Distributed processing of pain and vibration by the human brain

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Journal of Neuroscience, Vol 14, 4095-4108, Copyright © 1994 by Society for Neuroscience

ARTICLE

Distributed processing of pain and vibration by the human brain

RC Coghill, JD Talbot, AC Evans, E Meyer, A Gjedde, MC Bushnell and GH Duncan
Centre de Recherche en Sciences Neurologiques, Universite de Montreal, Quebec, Canada.
Pain is a diverse sensory and emotional experience that likely involves activation of numerous regions of the brain. Yet, many of these areas are also implicated in the processing of nonpainful somatosensory information. In order to better characterize the processing of pain within the human brain, activation produced by noxious stimuli was compared with that produced by robust innocuous stimuli. Painful heat (47-48 degrees C), nonpainful vibratory (110 Hz), and neutral control (34 degrees C) stimuli were applied to the left forearm of right-handed male subjects. Activation of regions within the diencephalon and telencephalon was evaluated by measuring regional cerebral blood flow using positron emission tomography (15O-water-bolus method). Painful stimulation produced contralateral activation in primary and secondary somatosensory cortices (SI and SII), anterior cingulate cortex, anterior insula, the supplemental motor area of the frontal cortex, and thalamus. Vibrotactile stimulation produced activation in contralateral SI, and bilaterally in SII and posterior insular cortices. A direct comparison of pain and vibrotactile stimulation revealed that both stimuli produced activation in similar regions of SI and SII, regions long thought to be involved in basic somatosensory processing. In contrast, painful stimuli were significantly more effective in activating the anterior insula, a region heavily linked with both somatosensory and limbic systems. Such connections may provide one route through which nociceptive input may be integrated with memory in order to allow a full appreciation of the meaning and dangers of painful stimuli. These data reveal that pain-related activation, although predominantly contralateral in distribution, is more widely dispersed across both cortical and thalamic regions than that produced during innocuous vibrotactile stimulation. This distributed cerebral activation reflects the complex nature of pain, involving discriminative, affective, autonomic, and motoric components. Furthermore, the high degree of interconnectivity among activated regions may account for the difficulty of eliminating pathological pain with discrete CNS lesions.

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J Neurophysiol, November 1, 1998; 80(5): 2699 - 2709.
[Abstract] [Full Text] [PDF]

F. A. Lenz, M. Rios, D. Chau, G. L. Krauss, T. A. Zirh, and R. P. Lesser
Painful Stimuli Evoke Potentials Recorded From the Parasylvian Cortex in Humans
J Neurophysiol, October 1, 1998; 80(4): 2077 - 2088.
[Abstract] [Full Text] [PDF]

K. D. Davis, C. L. Kwan, A. P. Crawley, and D. J. Mikulis
Functional MRI Study of Thalamic and Cortical Activations Evoked by Cutaneous Heat, Cold, and Tactile Stimuli
J Neurophysiol, September 1, 1998; 80(3): 1533 - 1546.
[Abstract] [Full Text] [PDF]

F. A. Lenz, M. Rios, A. Zirh, D. Chau, G. Krauss, and R. P. Lesser
Painful Stimuli Evoke Potentials Recorded Over the Human Anterior Cingulate Gyrus
J Neurophysiol, April 1, 1998; 79(4): 2231 - 2234.
[Abstract] [Full Text] [PDF]

P. E. Roland, B. O'Sullivan, and R. Kawashima
Shape and roughness activate different somatosensory areas in the human�brain
PNAS, March 17, 1998; 95(6): 3295 - 3300.
[Abstract] [Full Text] [PDF]

P. Rainville, G. H. Duncan, D. D. Price, B. Carrier, and M. C. Bushnell
Pain Affect Encoded in Human Anterior Cingulate But Not Somatosensory Cortex
Science, August 15, 1997; 277(5328): 968 - 971.
[Abstract] [Full Text]

P. Svensson, S. Minoshima, A. Beydoun, T. J. Morrow, and K. L. Casey
Cerebral Processing of Acute Skin and Muscle Pain in Humans
J Neurophysiol, July 1, 1997; 78(1): 450 - 460.
[Abstract] [Full Text] [PDF]

K. D. Davis, S. J. Taylor, A. P. Crawley, M. L. Wood, and D. J. Mikulis
Functional MRI of Pain- and Attention-Related Activations in the Human Cingulate Cortex
J Neurophysiol, June 1, 1997; 77(6): 3370 - 3380.
[Abstract] [Full Text] [PDF]