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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.
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17(3):
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68(3):
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|
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|
|
|
|
|
|
|
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64(1):
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|
|
|
|
|
|
|
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|
|
|
|
|
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|
|
|
|
|
|
|
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|
|
|
|
|
|
|
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129(4):
963 - 976.
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|
|
|
|
|
|
|
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12(1):
29 - 42.
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|
|
|
|
|
|
|
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16(2):
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[Full Text]
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|
|
|
|
|
|
|
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16(2):
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|
|
|
|
|
|
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129(2):
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[Full Text]
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|
|
|
|
|
|
|
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102(36):
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|
|
|
|
|
|
|
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94(3):
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|
|
|
|
|
|
|
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|
|
|
|
|
|
|
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94(1):
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[Full Text]
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|
|
|
|
|
|
|
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128(4):
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|
|
|
|
|
|
|
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53(11):
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[Full Text]
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|
|
|
|
|
|
|
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83(10):
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[PDF]
|
|
|
|
|
|
|
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92(3):
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[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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[PDF]
|
|
|
|
|
|
|
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[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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[Full Text]
[PDF]
|
|
|
|
|
|
|
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[Full Text]
[PDF]
|
|
|
|
|
|
|
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89(6):
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[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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89(6):
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[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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March 1, 2003;
65(1):
223 - 234.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. L. Phillips, L. J. Gregory, S. Cullen, S. Cohen, V. Ng, C. Andrew, V. Giampietro, E. Bullmore, F. Zelaya, E. Amaro, et al.
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126(3):
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[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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February 1, 2003;
126(2):
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[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. F. M. DaSilva, L. Becerra, N. Makris, A. M. Strassman, R. G. Gonzalez, N. Geatrakis, and D. Borsook
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J. Neurosci.,
September 15, 2002;
22(18):
8183 - 8192.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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J Neurophysiol,
July 1, 2002;
88(1):
464 - 474.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. C. Bushnell
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June 1, 2002;
49(90001):
R2 - 2.
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. Macaluso, C. D. Frith, and J. Driver
Supramodal Effects of Covert Spatial Orienting Triggered by Visual or Tactile Events
J. Cogn. Neurosci.,
April 1, 2002;
14(3):
389 - 401.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Ostrowsky, M. Magnin, P. Ryvlin, J. Isnard, M. Guenot, and F. Mauguiere
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Cereb Cortex,
April 1, 2002;
12(4):
376 - 385.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Fabri, G. Polonara, A. Quattrini, and U. Salvolini
Mechanical Noxious Stimuli Cause Bilateral Activation of Parietal Operculum in Callosotomized Subjects
Cereb Cortex,
April 1, 2002;
12(4):
