Neuroplastic Changes Related to Pain Occur at Multiple Levels of the Human Somatosensory System: A Somatosensory-Evoked Potentials Study in Patients with Cervical Radicular Pain

Studies suggest that pain may play a major role in determining cortical rearrangements in the adult human somatosensory system. Most studies, however, have been performed under conditions whereby pain coexists with massive deafferentation (e.g., amputations). Moreover, no information is available on whether spinal and brainstem changes contribute to pain-related reorganizational processes in humans. Here we assess the relationships between pain and plasticity by recording somatosensory-evoked potentials (SEPs) in patients who complained of pain to the right thumb after a right cervical monoradiculopathy caused by compression of the sixth cervical root, but did not present with clinical or neurophysiological signs of deafferentation. Subcortical and cortical potentials evoked by stimulation of digital nerves of the right thumb and middle finger were compared with those obtained after stimulation of the left thumb and middle finger and with those obtained in a control group tested in comparable conditions. Amplitudes of spinal N13, brainstem P14, parietal N20 and P27, and frontal N30 potentials after stimulation of the painful right thumb were greater than those of the nonpainful left thumb and showed a positive correlation with magnitude of pain. This right–left asymmetry was absent after stimulation of the patients' middle fingers and in control subjects. Results suggest that chronic cervical radicular pain is associated with changes in neural activity at multiple levels of the somatosensory system. The absence of correlation between the amplitude of spinal, brainstem, and cortical components of SEPs suggests that enhancement of cortical activity is not a simple amplification of subcortical enhancement.

[1]  M. Sheehy,et al.  Electrodiagnosis in Diseases of Nerve and Muscle: Principles and Practice , 1984 .

[2]  R. Dubner,et al.  Spatial and temporal transformations of input to spinothalamic tract neurons and their relation to somatic sensations. , 1978, Journal of neurophysiology.

[3]  G Zanette,et al.  Transient deafferentation in humans induces rapid modulation of primary sensory cortex not associated with subcortical changes: a somatosensory evoked potential study , 1997, Neuroscience Letters.

[4]  L. Bour,et al.  Digital nerve somatosensory evoked potentials and flexor carpi radialis H reflexes in cervical disc protrusion and involvement of the sixth or seventh cervical root: relations to clinical and myelographic findings. , 1988, Electroencephalography and clinical neurophysiology.

[5]  Miguel A. L. Nicolelis,et al.  Simultaneous reorganization in thalamocortical ensembles evolves over several hours after perioral capsaicin injections. , 1999, Journal of neurophysiology.

[6]  V S Ramachandran,et al.  Noninvasive detection of cerebral plasticity in adult human somatosensory cortex. , 1994, Neuroreport.

[7]  R. Melzack.  The McGill Pain Questionnaire: Major properties and scoring methods , 1975, PAIN.

[8]  S. Hoppenfeld,et al.  Physical examination of the spine and extremities , 1976 .

[9]  G Cheron,et al.  Prevertebral (oesophageal) recording of subcortical somatosensory evoked potentials in man: the spinal P13 component and the dual nature of the spinal generators. , 1981, Electroencephalography and clinical neurophysiology.

[10]  P. D. Wall,et al.  Receptive fields of rat lamina 1 projection cells move to incorporate a nearby region of injury , 1984, Pain.

[11]  PM Dougherty,et al.  Enhanced responses of spinothalamic tract neurons to excitatory amino acids accompany capsaicin-induced sensitization in the monkey , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  Imananagha Kk,et al.  Thalamic pain syndrome of Dejerine-Roussy. , 1993 .

[13]  F Mauguière,et al.  Astereognosis and dissociated loss of frontal or parietal components of somatosensory evoked potentials in hemispheric lesions. Detailed correlations with clinical signs and computerized tomographic scanning. , 1983, Brain : a journal of neurology.

[14]  H. Schwark,et al.  Receptive field reorganization in dorsal column nuclei during temporary denervation. , 1993, Science.

[15]  J E Desmedt,et al.  Bit-mapped color imaging of human evoked potentials with reference to the N20, P22, P27 and N30 somatosensory responses. , 1987, Electroencephalography and clinical neurophysiology.

[16]  M. Nicolelis,et al.  Immediate and simultaneous sensory reorganization at cortical and subcortical levels of the somatosensory system. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[17]  D. J. Felleman,et al.  Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation , 1983, Neuroscience.

[18]  N Birbaumer,et al.  Extensive reorganization of the somatosensory cortex in adult humans after nervous system injury. , 1994, Neuroreport.

