Cerebral processing of acute skin and muscle pain in humans

Journal of Neurophysiology

Volumn 78, Issue 1, 1997, Pages 450-460

  Svensson, Peter ^a   Minoshima, Satoshi ^b   Beydoun, Ahmad ^b,d   Morrow, Thomas J ^b,c,d   Casey, Kenneth L ^b,c,d  

^a AARHUS UNIVERSITY   (Denmark)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BRAIN BLOOD FLOW; CINGULATE GYRUS; ELECTROSTIMULATION; HUMAN; HUMAN EXPERIMENT; MALE; MYALGIA; NERVE CONDUCTION; NOCICEPTION; PAIN ASSESSMENT; PAIN THRESHOLD; PARIETAL LOBE; POSITRON EMISSION TOMOGRAPHY; PREFRONTAL CORTEX; PREMOTOR CORTEX; PRIORITY JOURNAL; SOMATOSENSORY CORTEX;

EID: 0030877866     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1997.78.1.450     Document Type: Article

References (80)

1. ALBE-FESSARD, D., BERKLEY, K. J., KRUGKR, L., RALSTON, H. J., III, AND WILLIS, W. D. Diencephalic mechanisms of pain sensation. Brain Res. Rev. 9: 217-296, 1985.
2. BASSETTI, C., BOGOUSSLAVSKY, J., AND REGLI, F. Sensory syndromes in parietal stroke. Neurology 43: 1941-1949, 1993.
3. BERKLEY, K. J. AND HUBSCHER, C. H. Are there separate central nervous system pathways for touch and pain? Nature Med. 1: 766-773, 1995.
4. BEYDOUN, A., MORROW, T. J., SHEN, J. F., AND CASEY, K. L. Variability of laser-evoked potentials: attention, arousal and lateralized differences. Electroencephalogr. Clin. Neurophysiol. 88: 173-181, 1993.
5. BOOKSTEIN, F. L. Principal warps: thin plate splines and the decomposition of deformations. IEEE Trans. Pattern Analysis Machine Intel. 11: 567-585, 1989.
6. 2 laser stimuli causing pain. Exp. Brain Res. 55: 158-166, 1984.
7. BROMM, B. AND TREEDE, R.-D. Laser-evoked cerebral potentials in the assessment of cutaneous pain sensitivity in normal subjects and patients. Rev. Neurol 147: 625-643, 1991.
8. BURTON, H., VIDEEN, T. O., AND RAICHLE, M. E. Tactile-vibration-activation foci in insular and parietal-opercular cortex studied with positron emission tomography: mapping the second somatosensory area in humans. Somatosens. Mot. Res. 10: 297-308, 1993.
9. CASEY, K. L., MINOSHIMA, S., BERGER, K. L., KOEPPE, R. A., MORROW, T. J., AND FREY, K. A. Positron emission tomographic analysis of cerebral structures activated by repetitive heat stimuli. J. Neurophysiol. 71: 802-807, 1994.
10. CASEY, K. L., MINOSHIMA, S., MORROW, T. J., AND KOEPPE, R. A. A comparison of human cerebral activation patterns during cutaneous warmth, heat pain, and deep cold pain. J. Neurophysiol. 76: 571-581, 1996.
11. CASEY, K. L. AND MORROW, T. J. Ventral posterior thalamic neurons differentially responsive to noxious stimulation of the awake monkey. Science Wash. DC 221: 675-677, 1983.
12. CASEY, K. L., ZUMBERG, M., HESLEP, H., AND MORROW, T. J. Afferent modulation of warmth sensation and heat pain in the human hand. Somatosens. Mot. Res. 10: 327-337, 1993.
13. CHEN, A.C.N. AND BROMM, B. Pain-related generators of laser-evoked brain potentials. In: Pain and the Brain: From Nociception to Cognition, edited by B. Bromm and J. E. Desmedt. New York: Raven, 1995, p. 245-266.
14. CHUDLER, E. H., ANTON, F., DUBNER, R., AND KENSHALO, D. R., JR. Responses of nociceptive SI neurons in monkeys and pain sensation in humans elicited by noxious thermal stimulation: effects of interstimulus interval. J. Neurophysiol. 63: 559-569, 1990.
