The Journal of Neurophysiology Vol. 77 No. 6 June 1997, pp. 3370-3380
Copyright ©1997 The American Physiological Society

Functional MRI of Pain- and Attention-Related Activations in the Human Cingulate Cortex

Karen D. Davis¹, Stephen J. Taylor², Adrian P. Crawley³, Michael L. Wood³, and David J. Mikulis³

¹ Department of Surgery, Division of Neurosurgery, ² Department of Psychology, and ³ Department of Medical Imaging, University of Toronto and The Toronto Hospital, Toronto, Ontario M5T 2S8, Canada

Davis, Karen D., Stephen J. Taylor, Adrian P. Crawley,Michael L. Wood, and David J. Mikulis. Functional MRI of pain- and attention-related activations in the human cingulate cortex. J. Neurophysiol. 77: 3370-3380, 1997. The aims of the study were to use functional magnetic resonance imaging (fMRI) to 1) locate pain-related regions in the anterior cingulate cortex (ACC) of normal human subjects and 2) determine whether each subject's pain-related activation is congruent with ACC regions involved in attention-demanding cognitive processes. Ten normal subjects underwent fMRI with a 1.5-T standard commercial MRI scanner. A conventional gradient echo technique was used to obtain data from a single 4-mm sagittal slice of the left ACC, ~3.5 mm from midline. For each subject, interleaved sets of 6 images were obtained during a pain task, an attention-demanding task, and at rest, for a total of 36 images per task. Pain of different intensities was evoked via electrical stimulation of the right median nerve. The attention-demanding task consisted of silent word generation (verbal fluency). Additional experiments obtained data from the right ACC. A pixel-by-pixel statistical analysis of task versus rest images was used to determine task-related activated regions. The pain task resulted in a 1.6-4.0% increase in mean signal intensity within a small region of the ACC. The exact location of this activation varied from subject to subject, but was typically in the posterior part of area 24. The signal intensity changes within this region correlated with pain intensity reported by the subject. The attention-demanding tasks increased the mean signal intensity by 1.3-3.3% in a region anterior and/or superior to the pain-related activation in each subject. The activated region was typically larger than the pain-related activation. In some cases this activation was at or superior to the ACC border, near the supplementary motor area. These regions did not show any pain-intensity-related activation. In one subject both right and left ACC were imaged, revealing bilateral ACC activation during the attention task but only contralateral pain-related activation. These findings shed light on pain- and attention-related cognitive processes. The results provide evidence for a region in the posterior part of the ACC that is involved in pain and a more anterior region involved in other attention-demanding cognitive tasks.

This article has been cited by other articles:

				K. N. Ochsner, J. Zaki, J. Hanelin, D. H. Ludlow, K. Knierim, T. Ramachandran, G. H. Glover, and S. C. Mackey Your pain or mine? Common and distinct neural systems supporting the perception of pain in self and other Soc Cogn Affect Neurosci, June 1, 2008; 3(2): 144 - 160. [Abstract] [Full Text] [PDF]

				J. Wang, M. Korczykowski, H. Rao, Y. Fan, J. Pluta, R. C. Gur, B. S. McEwen, and J. A. Detre Gender difference in neural response to psychological stress Soc Cogn Affect Neurosci, September 1, 2007; 2(3): 227 - 239. [Abstract] [Full Text] [PDF]

				D. A. Seminowicz and K. D. Davis Interactions of Pain Intensity and Cognitive Load: The Brain Stays on Task Cereb Cortex, June 1, 2007; 17(6): 1412 - 1422. [Abstract] [Full Text] [PDF]

				F. W.F. Shum, L.-J. Wu, M.-G. Zhao, H. Toyoda, H. Xu, M. Ren, R. Pinaud, S. W. Ko, Y.-S. Lee, B.-K. Kaang, et al. Alteration of cingulate long-term plasticity and behavioral sensitization to inflammation by environmental enrichment Learn. Mem., April 10, 2007; 14(4): 304 - 312. [Abstract] [Full Text] [PDF]

				M. V. Saarela, Y. Hlushchuk, A. C. d. C. Williams, M. Schurmann, E. Kalso, and R. Hari The Compassionate Brain: Humans Detect Intensity of Pain from Another's Face Cereb Cortex, January 1, 2007; 17(1): 230 - 237. [Abstract] [Full Text] [PDF]

