Brain imaging of neuropathic pain

Many studies have focused on defining the network of brain structures involved in normal physiological pain. The different dimensions of pain perception (i.e., sensory discriminative, affective/emotional, cognitive/evaluative) have been shown to depend on different areas of the brain. In contrast, much less is known about the neural basis of pathological chronic pain. In particular, it is unclear whether such pain results from changes to the physiological "pain matrix". We review here studies on changes in brain activity associated with neuropathic pain syndromes-a specific category of chronic pain associated with peripheral or central neurological lesions. Patients may report combinations of spontaneous pain and allodynia/hyperalgesia-abnormal pain evoked by stimuli that normally induce no/little sensation of pain. Modern neuroimaging methods (positron emission tomography (PET) and functional MRI (fMRI)) have been used to determine whether different neuropathic pain symptoms involve similar brain structures and whether these structures are related to the physiological "pain matrix". PET studies have suggested that spontaneous neuropathic pain is associated principally with changes in thalamic activity and the medial pain system, which is preferentially involved in the emotional dimension of pain. Both PET and fMRI have been used to investigate the basis of allodynia. The results obtained have been very variable, probably reflecting the heterogeneity of patients in terms of etiology, lesion topography, symptoms and stimulation procedures. Overall, these studies indicated that acute physiological pain and neuropathic pain have distinct although overlapping brain activation pattern, but that there is no unique "pain matrix" or "allodynia network".

[1]  M. Koltzenburg,et al.  Dynamic and static components of mechanical hyperalgesia in human hairy skin , 1992, Pain.

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

[3]  H. Watabe,et al.  Cerebral decreases in opioid receptor binding in patients with central neuropathic pain measured by [11C]diprenorphine binding and PET , 2004, European journal of pain.

[4]  Carlo A Porro,et al.  Functional Imaging and Pain: Behavior, Perception, and Modulation , 2003, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

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

[6]  Edward E. Smith,et al.  Placebo-Induced Changes in fMRI in the Anticipation and Experience of Pain , 2004, Science.

[7]  J. Gybels,et al.  Positron emission tomography study of a chronic pain patient successfully treated with somatosensory thalamic stimulation , 2000, Pain.

[8]  Irene Tracey,et al.  Imaging pain in patients: is it meaningful? , 2006, Current opinion in neurology.

[9]  F. Lenz,et al.  Microelectrode Studies of Normal Organization and Plasticity of Human Somatosensory Thalamus , 2000, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[10]  Gilles Defer,et al.  Central pain and thalamic hyperactivity: a single photon emission computerized tomographic study , 1991, Pain.

[11]  Bernard Laurent,et al.  Comparison of pain syndromes associated with nervous or somatic lesions and development of a new neuropathic pain diagnostic questionnaire (DN4) , 2005, Pain.

[12]  Roland Peyron,et al.  Motor cortex stimulation in neuropathic pain. Correlations between analgesic effect and hemodynamic changes in the brain. A PET study , 2007, NeuroImage.

[13]  C. Woolf,et al.  Neuropathic pain: aetiology, symptoms, mechanisms, and management , 1999, The Lancet.

[14]  R. Baron,et al.  Complex regional pain syndrome: mystery explained? , 2003, The Lancet Neurology.

[15]  S. Canavero,et al.  Functional thalamic depression in a case of reversible central pain due to a spinal intramedullary cyst. Case report. , 1995, Journal of neurosurgery.

[16]  R. Baron,et al.  Is CRPS I a neuropathic pain syndrome? , 2006, Pain.

[17]  Patrick Ragert,et al.  Patterns of cortical reorganization parallel impaired tactile discrimination and pain intensity in complex regional pain syndrome , 2006, NeuroImage.

[18]  I. Tracey Nociceptive processing in the human brain , 2005, Current Opinion in Neurobiology.

[19]  M. Catherine Bushnell,et al.  Cognitive modulation of pain: how do attention and emotion influence pain processing? , 2002, Pain.

[20]  Karen Faith Berman,et al.  Unilateral decrease in thalamic activity observed with positron emission tomography in patients with chronic neuropathic pain , 1995, Pain.

[21]  Irene Tracey,et al.  An fMRI study of cerebral processing of brush-evoked allodynia in neuropathic pain patients , 2006, NeuroImage.

[22]  Ralf Baron,et al.  Mechanisms of Disease: neuropathic pain—a clinical perspective , 2006, Nature Clinical Practice Neurology.

[23]  D. Perani,et al.  Chronic pain: a PET study of the central effects of percutaneous high cervical cordotomy , 1991, Pain.

[24]  S. Minoshima,et al.  Keeping pain out of mind: the role of the dorsolateral prefrontal cortex in pain modulation. , 2003, Brain : a journal of neurology.

[25]  Steven Laureys,et al.  The cognitive modulation of pain: hypnosis- and placebo-induced analgesia. , 2005, Progress in brain research.

[26]  A. Ptito,et al.  Central pain in a hemispherectomized patient , 2001, European journal of pain.

