Gender differences in patterns of cerebral activation during equal experience of painful laser stimulation
Derbyshire, Stuart W. G., Nichols, Thomas E., Firestone, Leonard L., Townsend, David W., Ph.D. and Jones, Anthony K. P.. (2002) Gender differences in patterns of cerebral activation during equal experience of painful laser stimulation. The Journal of Pain, Vol.3 (No.5). pp. 401-411. ISSN 15265900Full text not available from this repository.
Official URL: http://dx.doi.org/10.1054/jpai.2002.126788
A previous functional imaging study demonstrated greater female response in the anterior insula and thalamus and left prefrontal activation in men and right prefrontal activation in women during equal heat intensity but unequal pain experience. For the current study, subjective intensities of noxious heat delivered to the back of the right hand were equalized across subjects, and regional cerebral blood flow was recorded by using positron emission tomography. The female subjects required less laser energy before reporting pain, but the difference was not significant. Correlation of regional cerebral blood flow with subjective pain experience in the whole group showed significant bilateral responses in the parietal, lateral premotor, prefrontal, secondary somatosensory, anterior cingulate and insula cortices, as well as the thalamus. There was significantly greater activation in the left, contralateral, prefrontal, primary and secondary somatosensory, parietal, and insula cortices in the male subjects compared with the female subjects and greater response in the perigenual cingulate cortex in the female subjects. Our study is the first to associate consistent pain experience with gender differences in central response. These differences may relate to differential processing of acute pain with implications for clinical disorders that show a female dominance. The subtle behavioral differences and inconsistent findings across studies, however, suggest the need for caution and further experimentation before speculating further.
|Item Type:||Journal Article|
|Subjects:||Q Science > QA Mathematics
Q Science > QP Physiology
|Divisions:||Faculty of Science > Statistics|
|Library of Congress Subject Headings (LCSH):||Nociceptors -- Sex differences, Pain -- Sex factors, Cerebral circulation -- Imaging, Cerebral cortex, Pain -- Data processing|
|Journal or Publication Title:||The Journal of Pain|
|Date:||28 January 2002|
|Page Range:||pp. 401-411|
|Access rights to Published version:||Restricted or Subscription Access|
|References:||depression. Biol Psychiatry 34:687-689, 1993 2. Allen LS, Gorski RA: Sexual dimorphism of the anterior commisure and mass intermedia and massa intermedia of the human brain. J Comp Neurol 312:97-104, 1991 3. Allen LS, Gorski RA: Sex difference in the bed nucleus of the stria terminalis of the human brain. J Comp Neurol 302: 697-706, 1990 4. Allen LS, Hines M, Shryne JE, Gorski RA: Two sexually dimorphic cell groups in the human brain. J Neurosci 9:497- 506, 1989 5. Baamonde AI, Hidalgo A, Andres-Trelles F: Sex-rlated differences in the effects of morphine and stress on visceral pain. Neuropharmacology 28:967-970, 1989 6. Barbaresi P, Minelli A, Manzoni T: Thalamic connections of the second somatic sensory in cats studied with anterograde and retrograde tract-tracing techniques. Neuroscience 46:149-163, 1992 7. Benedetti F: The sensory and affective components of pain. Behav Brain Sci 20:439-440, 1997 8. Berkley KJ: Sex differences in pain. Behav Brain Sci 20:371- 380, 1997 9. Berman S, Munakata J, Naliboff B, Chang L, Mandelkern M, Silverman D, Kovalik E, Mayer E: Gender differences in regional brain response to visceral pressure in IBS patients. Eur J Pain 4:157-72, 2000 10. Burns JW, Kubilus A, Michael E: Cognitive-behavioral factors in the management of chronic low back pain: Conceptualization of evidence of treatment efficacy. Curr Rev Pain 3:300-307, 1999 11. Casey KL, Morrow TJ, Lorenz J, Minoshima S: Temporal and spatial dynamics of human forebrain activity during heat pain: Analysis by positron emission tomography. J Neurophysiol 85:951-959, 2001 12. Cechetto DF, Saper CB: Evidence for a viscertopic sensory representation in the cortex and thalamus in the rat. J Comp Neurol 262:27-45, 1987 13. Chen ACN, Bromm B: Pain related generators of laserevoked potentials: Brain mapping and dipole modeling, in Bromm B, Desmedt JE (eds): Pain and the Brain: From Nociception to Cognition, Advances in Pain