Comparison of anterior cingulate vs. insular cortex as targets for real-time fMRI regulation during pain stimulation

Real-time functional magnetic resonance imaging (rt-fMRI) neurofeedback allows learning voluntary control over specific brain areas by means of operant conditioning and has been shown to decrease pain perception. To further increase the effect of rt-fMRI neurofeedback on pain, we directly compared two different target regions of the pain network, notably the anterior insular cortex (AIC) and the anterior cingulate cortex (ACC). Participants for this prospective study were randomly assigned to two age-matched groups of 14 participants each (7 females per group) for AIC and ACC feedback. First, a functional localizer using block-design heat pain stimulation was performed to define the pain-sensitive target region within the AIC or ACC. Second, subjects were asked to down-regulate the BOLD activation in four neurofeedback runs during identical pain stimulation. Data analysis included task-related and functional connectivity analysis. At the behavioral level, pain ratings significantly decreased during feedback vs. localizer runs, but there was no difference between AIC and ACC groups. Concerning neuroimaging, ACC and AIC showed consistent involvement of the caudate nucleus for subjects that learned down-regulation (17/28) in both task-related and functional connectivity analysis. The functional connectivity toward the caudate nucleus is stronger for the ACC while the AIC is more heavily connected to the ventrolateral prefrontal cortex. Consequently, the ACC and AIC are suitable targets for real-time fMRI neurofeedback during pain perception as they both affect the caudate nucleus, although functional connectivity indicates that the direct connection seems to be stronger with the ACC. Additionally, the caudate, an important area involved in pain perception and suppression, could be a good rt-fMRI target itself. Future studies are needed to identify parameters characterizing successful regulators and to assess the effect of repeated rt-fMRI neurofeedback on pain perception.

[1]  C. Voscopoulos,et al.  When does acute pain become chronic? , 2010, British journal of anaesthesia.

[2]  A. Mouraux,et al.  From the neuromatrix to the pain matrix (and back) , 2010, Experimental Brain Research.

[3]  J. Rubins,et al.  ASYMBOLIA FOR PAIN , 1948 .

[4]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[5]  M. Valenstein,et al.  Pain and suicidal thoughts, plans and attempts in the United States. , 2008, General hospital psychiatry.

[6]  J. Bueller,et al.  Reduced Brainstem Inhibition during Anticipated Pelvic Visceral Pain Correlates with Enhanced Brain Response to the Visceral Stimulus in Women with Irritable Bowel Syndrome , 2008, The Journal of Neuroscience.

[7]  Krish D. Singh,et al.  fMRI of Thermal Pain: Effects of Stimulus Laterality and Attention , 2002, NeuroImage.

[8]  R. Veit,et al.  Regulation of emotional responses elicited by threat‐related stimuli , 2007, Human brain mapping.

[9]  G. Crombez,et al.  Worry and chronic pain: A misdirected problem solving model , 2007, PAIN.

[10]  M. Bushnell,et al.  Cognitive and emotional control of pain and its disruption in chronic pain , 2013, Nature Reviews Neuroscience.

[11]  C. Woolf Central sensitization: Implications for the diagnosis and treatment of pain , 2011, PAIN.

[12]  G. Dussor,et al.  Central modulation of pain. , 2010, The Journal of clinical investigation.

[13]  Tilo Kircher,et al.  Acquired self‐control of insula cortex modulates emotion recognition and brain network connectivity in schizophrenia , 2013, Human brain mapping.

[14]  L. Garcia-Larrea,et al.  The posterior insular-opercular region and the search of a primary cortex for pain , 2012, Neurophysiologie Clinique/Clinical Neurophysiology.

[15]  M. Bushnell,et al.  Effective Treatment of Chronic Low Back Pain in Humans Reverses Abnormal Brain Anatomy and Function , 2011, The Journal of Neuroscience.

[16]  S. Linton A Transdiagnostic Approach to Pain and Emotion , 2013, Journal of applied biobehavioral research.

[17]  Kevin A. Johnson,et al.  Volitional reduction of anterior cingulate cortex activity produces decreased cue craving in smoking cessation: a preliminary real‐time fMRI study , 2013, Addiction biology.

[18]  Hiroshi Baba,et al.  Partial Peripheral Nerve Injury Promotes a Selective Loss of GABAergic Inhibition in the Superficial Dorsal Horn of the Spinal Cord , 2002, The Journal of Neuroscience.

