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Distributed Processing of Pain and Vibration by the Human Brain

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Distributed Processing of Pain and Vibration by the Human Brain The Journal of Neuroscience, July 1994, 14(7): 4095-4108 Distributed Processing of Pain and Vibration by the Human Brain Robert C. Coghill,’ Jeanne D. Talbot,’ Alan C. Evans,* Ernst Meyer,2 Albert Gjedde,* M. Catherine Bushnell,’ and Gary H. Duncan’ ‘Centre de Recherche en Sciences Neurologiques and Facultk de Mbdecine Dentaire, Universitb de Mont&al, Montreal, Quebec, Canada H3C 3J7 and ‘Positron Imaging Laboratories, McConnell Brain Imaging Center, Montreal Neurological Institute, Montreal, Quebec, Canada H3A 2B4 Pain is a diverse sensory and emotional experience that [Key words: pain, vibration, thalamus, positron emission likely involves activation of numerous regions of the brain. tomography, human, primary somatosensory cortex, insula, Yet, many of these areas are also implicated in the pro- secondary somatosensory cortex, heat, cingulate cortex] cessing of nonpainful somatosensory information. In order to better characterize the processing of pain within the hu- man brain, activation produced by noxious stimuli was com- An understandingof nociceptive processingin the human brain pared with that produced by robust innocuous stimuli. Painful has remained elusive, perhaps becauseof the complexity and heat (47-48”C), nonpainful vibratory (110 Hz), and neutral multiplicity of mechanismssupporting this essential sensory control (34°C) stimuli were applied to the left forearm of right- experience. Early observations by neurosurgeonsled to the view handed male subjects. Activation of regions within the di- that pain is a diencephalic phenomenon and that the telen- encephalon and telencephalon was evaluated by measuring cephalonhas little to do with pain perception (Head and Holmes, regional cerebral blood flow using positron emission tomog- 1911; Penfield and Boldrey, 1937). These observations, how- raphy (150-water-bolus method). ever, were founded largely on the results of focal lesions and Painful stimulation produced contralateral activation in pri- focal stimulation and did not examine the possibility that ac- mary and secondary somatosensory cortices (SI and SII), tivation of multiple brain regions may be essentialfor the ex- anterior cingulate cortex, anterior insula, the supplemental perience of pain. Modern theories of pain processing(Melzack motor area of the frontal cortex, and thalamus. Vibrotactile and Casey, 1968; Price, 1988) acknowledgethat multiple brain stimulation produced activation in contralateral SI, and bi- regions may likely play key roles in nociceptive processingand laterally in SII and posterior insular cortices. A direct com- postulate that areasinvolved in discriminative aspectsof tactile parison of pain and vibrotactile stimulation revealed that sensation, such as ventroposterior thalamus (VP) and primary both stimuli produced activation in similar regions of SI and somatosensorycortex (SI), are also involved in discriminative SII, regions long thought to be involved in basic somatosen- aspectsof nociception, while medial areasof thalamus and their sory processing. In contrast, painful stimuli were signifi- diffuse cortical projection sites-for example, frontal, cingulate, cantly more effective in activating the anterior insula, a re- and insular cortices (Jones and Seavitt, 1974; Kaufman and gion heavily linked with both somatosensory and limbic Rosenquist, 198.5; Royce and Mourey, 1985; Friedman and systems. Such connections may provide one route through Murray, 1986)-are involved in the affective aspectsof noci- which nociceptive input may be integrated with memory in ception (Bowsher, 1957;Price and Dubner, 1977;Melzack, 1986). order to allow a full appreciation of the meaning and dangers This functional segregationhas been supported by a limited of painful stimuli. number of lesion and stimulation studies in humans and mon- These data reveal that pain-related activation, although key. Lesions to SI in monkey (Kenshalo et al., 1991) and to the predominantly contralateral in distribution, is more widely region around secondary somatosensorycortex (SII) in human dispersed across both cortical and thalamic regions than (Greenspanand Winfield, 1992) lead to deficits in pain discrim- that produced during innocuous vibrotactiie stimulation. This ination. Further, localized pain has been evoked from micro- distributed cerebral activation reflects the complex nature stimulation of the baseof VP in humans(Dostrovsky et al., 1990; of pain, involving discriminative, affective, autonomic, and Len2 et al., 1993). In contrast, lesions to anterior cingulate or motoric components. Furthermore, the high degree of inter- insular cortices in humans have been reported to alter affective connectivity among