				J.-W. Yang, H.-C. Shih, and B.-C. Shyu Intracortical Circuits in Rat Anterior Cingulate Cortex Are Activated by Nociceptive Inputs Mediated by Medial Thalamus J Neurophysiol, December 1, 2006; 96(6): 3409 - 3422. [Abstract] [Full Text] [PDF]

				C. A. Bagley, S. Ohara, H. C. Lawson, and F. A. Lenz Psychophysics of CNS pain-related activity: binary and analog channels and memory encoding. Neuroscientist, February 1, 2006; 12(1): 29 - 42. [Abstract] [PDF]

				J. Wang, H. Rao, G. S. Wetmore, P. M. Furlan, M. Korczykowski, D. F. Dinges, and J. A. Detre Perfusion functional MRI reveals cerebral blood flow pattern under psychological stress PNAS, December 6, 2005; 102(49): 17804 - 17809. [Abstract] [Full Text] [PDF]

				L.-J. Wu, M.-G. Zhao, H. Toyoda, S. W. Ko, and M. Zhuo Kainate Receptor-Mediated Synaptic Transmission in the Adult Anterior Cingulate Cortex J Neurophysiol, September 1, 2005; 94(3): 1805 - 1813. [Abstract] [Full Text] [PDF]

				E. A. Moulton, M. L. Keaser, R. P. Gullapalli, and J. D. Greenspan Regional Intensive and Temporal Patterns of Functional MRI Activation Distinguishing Noxious and Innocuous Contact Heat J Neurophysiol, April 1, 2005; 93(4): 2183 - 2193. [Abstract] [Full Text] [PDF]

				M. W. Luijpen, D. F. Swaab, J. A. Sergeant, and E. J. A. Scherder Effects of Transcutaneous Electrical Nerve Stimulation (TENS) on Self-Efficacy and Mood in Elderly with Mild Cognitive Impairment Neurorehabil Neural Repair, September 1, 2004; 18(3): 166 - 175. [Abstract] [PDF]

				H. Sidhu, M. Kern, and R. Shaker Absence of increasing cortical fMRI activity volume in response to increasing visceral stimulation in IBS patients Am J Physiol Gastrointest Liver Physiol, August 1, 2004; 287(2): G425 - G435. [Abstract] [Full Text] [PDF]

				T. D. Wager, J. K. Rilling, E. E. Smith, A. Sokolik, K. L. Casey, R. J. Davidson, S. M. Kosslyn, R. M. Rose, and J. D. Cohen Placebo-Induced Changes in fMRI in the Anticipation and Experience of Pain Science, February 20, 2004; 303(5661): 1162 - 1167. [Abstract] [Full Text] [PDF]

				M. Kern, C. Hofmann, J. Hyde, and R. Shaker Characterization of the cerebral cortical representation of heartburn in GERD patients Am J Physiol Gastrointest Liver Physiol, January 1, 2004; 286(1): G174 - G181. [Abstract] [Full Text] [PDF]

				L J Gregory, L Yaguez, S C R Williams, C Altmann, S J Coen, V Ng, M J Brammer, D G Thompson, and Q Aziz Cognitive modulation of the cerebral processing of human oesophageal sensation using functional magnetic resonance imaging Gut, December 1, 2003; 52(12): 1671 - 1677. [Abstract] [Full Text] [PDF]

				C. A. Porro Functional Imaging and Pain: Behavior, Perception, and Modulation Neuroscientist, October 1, 2003; 9(5): 354 - 369. [Abstract] [PDF]

				A. P. Weible, C. Weiss, and J. F. Disterhoft Activity Profiles of Single Neurons in Caudal Anterior Cingulate Cortex During Trace Eyeblink Conditioning in the Rabbit J Neurophysiol, August 1, 2003; 90(2): 599 - 612. [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. The effect of negative emotional context on neural and behavioural responses to oesophageal stimulation Brain, March 1, 2003; 126(3): 669 - 684. [Abstract] [Full Text] [PDF]

				A. L. Brody, M. A. Mandelkern, E. D. London, A. R. Childress, G. S. Lee, R. G. Bota, M. L. Ho, S. Saxena, L. R. Baxter Jr, D. Madsen, et al. Brain Metabolic Changes During Cigarette Craving Arch Gen Psychiatry, December 1, 2002; 59(12): 1162 - 1172. [Abstract] [Full Text] [PDF]