[19]  K. Brady,et al.  Sustained reduction of nicotine craving with real-time neurofeedback: exploring the role of severity of dependence. , 2013, Nicotine & tobacco research : official journal of the Society for Research on Nicotine and Tobacco.

[20]  Wolfgang Grodd,et al.  Regulation of anterior insular cortex activity using real-time fMRI , 2007, NeuroImage.

[21]  Nick Medford,et al.  Self-regulation of the anterior insula: Reinforcement learning using real-time fMRI neurofeedback , 2014, NeuroImage.

[22]  Y. de Koninck,et al.  Transformation of the output of spinal lamina I neurons after nerve injury and microglia stimulation underlying neuropathic pain , 2007, Molecular pain.

[23]  E. Kalso,et al.  Make a CHANGE: optimising communication and pain management decisions , 2011, Current medical research and opinion.

[24]  D. Turk,et al.  Chronic pain and depression: role of perceived impact and perceived control in different age cohorts , 1995, Pain.

[25]  C. Mitchell,et al.  Attention and relative novelty in human perceptual learning. , 2011, Journal of experimental psychology. Animal behavior processes.

[26]  B. Pfleiderer,et al.  Fibromyalgia unique temporal brain activation during experimental pain: a controlled fMRI Study , 2009, Journal of Neural Transmission.

[27]  Bettina Sorger,et al.  Real-Time Self-Regulation of Emotion Networks in Patients with Depression , 2012, PloS one.

[28]  Mariela Rance,et al.  Real time fMRI feedback of the anterior cingulate and posterior insular cortex in the processing of pain , 2014, Human brain mapping.

[29]  C. Degueldre,et al.  Neural Mechanisms of Antinociceptive Effects of Hypnosis , 2000, Anesthesiology.

[30]  P. Rainville,et al.  A non-elaborative mental stance and decoupling of executive and pain-related cortices predicts low pain sensitivity in Zen meditators , 2011, PAIN®.

[31]  G. Crombez,et al.  The Fear-Avoidance Model of Musculoskeletal Pain: Current State of Scientific Evidence , 2006, Journal of Behavioral Medicine.

[32]  A. Mouraux,et al.  Determinants of laser-evoked EEG responses: pain perception or stimulus saliency? , 2008, Journal of neurophysiology.

[33]  Jin Fan,et al.  Cognition-emotion integration in the anterior insular cortex. , 2013, Cerebral cortex.

[34]  D. Rall,et al.  Thresholds? , 1978, Environmental health perspectives.

[35]  Klaus Scheffler,et al.  Background MR gradient noise and non-auditory BOLD activations: A data-driven perspective , 2009, Brain Research.

[36]  F. Leavitt,et al.  Distraction as a key determinant of impaired memory in patients with fibromyalgia. , 2006, The Journal of rheumatology.

[37]  J. Riley,et al.  Negative affect, self-report of depressive symptoms, and clinical depression: relation to the experience of chronic pain. , 2000, The Clinical journal of pain.

[38]  J. O'Doherty,et al.  Empathy for Pain Involves the Affective but not Sensory Components of Pain , 2004, Science.

[39]  T. Nikolaus,et al.  Multisite pain, pain frequency and pain severity are associated with depression in older adults: results from the ActiFE Ulm study. , 2014, Age and ageing.

[40]  Nicola Filippini,et al.  Thalamic atrophy associated with painful osteoarthritis of the hip is reversible after arthroplasty: a longitudinal voxel-based morphometric study. , 2010, Arthritis and rheumatism.

[41]  J. Vlaeyen,et al.  Pain‐related fear in low back pain: A prospective study in the general population , 2007, European journal of pain.

[42]  Katiuscia Sacco,et al.  Meta-analytic clustering of the insular cortex Characterizing the meta-analytic connectivity of the insula when involved in active tasks , 2012, NeuroImage.

[43]  John D E Gabrieli,et al.  Control over brain activation and pain learned by using real-time functional MRI. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[44]  M. Honda,et al.  Expectation of Pain Enhances Responses to Nonpainful Somatosensory Stimulation in the Anterior Cingulate Cortex and Parietal Operculum/Posterior Insula: an Event-Related Functional Magnetic Resonance Imaging Study , 2000, The Journal of Neuroscience.