Research and Therapy, 22. New York, NY, Raven Press, 1995, pp 245-266 14. Coghill RC, Sang CN, Maisog JM, Iadarola MJ: Pain intensity processing within the human brain: A bilateral, distributed mechanism. J Neurophysiol 82:1934-1943, 1999 15. Craig AD, Bushnell MC, Zhang ET, Blomqvist A: A thalamic nucleus specific for pain and temperature sensation. Nature 372:770-773, 1994 16. Craig AD, Chen K, Bandy D, Reiman EM: Thermosensory activation of insular cortex. Nature Neurosci 3:184-190, 2000 17. Croft PR, Rigby AS: Socioeconomic influences on back problems in the community in Britain. J Epidemiol Community Health 48:166-170, 1994 18. Davis KD, Kwan CL, Crawley AP, Mikulis DJ: Functional MRI study of thalamic and cortical activations evoked by cutaneous heat, cold and tactile stimuli. J Neurophysiol 80: 1533-1546, 1998 19. Derbyshire SWG: Exploring the pain “neuromatrix”. Curr Rev Pain 6:467-477, 2000 20. Derbyshire SWG: Meta-analysis of thirty-four independent samples studied using positron emission tomography (PET) reveals a significantly attenuated central response to noxious stimulation in clinical pain patients. Curr Rev Pain 3:265-280, 1999 ORIGINAL REPORT/Derbyshire et al 409 21. Derbyshire SWG: Sources of variation in assessing male and female responses to pain. New Ideas Psychol 15:83-95, 1997 22. Derbyshire SWG, Jones AKP, Gyulai F, Clark S, Townsend D, Firestone L: Pain processing during three levels of noxious stimulation produces differential patterns of central activity. Pain 73:431-445, 1997 23. Derbyshire SWG, Gyulai F, Jones AKP, Clark S, Townsend D, Firestone L: Attenuation of laser pain by fentanyl correlates with focal changes in cerebral response. J Cereb Blood Flow Metab 17(S1):654, 1997 24. Derbyshire SWG, Jones AKP, Townsend D, Gyulai F, Firestone L: Gender differences in the central response to pain controlled for stimulus intensity. Soc Neurosci 24:212.11, 1998 25. Ellermeir W, Westphal W: Gender differences in pain ratings and pupil reactions to painful pressure stimuli. Pain 61:435-439, 1995 26. Esposito G, Van Horn JD, Weinberger DR, Berman KF: Gender differences in cerebral blood flow as a function of cognitive state with PET. J Nucl Med 37:559-564, 1996 27. Fillingim RB, Maddux V, Shackelford JA: Sex differences in heat pain thresholds as a function of assessment method and rate of rise. Somatosens Mot Res 16:57-62, 1999 28. Fillingim RB, Ness TJ: Sex-related hormonal influences on pain and analgesic responses. Neurosci Biobehav Rev 24: 485-501, 2000 29. Fox PT, Mintun MA: Noninvasive functional brain mapping by change-distribution analysis of averaged PET images of H215O tissue activity. J Nucl Med 30:141-149, 1989 30. Friedman DP, Murray EA: Thalamic connectivity of the second somatosensory area and neighboring somatosensory fields of the lateral sulcus of the macaque. J Comp Neurol 252:348-374, 1986 31. Friston KJ, Frackowiak RSJ: Imaging functional anatomy. Alfred Benzon Symposium 31, Munksgaard, Copenhagen, 1991 32. Friston KJ, Frith CD, Liddle PF, Dolan RJ, Lammertsma AA, Frackowiak RSJ: The relationship between local and global changes in PET scans. J Cereb Blood Flow Metab 10:458-466, 1990 33. Friston KJ, Holmes AP, Worsley KJ, Poline JP, Frith CD, Frackowiak RSJ: Statistical parametric maps in functional imaging: A general approach. Hum Brain Mapp 2:189-210, 1995 34. Friston KJ, Holmes A, Poline J-B, Price CJ, Frith CD: Detecting activations in PET and fMRI: Levels of inference and power. Neuroimage 4:223-235, 1995 35. Gur RC, Mozley LH, Mozley PD, Resnick SM, Karp JS, Alavi A, Arnold SE, Gur RE: Sex differences in regional cerebral glucose metabolism during a resting state. Science 267:528- 531, 1995 36. Hutchison WD, Luhn MA, Schmidt RF: Responses of lateral thalamic neurons to algesic chemical stimulation of the cat knee joint. Exp Brain Research 101:452-464, 1994 37. Keppler KL, Standifer KM, Paul D, Kest B, Pasternak GW, Bodnar RJ: Gender effects and central opioid analgesia. Pain 45:87-94, 1991 38. Kulynych J, Vladar K, Jones D, Weinberger D: Gender differences in the normal lateralization of the supratemporal cortex: MRI surface-rendering morphology of Heschl’s gyrus and planum temporale. Cereb Cortex 4:107-118, 1994 39. Laird NM, Ware JH: Random-effects models for longitudinal data. Biometrics 38:963-974, 1982 40. Lautenbacher S, Rollman GB: Sex differences in responsiveness to painful and non-painful stimuli are dependent upon the stimulation method. Pain 53:255-264, 1993 