μ-opioid Receptor-Mediated Antinociceptive Responses Differ in Men and Women

Journal of Neuroscience

Volumn 22, Issue 12, 2002, Pages 5100-5107

  Zubieta, Jon Kar ^a,b   Smith, Yolanda R ^b   Bueller, Joshua A ^a   Xu, Yanjun ^a   Kilbourn, Michael R ^b   Jewett, Douglas M ^b   Meyer, Charles R ^b   Koeppe, Robert A ^b   Stohler, Christian S ^c  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Amygdala; Endogenous opioids; Nucleus accumbens; Pain; Positron emission tomography; Sex differences; Substantia innominata; Thalamus; Ventral pallidum; opioid receptors

Indexed keywords

MU OPIATE RECEPTOR; TRACER;

ADULT; AMYGDALOID NUCLEUS; ANTINOCICEPTION; ARTICLE; BASAL GANGLION; BRAIN NUCLEUS; BRAIN REGION; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; FEMALE; FOLLICULAR PHASE; HUMAN; HYPERALGESIA; INTERMETHOD COMPARISON; MALE; NORMAL HUMAN; NUCLEUS ACCUMBENS; PAIN ASSESSMENT; PAIN THRESHOLD; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; RECEPTOR INTRINSIC ACTIVITY; SEX DIFFERENCE; THALAMUS ANTERIOR NUCLEUS; BRAIN; COMPARATIVE STUDY; COMPUTER ASSISTED EMISSION TOMOGRAPHY; PAIN; PHYSIOLOGY; SCINTISCANNING; THALAMUS;

ADULT; AMYGDALA; BRAIN; DOUBLE-BLIND METHOD; FEMALE; HUMANS; MALE; NUCLEUS ACCUMBENS; PAIN; RECEPTORS, OPIOID, MU; SEX FACTORS; THALAMUS; TOMOGRAPHY, EMISSION-COMPUTED;

EID: 0037096431     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-12-05100.2002     Document Type: Article

References (76)