[45]  D. Chialvo,et al.  Chronic Pain and the Emotional Brain: Specific Brain Activity Associated with Spontaneous Fluctuations of Intensity of Chronic Back Pain , 2006, The Journal of Neuroscience.

[46]  Geraint Rees,et al.  Improving Visual Perception through Neurofeedback , 2012, The Journal of Neuroscience.

[47]  A. Kleinschmidt,et al.  Anterior insula activations in perceptual paradigms: often observed but barely understood , 2010, Brain Structure and Function.

[48]  J. Katz,et al.  Understanding the co‐occurrence of anxiety disorders and chronic pain: state‐of‐the‐art , 2009, Depression and anxiety.

[49]  Niels Birbaumer,et al.  Using real-time fMRI to learn voluntary regulation of the anterior insula in the presence of threat-related stimuli. , 2012, Social cognitive and affective neuroscience.

[50]  B. Landwehrmeyer,et al.  Caudate Nucleus and Insular Activation During a Pain Suppression Paradigm Comparing Thermal and Electrical Stimulation , 2011, The open neuroimaging journal.

[51]  Fred A Lenz,et al.  Pain sensitivity alterations as a function of lesion location in the parasylvian cortex , 1999, Pain.

[52]  E. Hudon,et al.  Pharmacotherapeutic management of chronic noncancer pain in primary care: lessons for pharmacists , 2014, Journal of pain research.

[53]  J. Sandkühler,et al.  Long-term potentiation at C-fibre synapses by low-level presynaptic activity in vivo , 2008, Molecular pain.

[54]  Niels Birbaumer,et al.  Real-Time fMRI , 2012, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[55]  J. O'Doherty,et al.  Direct Instrumental Conditioning of Neural Activity Using Functional Magnetic Resonance Imaging-Derived Reward Feedback , 2007, The Journal of Neuroscience.

[56]  Till Sprenger,et al.  Distraction modulates connectivity of the cingulo-frontal cortex and the midbrain during pain—an fMRI analysis , 2004, Pain.

[57]  C. Degueldre,et al.  Neural Mechanisms of Antinociceptive Effects of , 2000 .

[58]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[59]  A. Wunderlich,et al.  Perception and suppression of thermally induced pain: A fMRI study , 2009, Somatosensory & motor research.

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

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

[62]  J. Rhudy,et al.  Fear and anxiety: divergent effects on human pain thresholds , 2000, Pain.

[63]  R MELZACK,et al.  The perception of pain. , 1961, Scientific American.

[64]  Britta K. Hölzel,et al.  Pain attenuation through mindfulness is associated with decreased cognitive control and increased sensory processing in the brain. , 2012, Cerebral cortex.

[65]  Sven Haller,et al.  Real-time fMRI feedback training may improve chronic tinnitus , 2010, European Radiology.

[66]  M. Woldorff,et al.  Dorsal anterior cingulate cortex resolves conflict from distracting stimuli by boosting attention toward relevant events. , 2004, Cerebral cortex.

[67]  M. Ingvar,et al.  Cognitive Behavioral Therapy increases pain-evoked activation of the prefrontal cortex in patients with fibromyalgeia , 2012, PAIN.

[68]  D. Munguía-Izquierdo,et al.  Exercise in warm water decreases pain and improves cognitive function in middle-aged women with fibromyalgia. , 2007, Clinical and experimental rheumatology.

[69]  Michael Erb,et al.  Physiological self-regulation of regional brain activity using real-time functional magnetic resonance imaging (fMRI): methodology and exemplary data , 2003, NeuroImage.

[70]  James J Prisciandaro,et al.  Real-time fMRI in the treatment of nicotine dependence: a conceptual review and pilot studies. , 2013, Psychology of addictive behaviors : journal of the Society of Psychologists in Addictive Behaviors.

[71]  G. Grace,et al.  Concentration and memory deficits in patients with fibromyalgia syndrome. , 1999, Journal of clinical and experimental neuropsychology.

[72]  Klaus Scheffler,et al.  Effect of fMRI acoustic noise on non-auditory working memory task: comparison between continuous and pulsed sound emitting EPI , 2005, Magnetic Resonance Materials in Physics, Biology and Medicine.

[73]  K. Wiech,et al.  The Effect of Treatment Expectation on Drug Efficacy: Imaging the Analgesic Benefit of the Opioid Remifentanil , 2011, Science Translational Medicine.