[19]  C. Miniussi,et al.  Neurophysiological evidence of neuroplasticity at multiple levels of the somatosensory system in patients with carpal tunnel syndrome. , 1998, Brain : a journal of neurology.

[20]  Niels Birbaumer,et al.  Extensive reorganization of primary somatosensory cortex in chronic back pain patients , 1997, Neuroscience Letters.

[21]  F. Bernt.  McGill Pain Questionnaire , 1991 .

[22]  D. J. Felleman,et al.  Progression of change following median nerve section in the cortical representation of the hand in areas 3b and 1 in adult owl and squirrel monkeys , 1983, Neuroscience.

[23]  E. Sanavio,et al.  Semantics of pain in Italy: the Italian version of the McGill Pain Questionnaire , 1985, Pain.

[24]  C. Woolf,et al.  Dynamic alterations in the cutaneous mechanoreceptive fields of dorsal horn neurons in the rat spinal cord , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  N Birbaumer,et al.  Effects of Regional Anesthesia on Phantom Limb Pain Are Mirrored in Changes in Cortical Reorganization , 1997, The Journal of Neuroscience.

[26]  M. Mishkin,et al.  Massive cortical reorganization after sensory deafferentation in adult macaques. , 1991, Science.

[27]  R. LaMotte,et al.  Neurogenic hyperalgesia: central neural correlates in responses of spinothalamic tract neurons. , 1991, Journal of neurophysiology.

[28]  T. Elbert,et al.  Phantom-limb pain as a perceptual correlate of cortical reorganization following arm amputation , 1995, Nature.

[29]  E. Perl,et al.  Sensitization of high threshold receptors with unmyelinated (C) afferent fibers. , 1976, Progress in brain research.

[30]  J. Dostrovsky,et al.  Phantom sensations generated by thalamic microstimulation , 1998, Nature.

[31]  R. E. Yoss,et al.  Significance of Symptoms and Signs in Localization of Involved Root in Cervical Disk Protrusion , 1957, Neurology.

[32]  J. Kaas,et al.  Growth of new brainstem connections in adult monkeys with massive sensory loss. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[33]  木村 淳.  Electrodiagnosis in diseases of nerve and muscle : principles and practice , 1983 .

[34]  F Mauguière,et al.  Abnormal central integration of a dual somatosensory input in dystonia. Evidence for sensory overflow. , 2000, Brain : a journal of neurology.

[35]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[36]  S. Knecht,et al.  Phantom sensations following acute pain , 1998, Pain.

[37]  J. Desmedt,et al.  Thalamic pain syndrome of Dejérine-Roussy. Differentiation of four subtypes assisted by somatosensory evoked potentials data. , 1988, Archives of neurology.

[38]  Ronald Melzack,et al.  Contribution of central neuroplasticity to pathological pain: review of clinical and experimental evidence , 1993, Pain.

[39]  Y. Lamour,et al.  Altered properties and laminar distribution of neuronal responses to peripheral stimulation in the Sml cortex of the arthritic rat , 1983, Brain Research.

[40]  Stephen J. Jones,et al.  Potentials evoked in human and monkey cerebral cortex by stimulation of the median nerve. A review of scalp and intracranial recordings. , 1991, Brain : a journal of neurology.

[41]  T. Hackett,et al.  Thalamic and cortical contributions to neural plasticity after limb amputation. , 2000, Journal of neurophysiology.

[42]  W. Willis,et al.  Responses of primate spinothalamic neurons to graded and to repeated noxious heat stimuli. , 1979, Journal of neurophysiology.

[43]  M. Peschanski,et al.  The organization of spinal pathways to ventrobasal thalamus in an experimental model of pain (the arthritic rat). An electrophysiological study , 1986, Pain.

[44]  J. Kaas,et al.  Large-scale reorganization at multiple levels of the somatosensory pathway follows therapeutic amputation of the hand in monkeys , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  P. M. Rossini,et al.  Short-term brain ‘plasticity’ in humans: transient finger representation changes in sensory cortex somatotopy following ischemic anesthesia , 1994, Brain Research.

[46]  D. R. Kenshalo,et al.  Facilitation of the responses of primate spinothalamic cells to cold and to tactile stimuli by noxious heating of the skin , 1982, PAIN®.

[47]  J. Dostrovsky,et al.  Cortical Involvement in the Induction, But Not Expression, of Thalamic Plasticity , 1999, The Journal of Neuroscience.