15. CHUDLER, E. H. AND DONG, W. K. The role of basal ganglia in nociception and pain. Pain 60: 3-38, 1995.
16. COGHILL, R. C., TALBOT, J. D., EVANS, A. C., MEYER, E., GJEDDE, A., BUSHNELL, M. C., AND DUNCAN, G. H. Distributed processing of pain and vibration by the human brain. J. Neurosci. 14: 4095-4108, 1994.
17. CRAIG, A. D., BUSHNELL, M. C., ZHANG, E.-T., AND BLOMQUIST, A. A thalamic nucleus specific for pain and temperature sensation. Nature Lond. 372: 770-773, 1994.
18. DERBYSHIRE, S.W.G., JONES, A.K.P., DEVANI, P., FRISTON, K. J., HARRIS, M., PEARCE, S., WATSON, J.D.G., AND FRACKOWIAK, R.S.J. Cerebral responses to pain in patients with atypical facial pain measured by positron emission tomography. J. Neurol. Neurosurg. Psychiatry 57: 1166-1172, 1994.
19. DIPIERO, V., JONES, A.K.P., IANNOTTI, F., POWELL, M., PERANI, D., LENZI, G. L. AND FRACKOWIAK, R.S.J. Chronic pain: a PET study of the central effects of percutaneous high cervical cordotomy. Pain 46: 9-12, 1991.
20. DONG, W. K., CHUDLER, E. H., SUGIYAMA, K., ROBERTS, V. J., AND HAYASHI, T. Somatosensory, multisensory, and task-related neurons in cortical area 7b (PF) of unanesthetized monkeys. J. Neurophysiol. 72: 542-564, 1994.
21. DONG, W. K., HAYASHI, T., ROBERTS, V. J., FUSCO, B. M., AND CHUDLER, E. H. Behavioral outcome of posterior parietal cortex injury in the monkey. Pain 64: 579-586, 1996.
22. DUBNER, R. Hyperalgesia in response to injury to cutaneous and deep tissues. In: Orofacial Pain and Temporomandibular Disorders, edited by J. R. Fricton and R. Dubner. New York: Raven, 1995, p. 61-71.
23. EKEROT, C. F., GARWICZ, M., AND SCHOUENBORG, J. Topography and nociceptive receptive fields of climbing fibres projecting to the cerebellar anterior lobe in the cat. J. Physiol. Lond. 441: 257-274, 1991a.
24. EKEROT, C. F., GARWICZ, M., AND SCHOUENBORG, J. The postsynaptic dorsal column pathway mediates cutaneous nociceptive information to cerebellar climbing fibres in the cat. J. Physiol. Lond. 441: 275-284, 1991b.
25. FOREMAN, R. D., SCHMIDT, R. F., AND WILLIS, W. D. Convergence of muscle and cutaneous input onto primate spinothalamic tract neurons. Brain Res. 124: 555-560, 1977.
26. FOX, P. T. AND RAICHLE, M. E. Stimulus rate dependence of regional cerebral blood flow in human striate cortex, demonstrated by positron emission tomography. J. Neurophysiol. 51: 1109-1120, 1984.
27. FRIEDMAN, D. P. AND MURRAY, E. A. Thalamic connectivity of the second somatosensory area and the neighboring somatosensory fields of the lateral sulcus of the macaque. J. Comp. Neurol. 252: 348-373, 1986.
28. FRIEDMAN, D. P., MURRAY, E. A., O'NEILL, J. B., AND MISHKIN, M. Cortical connections of the somatosensory fields of the lateral sulcus of macaques: evidence for a corticolimbic pathway for touch. J. Comp. Neurol. 252: 323-347, 1986.
29. FRISTON, K. J., FRITH, C. D., LIDDLE, P. F., AND FRACKOWIAK, R.S.J. Comparing functional (PET) images: the assessment of significant change. J. Cereb. Blood Flow Metab. 11: 690-699, 1991.
30. GANDEVIA, S. C., BURKE, D., AND MCKEON, B. The projection of muscle afferents from the hand to cerebral cortex in man. Brain 107: 1-13, 1984.