				K. Bornhovd, M. Quante, V. Glauche, B. Bromm, C. Weiller, and C. Buchel Painful stimuli evoke different stimulus-response functions in the amygdala, prefrontal, insula and somatosensory cortex: a single-trial fMRI study Brain, June 1, 2002; 125(6): 1326 - 1336. [Abstract] [Full Text] [PDF]

				C. A. Porro, P. Baraldi, G. Pagnoni, M. Serafini, P. Facchin, M. Maieron, and P. Nichelli Does Anticipation of Pain Affect Cortical Nociceptive Systems? J. Neurosci., April 15, 2002; 22(8): 3206 - 3214. [Abstract] [Full Text] [PDF]

				C. Buchel, K. Bornhovd, M. Quante, V. Glauche, B. Bromm, and C. Weiller Dissociable Neural Responses Related to Pain Intensity, Stimulus Intensity, and Stimulus Awareness within the Anterior Cingulate Cortex: A Parametric Single-Trial Laser Functional Magnetic Resonance Imaging Study J. Neurosci., February 1, 2002; 22(3): 970 - 976. [Abstract] [Full Text] [PDF]

				A. Raz and T. Shapiro Hypnosis and Neuroscience: A Cross Talk Between Clinical and Cognitive Research Arch Gen Psychiatry, January 1, 2002; 59(1): 85 - 90. [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]

				J. P. Johansen, H. L. Fields, and B. H. Manning The affective component of pain in rodents: Direct evidence for a contribution of the anterior cingulate cortex PNAS, June 12, 2001; (2001) 141218998. [Abstract] [Full Text] [PDF]

				R. J. Morecraft, J. L. Louie, J. L. Herrick, and K. S. Stilwell-Morecraft Cortical innervation of the facial nucleus in the non-human primate: A new interpretation of the effects of stroke and related subtotal brain trauma on the muscles of facial expression Brain, January 1, 2001; 124(1): 176 - 208. [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]

				U. Ladabaum, S. Minoshima, and C. Owyang Pathobiology of Visceral Pain: Molecular Mechanisms and Therapeutic Implications V. Central nervous system processing of somatic and visceral sensory signals Am J Physiol Gastrointest Liver Physiol, July 1, 2000; 279(1): G1 - G6. [Abstract] [Full Text] [PDF]

				K. D. Davis, W. D. Hutchison, A. M. Lozano, R. R. Tasker, and J. O. Dostrovsky Human Anterior Cingulate Cortex Neurons Modulated by Attention-Demanding Tasks J Neurophysiol, June 1, 2000; 83(6): 3575 - 3577. [Abstract] [Full Text] [PDF]

				F. Wei, P. Li, and M. Zhuo Loss of Synaptic Depression in Mammalian Anterior Cingulate Cortex after Amputation J. Neurosci., November 1, 1999; 19(21): 9346 - 9354. [Abstract] [Full Text] [PDF]

				R. Peyron, L. Garcia-Larrea, M.-C. Gregoire, N. Costes, P. Convers, F. Lavenne, F. Mauguiere, D. Michel, and B. Laurent Haemodynamic brain responses to acute pain in humans: Sensory and attentional networks Brain, September 1, 1999; 122(9): 1765 - 1780. [Abstract] [Full Text] [PDF]

				S. Hamdy, D. J. Mikulis, A. Crawley, S. Xue, H. Lau, S. Henry, and N. E. Diamant Cortical activation during human volitional swallowing: an event-related fMRI study Am J Physiol Gastrointest Liver Physiol, July 1, 1999; 277(1): G219 - G225. [Abstract] [Full Text] [PDF]

				P. Rainville, R. K. Hofbauer, G. H. Duncan, M. C. Bushnell, and D. D. Price Cerebral Mechanisms of Hypnotic Induction and Suggestion J. Cogn. Neurosci., January 1, 1999; 11(1): 110 - 125. [Abstract] [Full Text]

				C. A. Porro, V. Cettolo, M. P. Francescato, and P. Baraldi Temporal and Intensity Coding of Pain in Human Cortex J Neurophysiol, December 1, 1998; 80(6): 3312 - 3320. [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]

				J. P. Johansen, H. L. Fields, and B. H. Manning The affective component of pain in rodents: Direct evidence for a contribution of the anterior cingulate cortex PNAS, July 3, 2001; 98(14): 8077 - 8082. [Abstract] [Full Text] [PDF]