[27]  D. Bouhassira,et al.  Systemic lidocaine in pain due to peripheral nerve injury and predictors of response , 2004, Neurology.

[28]  Jen-Chuen Hsieh,et al.  Central representation of chronic ongoing neuropathic pain studied by positron emission tomography , 1995, PAIN®.

[29]  Ron Kupers,et al.  Brain imaging of clinical pain states: a critical review and strategies for future studies , 2006, The Lancet Neurology.

[30]  M. Millan Descending control of pain , 2002, Progress in Neurobiology.

[31]  Mario Saltarelli,et al.  Advances in neuropathic pain: diagnosis, mechanisms, and treatment recommendations. , 2003, Archives of neurology.

[32]  A. K. Jones,et al.  Measurement of Changes in Opioid Receptor Binding in Vivo During Trigeminal Neuralgic Pain Using [11C]Diprenorphine and Positron Emission Tomography , 1999, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[33]  Frank Birklein,et al.  Brain processing during mechanical hyperalgesia in complex regional pain syndrome: a functional MRI study , 2005, Pain.

[34]  L Arendt-Nielsen,et al.  Experimental brush-evoked allodynia activates posterior parietal cortex , 2001, Neurology.

[35]  D. Bouhassira,et al.  Intravenous lidocaine in central pain , 2000, Neurology.

[36]  H. J. McQuay,et al.  Algorithm for neuropathic pain treatment: An evidence based proposal , 2005, Pain.

[37]  D. Price,et al.  Patterns of increased brain activity indicative of pain in a rat model of peripheral mononeuropathy , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  G H Duncan,et al.  Stimulation of human thalamus for pain relief: possible modulatory circuits revealed by positron emission tomography. , 1998, Journal of neurophysiology.

[39]  David Borsook,et al.  Trigeminal Neuropathic Pain Alters Responses in CNS Circuits to Mechanical (Brush) and Thermal (Cold and Heat) Stimuli , 2006, The Journal of Neuroscience.

[40]  K. Davis,et al.  The neural circuitry of pain as explored with functional MRI , 2000, Neurological research.

[41]  P. Rainville Brain mechanisms of pain affect and pain modulation , 2002, Current Opinion in Neurobiology.

[42]  Frode Willoch,et al.  Central poststroke pain and reduced opioid receptor binding within pain processing circuitries: a [11C]diprenorphine PET study , 2004, Pain.

[43]  K L Casey,et al.  Forebrain mechanisms of nociception and pain: analysis through imaging. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[44]  D. Bouhassira,et al.  Mechanisms of central neuropathic pain: a combined psychophysical and fMRI study in syringomyelia. , 2006, Brain : a journal of neurology.

[45]  E. Disbrow,et al.  Brain processing of capsaicin-induced secondary hyperalgesia , 1999, Neurology.

[46]  E. Chudler,et al.  The role of the basal ganglia in nociception and pain , 1995, Pain.

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

[48]  M. Deiber,et al.  Electrical stimulation of precentral cortical area in the treatment of central pain: electrophysiological and PET study , 1995, Pain.

[49]  E C Laterre,et al.  Brain glucose metabolism in thalamic syndrome. , 1988, Journal of neurology, neurosurgery, and psychiatry.

[50]  Jacques Fermanian,et al.  Development and validation of the Neuropathic Pain Symptom Inventory , 2004, Pain.

[51]  F. Mauguière,et al.  Positron emission tomography during motor cortex stimulation for pain control. , 1997, Stereotactic and functional neurosurgery.

[52]  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.

[53]  K. Berman,et al.  Neural activation during acute capsaicin-evoked pain and allodynia assessed with PET. , 1998, Brain : a journal of neurology.

[54]  J C Froment,et al.  Allodynia after lateral-medullary (Wallenberg) infarct. A PET study. , 1998, Brain : a journal of neurology.

[55]  Roland Peyron,et al.  Differential brain opioid receptor availability in central and peripheral neuropathic pain , 2007, Pain.

[56]  M Ingvar,et al.  A PET activation study of dynamic mechanical allodynia in patients with mononeuropathy , 1999, PAIN®.

[57]  M. Bennett,et al.  Using screening tools to identify neuropathic pain , 2007, PAIN.

[58]  Peter Svensson,et al.  A PET activation study of brush-evoked allodynia in patientswith nerve injury pain , 2006, Pain.

[59]  Anthony K. P. Jones,et al.  The cortical representation of pain , 1999, PAIN.

[60]  D. Bouhassira,et al.  Effects of IV morphine in central pain: A randomized placebo-controlled study , 2002, Neurology.

[61]  R. Peyron,et al.  An fMRI study of cortical representation of mechanical allodynia in patients with neuropathic pain , 2004, Neurology.

[62]  Frank Birklein,et al.  Functional imaging of allodynia in complex regional pain syndrome , 2006, Neurology.

[63]  Jürgen Lorenz,et al.  A Unique Representation of Heat Allodynia in the Human Brain , 2002, Neuron.

[64]  A. D. De Salles,et al.  Thalamic pain syndrome: anatomic and metabolic correlation. , 1994, Surgical neurology.