31. GREENSPAN, J. D. AND WINFIELD, J. A. Reversible pain and tactile deficits associated with a cerebral tumor compressing the posterior insula and parietal operculum. Pain 58: 29-39, 1992.
32. HANSON, J. Hypoglossal high threshold afferents projecting to the secondary somatosensory area in the cat. Arch. Ital. Biol. 123: 63-68, 1985.
33. HARI, R., KAUKORANTA, E., REINIKAINEN, K., HUOPANIEMIE, T., AND MAUNO, J. Neuromagnetic localization of cortical activity evoked by painful dental stimulation in man. Neurosci. Lett. 42: 77-82, 1983.
34. HORE, J., PRESTON, J. B., DURKOVIC, R. G., AND CHENEY, P. D. Responses of cortical neurons (areas 3a and 4) to ramp stretch of hind limb muscles in the baboon. J. Neurophysiol. 39: 484-500, 1976.
35. HSIEH, J.-C., BELFRAGE, M., STONE-ELANDER, S., HANSSON, P., AND INGVAR, M. Central representation of chronic ongoing neuropathic pain studied by positron emission tomography. Pain 63: 225-236, 1995.
36. HSIEH, J., HAGERMARK, O., STAHLE-BACKDAHL, M., ERICSON, K., ERIKSSON, L., STONE-BLANDER, S., AND INGVAR, M. Urge to scratch represented in the human cerebral cortex during itch. J. Neurophysiol. 72: 3004-3008, 1994.
37. HSIEH, J.-C., STRÅHLE-BÄCKDAHL, M., HÄGERMARK, Ö, STONE-ELANDER, S., ROSENQUIST, G., AND INGVAR, M. Traumatic nociceptive pain activates the hypothalamus and the periaqueductal gray: a positron emission tomography study. Pain 64: 303-314, 1996.
38. 2 stimulation of nasal mucosa: a neuromagnetoencephalographic study in man. Electroencephalogr. Clin. Neurophysiol. 64: 347-349, 1986.
39. IADAROLA, M. J., MAX, M. B., HERMAN, K. F., BYAS-SMITH, M. G., COGHILL, R. C., GRACELY, R. H., AND BENNETT, G. J. Unilateral decrease in thalamic activity observed with positron emission tomography in patients with chronic neuropathic pain. Pain 63: 55-64, 1995.
40. IWAMURA, Y., KNIFFKI, K.-D., MIZAUMURA, K., AND WILBERG, K. Responses of feline SI neurones to noxious stimulation of muscle and tendon (Abstract). Pain 1: 213, 1981.
41. JIE, W. AND PEI-XI, C. Cerebellar evoked potential elicited by stimulation of C-fiber in saphenous nerve of cat. Brain Res. 522: 144-146, 1990.
42. JONES, A.K.P., BROWN, W. D., FRISTON, K. J., QI, L. Y., AND FRACKOWIAK, R.S.J. Cortical and subcortical localization of response to pain in man using positron emission tomography. Proc. R. Soc. Lond. B Biol. Sci. 244: 39-44, 1991.
43. JONES, A.K.P. AND DERBYSHIRE, S.W.G. Positron emission tomography as a tool for understanding the cerebral processing of pain In: Touch, Temperature, and Pain in Health and Disease: Mechanisms and Assessments, edited by J. Boivie, P. Hansson, and U. Lindblom. Seattle: IASP, 1994, p. 491-520.
44. 2 stimulation in man. Neurosci. Lett. 192: 45-48, 1995.
45. KENSHALO, D. R., JR., CHUDLER, E. H., ANTON, F., AND DUBNER, R. SI cortical nociceptive neurons participate in the encoding proces by which monkeys perceive the intensity of noxious stimulation. Brain Res. 454: 378-382, 1988.
46. KENSHALO, D. R., JR. AND DOUGLASS, D. K. The role of the cerebral cortex in the experience of pain. In: Pain and the Brain: From Nociception to Cognition, edited by B. Bromm and J. E. Desmedt. New York: Raven, 1995, p. 21-34.