activated regions may account for the responsesto pain (Foltz and Lowell, 1962; Hurt and Ballantine, difficulty of eliminating pathological pain with discrete CNS 1973; Berthier et al., 1988). lesions. Nevertheless,the conspicuouspaucity of nociceptive neurons in primary somatosensorypathways continues to raise doubts Received Aug. 5, 1993; revised Dec. 27, 1993; accepted Feb. 2, 1994. about the importance ofthese areasto pain perception. Although We thank Sylvain Milot, Peter Neelin, Sean Marrett, and the staffofthe McConnell Brain Imaging Centre and the Medical Cyclotron Unit for their technical assis- anatomical studies in primates show projections from regions tance. This work was supported by the Medical Research Council of Canada. of the dorsal horn that contain nociceptive neurons to parts of R.C.C. was supported by an MRC fellowship. VP thalamus (Apkarian and Hodge, 1989; Craig, 1992) most Correspondence should be addressed to G. H. Duncan, D.D.S., Ph.D., DC- partement de Stomatologie, Facultt de Mtdecine Dentaire, Universitt de Mon- investigations have yielded only a small percentageof neurons trkal, C.P. 6 128, Succursale A, Montreal, Quebec, Canada H3C 357. in VP that respond to noxious stimuli in the primate (Kenshalo Copyright 0 1994 Society for Neuroscience 0270-6474/94/144095-14$05.00/O et al., 1980; Casey and Morrow, 1983; Bushnell and Duncan, 4096 Coghill et al. - Processing of Pain and Vibration by the Human Brain 1987; Bushnell et al. 1993). Similarly, although regions of pri- mate thalamus containing nociceptive cells project to SI and SII Materials and Methods (Kenshalo et al., 1980; Friedman and Murray, 1986; Gingold Subjects. Nine right-handed pain-free male subjects between 20 and 35 et al., 199 1; Rausell and Jones, 199 l), relatively few nociceptive years old (mean, 27 years) participated in this experiment. Subjects gave neurons have been identified in these cortical regions (Kenshalo informed consent acknowledging that (1) they would be exposed to low and Isensee, 1983; Kenshalo et al., 1988; Dong et al., 1989). doses of radiation and heat-induced pain, (2) the methods to be used and the risks involved were clearly explained and understood, and (3) Other data question the view that nociceptive processing in they were free to withdraw from the experiment at any time without “extralemniscal” pathways is restricted exclusively to the affec- prejudice. All procedures were approved by the Ethics and Research tive/motivational aspects of pain perception. In awake monkeys Committee of the Montreal Neurological Institute and Hospital and we have found cells in the region ofthe thalamic nucleus parafas- were in accordance with the Declaration of Human Rights, Helsinki, 1975. cicularis (Pf) that respond differentially to perceptually liminal Stimulation procedures. Neutral 34°C thermal (Control), 4748°C differences in noxious heat stimuli, and thus could provide a painful heat (Pain), and 110 Hz vibrotactile (Vibration) stimuli were neural substrate for the discrimination of pain intensity (Bush- employed as experimental conditions that were presented to the subjects nell and Duncan, 1989). Further, quantitative psychophysical during separate scans. Thermal stimuli were produced by a computer- data from a case study involving anterior capsulotomy indicate controlled contact thermode with a rise time of 6”Usec (Larson et al., 1987) and 110 Hz vibrotactile stimuli were delivered by an electric that lesions which interrupt thalamocortical projections to the vibrator (Daito, Osaka, Japan). Each device had a circular stimulating anterior cingulate and frontal cortices reduce the perceived in- surface of 1 cm’, that was placed on the skin of the subject’s left (non- tensity of noxious heat stimuli (Talbot et al., 1993). dominant) forearm. Recent advances in functional imaging now provide a pow- During each 60 set scanning period, one of the three stimulus con- ditions (Control, Pain, Vibration) was presented to the subject. Stimuli erful tool for addressing questions about cerebral mechanisms were delivered at six marked locations (3 x 2 matrix with interstimulus of pain in normal humans. These techniques allow a simulta- distance of 3 cm) on the ventral surface of the forearm. In order to neous assessment of activation within multiple brain regions, minimize sensitization or habituation that may result from repeated thereby providing global information unattainable in individual presentations of noxious heat (Price et al., 1983) stimuli were rotated stimulation, lesion, or recording experiments. In an initial study among the six locations, with a 6 set presentation at each site followed by a 4 set interstimulus level. The painful heat was presented as a two- using positron emission tomography (PET) to examine the re- step pulse, in which the temperature was held at 47°C for 5 set and then
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