[74]  B. Vogt,et al.  Pain Processing in Four Regions of Human Cingulate Cortex Localized with Co‐registered PET and MR Imaging , 1996, The European journal of neuroscience.

[75]  Steven Laureys,et al.  Neural Mechanisms of Antinociceptive Effects of Hypnosis , 2000 .

[76]  Stephan G. Boehm,et al.  Upregulation of emotion areas through neurofeedback with a focus on positive mood , 2011, Cognitive, affective & behavioral neuroscience.

[77]  P. Cesare,et al.  A novel heat-activated current in nociceptive neurons and its sensitization by bradykinin. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[78]  K. Lovblad,et al.  Acute caffeine administration effect on brain activation patterns in mild cognitive impairment. , 2014, Journal of Alzheimer's disease : JAD.

[79]  L. Larrea,et al.  The posterior insular-opercular region and the search of a primary cortex for pain , 2017 .

[80]  A. Mikami,et al.  During pain-avoidance neurons activated in the macaque anterior cingulate and caudate , 2000, Neuroscience Letters.

[81]  M. Baliki,et al.  The Cortical Rhythms of Chronic Back Pain , 2011, The Journal of Neuroscience.

[82]  Stefania Favilla,et al.  Ranking brain areas encoding the perceived level of pain from fMRI data , 2014, NeuroImage.

[83]  Kyungmo Park,et al.  Intrinsic brain connectivity in fibromyalgia is associated with chronic pain intensity. , 2010, Arthritis and rheumatism.

[84]  S. Linton,et al.  Cognitive dimensions of anger in chronic pain , 2012, PAIN.

[85]  Jessica A. Grahn,et al.  The cognitive functions of the caudate nucleus , 2008, Progress in Neurobiology.

[86]  R. Davidson,et al.  The integration of negative affect, pain and cognitive control in the cingulate cortex , 2011, Nature Reviews Neuroscience.

[87]  J. Greenspan,et al.  Reversible pain and tactile deficits associated with a cerebral tumor compressing the posterior insula and parietal operculum , 1992, Pain.

[88]  P. Roland Cortical representation of pain , 1992, Trends in Neurosciences.

[89]  K. Verhoeven,et al.  Distraction from pain and executive functioning: An experimental investigation of the role of inhibition, task switching and working memory , 2011, European journal of pain.

[90]  R. Treede,et al.  Human brain mechanisms of pain perception and regulation in health and disease , 2005, European journal of pain.

[91]  G. Gebhart,et al.  Chronic pain and medullary descending facilitation , 2002, Trends in Neurosciences.

[92]  P. Schilder,et al.  ASYMBOLIA FOR PAIN , 1931 .

[93]  Jong-Hwan Lee,et al.  Real-time fMRI-based neurofeedback reinforces causality of attention networks , 2012, Neuroscience Research.

[94]  I. Sinanaj,et al.  Acute caffeine administration impact on working memory-related brain activation and functional connectivity in the elderly: A BOLD and perfusion MRI study , 2013, Neuroscience.

[95]  R. Leiguarda,et al.  Asymbolia for pain: A sensory‐limbic disconnection syndrome , 1988, Annals of neurology.

[96]  T. Tran,et al.  Temporal summation of heat pain in humans: Evidence supporting thalamocortical modulation , 2010, PAIN.

[97]  A. May,et al.  Sensory and sympathetic correlates of heat pain sensitization and habituation in men and women , 2012, European journal of pain.

[98]  J. Vlaeyen,et al.  Fear-avoidance model of chronic musculoskeletal pain: 12 years on , 2012, PAIN.

[99]  Dimitri Van De Ville,et al.  Self-regulation of inter-hemispheric visual cortex balance through real-time fMRI neurofeedback training , 2014, NeuroImage.

[100]  Roman Rolke,et al.  Isolated insular infarction eliminates contralateral cold, cold pain, and pinprick perception , 2005, Neurology.

[101]  W. Katon,et al.  Depression and pain comorbidity: a literature review. , 2003, Archives of internal medicine.

[102]  David Borsook,et al.  A key role of the basal ganglia in pain and analgesia - insights gained through human functional imaging , 2010, Molecular pain.

[103]  Steven C. R. Williams,et al.  Evidence of dysfunctional pain inhibition in Fibromyalgia reflected in rACC during provoked pain , 2009, PAIN®.