47. KENSHALO, D. R., JR. AND WILLIS, W. D., JR. The role of the cerebral cortex in pain sensation. In: Cerebral Cortex, edited by E. G. Jones and A. Peters. New York: Plenum, 1991, p. 153-212.
48. KIM, S.-G., UGURBIL, K., AND STRICK, P. L. Activation of a cerebellar output nucleus during cognitive processing. Science Wash. DC 265: 949-951, 1994.
49. KLEMENT, W. AND ARNDT, J. O. The role of nociceptors of cutaneous veins in the mediation of cold pain in man. J. Physiol. Lond. 449: 73-83, 1992.
50. LAMOUR, Y., GUILBAUD, G., AND WILLER, J. C. Rat somatosensory (SmI) cortex. II. Laminar and columnar organization of noxious and non-noxious inputs. Exp. Brain Res. 49: 46-54, 1983a.
51. LAMOUR, Y., WILLER, J. C., AND GUILBAUD, G. Rat somatosensory (SmI) cortex. I. Characteristics of neuronal responses to noxious stimulation and comparison with responses to non-noxious stimulation. Exp. Brain Res. 49: 35-45, 1983b.
52. LAUDAHN, R., KOHLHOFF, H., AND BROMM, B. Magnetoencephalography in the investigation of the cortical pain processing system. In: Pain and the Brain: From Nociception to Cognition, edited by B. Bromm and J. E. Desmedt. New York: Raven, 1995, p. 267-282.
53. LENZ, F. A., GRACELY, R. H., ROMANOSKI, A. J., HOPE, E. J., ROWLAND, L. H., AND DOUGHERTY, P. M. Stimulation in the human somatosensory thalamus can reproduce both the affective and sensory dimensions of previously experienced pain. Nature Med. 1: 910-913, 1995.
54. MELZACK, R. AND CASEY, K. L. Sensory, motivational and central control determinants of pain: a new conceptual model. In: The Skin Senses, edited by D. R. Kenshalo. Springfield, IL: Thomas, 1968, p. 423-443.
55. MENSE, S. Nociception from skeletal muscle in relation to clinical muscle pain. Pain 54: 241-289, 1993.
56. MEYER, E., FERGUSON, S.S.G., ZATORRE, R. J., ALIVISATOS, B., MARRETT, S., EVANS, A. C., AND HAKIM, A. M. Attention modulates somatosensory cerebral blood flow response to vibrotactile stimulation as measured by positron emission tomography. Ann. Neurol. 29: 440-443, 1991.
57. MIDDLETON, F. A. AND STRICK, P. L. Anatomical evidence for cerebellar and basal ganglia involvement in higher cognitive function. Science Wash. DC 266: 458-461, 1994.
58. MINOSHIMA, S., BERGER, K. L., LEE, K. S., AND MINTUN, M. A. An automated method for rotational correction and centering of three-dimensional functional brain images. J. Nucl. Med. 33: 1579-1585, 1992.
59. MINOSHIMA, S., KOEPPE, R. A., FREY, K. A., AND KUHL, D. E. Anatomical standardization: linear scaling and non-linear warping of functional brain images. J. Nucl. Med. 35: 1528-1537, 1994.
60. MINOSHIMA, S., KOEPPE, R. A., MINTUN, M. A., BERGER, K. L., TAYLOR, S. F., FREY, K. A., AND KUHL, D. E. Automated detection of the intercommisural (AC-PC) line for stereotactic localization of functional brain images. J. Nucl. Med. 34: 322-329, 1993.
61. PAUS, T., PETRIDES, M., EVANS, A. C., AND MEYER, E. Role of the human anterior cingulate cortex in the control of oculomotor, manual, and speech responses: a positron emission tomography study. J. Neurophysiol. 70: 453-469, 1993.
62. 2 laser pulses in humans: evidence on afferent mechanisms and the influence of varying the stimulus conditions. Pain 34: 261-269, 1988.
63. ROBINSON, C. J. AND BURTON, H. Somatic submodality distribution within the second somatosensory (SII), 7b, retroinsular, postauditory, and granular insular cortical areas of M. fascicularis. J. Comp. Neurol. 192: 93-108, 1980.
