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