446 - 451.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. J. Vogt, L. J. Sim-Selley, S. R. Childers, R. G. Wiley, and B. A. Vogt
Colocalization of {micro}-Opioid Receptors and Activated G-Proteins in Rat Cingulate Cortex
J. Pharmacol. Exp. Ther.,
December 1, 2001;
299(3):
840 - 848.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Witting, R. C. Kupers, P. Svensson, L. Arendt-Nielsen; A. Gjedde, and T. S. Jensen
Experimental brush-evoked allodynia activates posterior parietal cortex
Neurology,
November 27, 2001;
57(10):
1817 - 1824.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Fabri, G. Polonara, M. Del Pesce, A. Quattrini, U. Salvolini, and T. Manzoni
Posterior Corpus Callosum and Interhemispheric Transfer of Somatosensory Information: An fMRI and Neuropsychological Study of a Partially Callosotomized Patient
J. Cogn. Neurosci.,
November 1, 2001;
13(8):
1071 - 1079.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. K. Fulbright, C. J. Troche, P. Skudlarski, J. C. Gore, and B. E. Wexler
Functional MR Imaging of Regional Brain Activation Associated with the Affective Experience of Pain
Am. J. Roentgenol.,
November 1, 2001;
177(5):
1205 - 1210.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Timmermann, M. Ploner, K. Haucke, F. Schmitz, R. Baltissen, and A. Schnitzler
Differential Coding of Pain Intensity in the Human Primary and Secondary Somatosensory Cortex
J Neurophysiol,
September 1, 2001;
86(3):
1499 - 1503.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. K. Hofbauer, P. Rainville, G. H. Duncan, and M. C. Bushnell
Cortical Representation of the Sensory Dimension of Pain
J Neurophysiol,
July 1, 2001;
86(1):
402 - 411.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. C. Coghill, I. Gilron, and M. J. Iadarola
Hemispheric Lateralization of Somatosensory Processing
J Neurophysiol,
June 1, 2001;
85(6):
2602 - 2612.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. Vuilleumier, C. Chicherio, F. Assal, S. Schwartz, D. Slosman, and T. Landis
Functional neuroanatomical correlates of hysterical sensorimotor loss
Brain,
June 1, 2001;
124(6):
1077 - 1090.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Olausson, B. Ha, G. H. Duncan, C. Morin, A. Ptito, M. Ptito, S. Marchand, and M. C. Bushnell
Cortical activation by tactile and painful stimuli in hemispherectomized patients
Brain,
May 1, 2001;
124(5):
916 - 927.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Ruben, J. Schwiemann, M. Deuchert, R. Meyer, T. Krause, G. Curio, K. Villringer, R. Kurth, and A. Villringer
Somatotopic Organization of Human Secondary Somatosensory Cortex
Cereb Cortex,
May 1, 2001;
11(5):
463 - 473.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. D. Naliboff, S. W. G. Derbyshire, J. Munakata, S. Berman, M. Mandelkern, L. Chang, and E. A. Mayer
Cerebral Activation in Patients With Irritable Bowel Syndrome and Control Subjects During Rectosigmoid Stimulation
Psychosom Med,
May 1, 2001;
63(3):
365 - 375.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
V. Bonhomme, P. Fiset, P. Meuret, S. Backman, G. Plourde, T. Paus, M. C. Bushnell, and A. C. Evans
Propofol Anesthesia and Cerebral Blood Flow Changes Elicited by Vibrotactile Stimulation: A Positron Emission Tomography Study
J Neurophysiol,
March 1, 2001;
85(3):
1299 - 1308.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Liotti, S. Brannan, G. Egan, R. Shade, L. Madden, B. Abplanalp, R. Robillard, J. Lancaster, F. E. Zamarripa, P. T. Fox, et al.
Brain responses associated with consciousness of breathlessness (air hunger)
PNAS,
February 13, 2001;
98(4):
2035 - 2040.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Bense, T. Stephan, T. A. Yousry, T. Brandt, and M. Dieterich
Multisensory Cortical Signal Increases and Decreases During Vestibular Galvanic Stimulation (fMRI)
J Neurophysiol,
February 1, 2001;
85(2):
886 - 899.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. I. Hobday, Q. Aziz, N. Thacker, I. Hollander, A. Jackson, and D. G. Thompson
A study of the cortical processing of ano-rectal sensation using functional MRI
Brain,
February 1, 2001;
124(2):
361 - 368.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Sawamoto, M. Honda, T. Okada, T. Hanakawa, M. Kanda, H. Fukuyama, J. Konishi, and H. Shibasaki
Expectation of Pain Enhances Responses to Nonpainful Somatosensory Stimulation in the Anterior Cingulate Cortex and Parietal Operculum/Posterior Insula: an Event-Related Functional Magnetic Resonance Imaging Study
J. Neurosci.,
October 1, 2000;
20(19):
7438 - 7445.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Créac'h, P. Henry, J. M. Caillé, and M. Allard
Functional MR Imaging Analysis of Pain-related Brain Activation after Acute Mechanical Stimulation
AJNR Am. J. Neuroradiol.,
August 1, 2000;
21(8):
1402 - 1406.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
C. I. Moore, C. E. Stern, S. Corkin, B. Fischl, A. C. Gray, B. R. Rosen, and A. M. Dale
Segregation of Somatosensory Activation in the Human Rolandic Cortex Using fMRI
J Neurophysiol,
July 1, 2000;
84(1):
558 - 569.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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|
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