjacent regions: A combined fluorescent retrograde tracer and immunofluorescence study in the rat , 1982, Brain Research Bulletin.

[90]  H. C. Cromwell,et al.  Rethinking the cognitive revolution from a neural perspective: How overuse/misuse of the term ‘cognition’ and the neglect of affective controls in behavioral neuroscience could be delaying progress in understanding the BrainMind , 2011, Neuroscience & Biobehavioral Reviews.

[91]  E. Navratilova,et al.  Reward and motivation in pain and pain relief , 2014, Nature Neuroscience.