64. SCHMAMHMANN, J. D. AND LEIFER, D. Parietal pseudothalamic pain syndrome. Arch. Neurol. 49: 1032-1037, 1992.
65. SCHMAMHMANN, J. D. AND PANDYA, D. N. Anatomical investigation of projections from thalamus to the posterior parietal association cortices in rhesus monkey. J. Comp. Neurol. 295: 299-326, 1990.
66. SESSLE, B. J. Masticatory muscle disorders: basic science perspectives. In: Temporomandibular Disorders and Related Pain Conditions, edited by B. J. Sessle, P. S. Bryant, and R. A. Dionne. Seattle: IASP, 1995, p. 47-61.
67. SIKES, R. W. AND VOGT, B. A. Nociceptive neurons in area 24 of rabbit cingulate cortex. J. Neurophysiol. 68: 1720-1732, 1993.
68. SIMONE, D. A., MARCHETTINI, P., CAPUTI, G., AND OCHOA, J. L. Identification of muscle afferents subserving sensation of deep pain in humans. J. Neurophysiol. 72: 883-889, 1994.
69. SIRISKO, M. A. AND SESSLE, B. J. Corticobulbar projections and orofacial muscle afferent inputs of neurons in primate sensorimotor cerebral cortex. Exp. Neurol. 82: 716-720, 1983.
70. STEPHAN, K. M., FINK, G. R., PASSINGHAM, R. E., SILBERSWEIG, D., CEBALLOS-BAUMANN, A. O., FRITH, C. D., AND FRACKOWIAK, R.S.J. Functional anatomy of the mental representation of upper extremity movements in healthy subjects. J. Neurophysiol. 73: 373-386, 1995.
71. SVENSSON, P. AND ARENDT-NIELSEN, L. Induction and assessment of experimental muscle pain. J. Electromyogr. Kinesiol. 5: 131-140, 1995.
72. SWEET, W. H. Cerebral localization of pain. In: New Perspectives in Cerebral Localization, edited by R. A. Thompson and J. R. Green. New York: Raven, 1982, p. 205-242.
73. TALAIRACH, J. AND TOURNOUX, P. Co-Planar Stereotaxic Atlas of the Human Brain. Stuttgart, Germany: Thieme, 1988.
74. TALBOT, J. D., MARRETT, S., EVANS, A. C., MEYER, E., BUSHNELL, M. C., AND DUNCAN, G. H. Multiple representations of pain in human cerebral cortex. Science Wash. DC 251: 1355-1358, 1991.
75. TREEDE, R.-D., MEYER, R. A., RAJA, S. N., AND CAMPELL, J. N. Evidence for two different heat transduction mechanisms in nociceptive primary afferents innervating monkey skin. J. Physiol. Lond. 483: 747-758, 1995.
76. VECCHIET, L., DRAGANI, L., BIGOTINA, P., OBLETTER, G., AND GIAMBERARDINO, A. Experimental referred pain and hyperalgesia from muscles in humans. In: New Trends in Referred Pain and Hyperalgesia, edited by L. Vecchiet, D. Albe-Fessard, and U. Lindblom. Amsterdam: Elsevier, 1993, p. 239-249.
77. WENZEL, R., BARTENSTEIN, P., DIETERICH, M., DANEK, A., WEINDL, A., MINOSHIMA, S., ZIEGLER, S., SCHWAIGER, M., AND BRANDT, T. Deactivation of human visual cortex during involuntary ocular oscillations: a PET activation study. Brain 119: 101-110, 1996.
78. WIESENDANGER, M. Input from muscle and cutaneous nerves of the hand and forearm to neurones of the precentral gyrus of the baboons and monkeys. J. Physiol. Lond. 228: 203-219, 1973.
79. WORSLEY, K. J., EVANS, A. C., MARRETT, S., AND NEELIN, P. A three-dimensional statistical analysis for CBF activation studies in human brain. J. Cereb. Blood Flow Metab. 12: 900-918, 1992.
80. YASUI, I., ITOH, K., KAMIYA, H., INO, T., AND MIZUNO, N. Cingulate gyrus of the cat receives projection fibers from the thalamic region ventral to the ventral border of the ventrobasal complex. J. Comp. Neurol. 274: 91-100, 1988.