41. Lautenbacher S, Strian F: Sex differences in pain and thermal sensitivity: The role of body size. Percept Psychophys 50:179-183, 1991 42. Leventhal H: A perceptual-motor theory of emotion. Adv Exp Soc Psychol 17:117-175, 1984 43. Lipman JJ, Blumenkopf B, Lawrence P: Normal and radiculopathic cutaneous pain tolerance levels evaluated by heat beam dolorimetry. J Neurosurg 72:883-888, 1990 44. Meana M: The meeting of pain and depression: Comorbidity in women. Can J Psychiatry 43:893-899, 1998 45. Merskey H: Psychiatry and pain, in Sternberg RA (ed): The Psychology of Pain (ed 2). New York, NY, Raven Press, 1986, pp 97-120 46. Mogil JS, Sternberg WF, Kest B, Marek P, Liebeskind JC: Sex differences in the antagonism of swim stress-induced analgesia: Effects of gonadectomy and estrogen replacement. Pain 53:17-25, 1993 47. Neafsey EJ, Terreberry RR, Hurley KM, Ruit KG, Frysztak RJ: Anterior cingulate cortex in rodents: Connections, visceral control functions, and implications for emotion, in Vogt BA, GabrielM(eds): Neurobiology of Cingulate Cortex and Limbic Thalamus: A Comprehensive Treatise. Boston, MA, Birkhauser, 1993, pp 206-223 48. Otto MW, Dougher MJ: Sex differences and personality factors in responsivity to pain. Percept Mot Skills 61:383-390, 1985 49. Paulson PM, Minoshima S, Morrow TJ, Casey KL: Gender differences in pain perception and patterns of cerebral activation during noxious heat stimulation in humans. Pain 76: 223-229, 1998 50. Pennebaker J: The psychology of physical symptoms. New York, NY, Springer-Verlag Inc, 1982 51. Rainville P, Duncan GH, Price DD: Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science 277:968-971, 1997 52. Riley JL, Robinson ME, Wise EA, Myers CD, Fillingim RB: Sex differences in the perception of noxious experimental stimuli: A meta-analysis. Pain 74:181-187, 1998 53. Rollman GB: Gender differences in pain: Role of anxiety. Pain Forum 4:231-234, 1995 54. Ruda MA: Gender and pain. Pain 53:1-2, 1993 55. Shaywitz BA, Shaywitz SE, Pugh KR, Constable RT, Skudlarski P, Fulbright RK, Bronen RA, Fletcher JM, Shankweiler DP, Katz L, Gore JC: Sex differences in the functional organization of the brain for language. Nature 373:607-609, 1995 56. Sheffield D, Biles PL, Orom H, Maixner W, Sheps DS: Race and sex differences in cutaneous pain perception. Psychosom Med 62:517-523, 2000 57. Smyth JS: Some problems of dental treatment. Part 1. Patient anxiety: Some correlates and sex differences. Aust Dent J 38:354-359, 1993 410 Central Responses to Pain Across Gender 58. Sternberg WF, Liebeskind JC: The analgesic response to stress: Genetic and gender considerations. Eur J Anaesthesiol 12(S10):14-17, 1995 59. Swaab DF, Fliers E: A sexually dimorphic nucleus in the human brain. Science 228:1112-1115, 1985 60. Unruh AM: Gender variations in clinical pain experience. Pain 65:123-167, 1996 61. Van Hoesen GW, Morecraft RJ, Vogt BA: Connections of the monkey cingulate cortex, in Vogt BA, Gabriel M (eds): Neurobiology of Cingulate Cortex and Limbic Thalamus: A Comprehensive Treatise. Boston, MA, Birkhauser, 1993, pp 249-284 62. Vierck CJ, Cannon RL, Fry G, Maixner W, Whitsel BL: Characteristics of temporal summation of second pain sensations elicited by brief contact of glabrous skin by a preheated thermode. J Neurophysiol 78:992-1002, 1997 63. Vogt BA, Derbyshire SWG, Jones AKP: Pain processing in four regions of human cingulate cortex localized with coregistered PET and MR imaging. Eur J Neurosci 8:1461- 1473, 1996 64. Wade JB, Price DD, Hamer RH, Scwartz SM, Hart RP: An emotional component analysis of chronic pain. Pain 40:303- 310, 1990 65. Witelson SF, Glezer II, Kigar DL: Women have greater density of neurons in posterior temporal cortex. J Neurosci 15:3418-3428, 1995 66. Woods RP, Cherry SR, Mazziotta JC: A rapid automated algorithm for accurately aligning and reslicing positron emission tomography images. J Comput Assist Tomogr 16: 620-633, 1992 67. Worsley KJ: An overview and some new developments in the statistical analysis of PET and fMRI data. Hum Brain Mapp 5:254-258, 1997 68. Worsley K, Evans AC, Marret S, Neelin P: A three dimensional statistical analysis for CBF activation in the human brain. J Cereb Blood Flow Metab 12:900-918, 1992 69. Worsley K, Marret S, Neelin P, Vandal A, Friston K, Evans AC: A unified statistical approach for determining significant signals in images of cerebral activation. Hum Brain Mapp 4:58-73, 1996|
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