1. Akil H, Watson S, Young E, Lewis M, Khachaturian H, Walker J (1984) Endogenous opioids: biology and function. Annu Rev Neurosci 7:223-255.
2. Aloisi AM, Albonetti ME, Carli G (1994a) Sex differences in the behavioural response to persistent pain in rats. Neurosci Lett 179:79-82.
3. Aloisi AM, Steenbergen HL, van de Poll NE, Farabollini F (1994b) Sex-dependent effects of restraint on nociception and pituitary-adrenal hormones in the rat. Physiol Behav 55:789-793.
4. Austin M, Kalivas P (1991) Dopaminergic involvement in locomotion elicited from the ventral pallidum/substantia innominata. Brain Res 542:123-131.
5. Baamonde A, Hidalgo A, Andres-Trelles F (1989) Sex-related differences in the effects of morphine and stress on visceral pain. Neuropharmacology 28:967-970.
6. Basbaum A, Fields H (1984) Endogenous pain control system: brain spinal pathways and endorphin circuitry. Annu Rev Neurosci 7:309-338.
7. Bourgeais L, Gauriau C, Bernard J (2001) Projections from the nociceptive area of the central nucleus of the amygdala to the forebrain: a PHA-L study in the rat. Eur J Neurosci 14:229-255.
8. Bushnell MC, Duncan GH (1989) Sensory and affective aspects of pain perception: is medial thalamus restricted to emotional issues? Exp Brain Res 78:415-418.
9. Carr K, Bak T (1988) Medial thalamic injection of opioid agonists: μ-agonist increases while κ-agonist decreases stimulus thresholds for pain and reward. Brain Res 441:173-184.
10. Casey K (1999) Forebrain mechanisms of nociception and pain: analysis through imaging. Proc Natl Acad Sci USA 96:7668-7674.
11. Caterina M, Leffler A, Malmberg A, Martin W, Trafton J, Petersen-Zeitz K, Koltzenburg M, Basbaum A, Julius D (2000) Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288:306-313.
12. Chrobak J, Napier T (1993) Opioid and GABA modulation of accumbens-evoked ventral pallidal activity. J Neural Transm Gen Sect 93:123-143.
13. Cicero TJ, Nock B, Meyer ER (1996) Gender-related differences in the antinociceptive properties of morphine. J Pharmacol Exp Ther 279:767-773.
14. Cicero TJ, Ennis T, Ogden J, Meyer ER (1999) Gender differences in the reinforcing properties of morphine. Pharmacol Biochem Behav 65:91-96.
15. Coghill R, Sang C, Maisog J, Iadarola M (1999) Pain intensity processing within the human brain: a bilateral, distributed mechanism. J Neurophysiol 82:1934-1943.
16. 11C]carfentanil. Int J Appl Radiat Isot 36:303-306.
17. Dawson-Basoa M, Gintzler A (1993) 17-β-estradiol and progesterone modulate an intrinsic opioid analgesic system. Brain Res 601:241-245.
18. D'Souza DN, Harlan RE, Garcia MM (1999) Sexual dimorphism in the response to N-methyl-D-aspartate receptor antagonists and morphine on behavior and c-Fos induction in the rat brain. Neuroscience 93:1539-1547.
19. Eckersell C, Popper P, Micevych P (1998) Estrogen-induced alteration of μ-opioid receptor immunoreactivity in the medial preoptic nucleus and medial amygdala. J Neurosci 18:3967-3976.
20. Fillingim R, Maixner W (1995) Gender differences in the responses to noxious stimuli. Pain Forum 4:209-221.
21. Fillingim R, Ness J (2000) Sex-related hormonal influences on pain and analgesic responses. Neurosci Biobehav Rev 24:485-501.
22. Friston KJ, Frith CD, Liddle PF, Frackowiak RSJ (1991) Comparing functional (PET) images: the assessment of significant change. J Cereb Blood Flow Metab 11:690-699.
23. Friston KJ, Worsley KJ, Frackowiak RSJ, Mazziotta JC, Evans AC (1994) Assessing the significance of focal activations using their spatial extent. Hum Brain Mapp 1:210-220.
24. Friston KJ, Holmes AP, Worsley KJ, Poline J-P, Frith CD, Frackowiak RSJ (1995) Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 2:189-210.
25. Gabilondo A, Meana J, Garcia-Sevilla J (1995) Increased density of μ-opioid receptors in the postmortem brain of suicide victims. Brain Res 682:245-250.
26. Gear R, Levine J (1995) Antinociception produced by an ascending spino-supraspinal pathway. J Neurosci 15:3154-3161.
27. Gear R, Miaskowski C, Gordon N, Paul S, Heller P, Levine J (1996) κ-opioids produce significantly greater analgesia in women than in men. Nat Med 2:1248-1250.
28. Gear R, Aley K, Levine J (1999) Pain-induced analgesia mediated by mesolimbic reward circuits. J Neurosci 19:7175-7181.
29. Gross-Isseroff R, Dillon K, Israeli M, Biegon A (1990) Regionally selective increases in μ opioid receptor density in the brains of suicide victims. Brain Res 530:312-316.
30. Hammer RP (1990) μ-opiate receptor binding in the medial preoptic area is cyclical and sexually dimorphic. Brain Res 515:187-192.
31. Harte S, Lagman A, Borszcz G (2000) Antinociceptive effects of morphine injected into the nucleus parafascicularis thalami of the rat. Brain Res 874:78-86.
32. Hernandez L, Valentine J, Powell D (1991) Opioid modulation of pavlovian learning in rabbits: involvement of sublenticular pathways. Behav Neurosci 105:431-442.
33. 11C]carfentanil. Nucl Med Biol 28:733-734.
34. Johnson P, Napier T (1997) Morphine modulation of GABA- and glutamate-induced changes of ventral pallidal neuronal activity. Neuroscience 77:187-197.
35. 11C] diprenorphine and positron emission tomography. J Cereb Blood Flow Metab 19:803-808.
36. Kavaliers M, Colwell D (1991) Sex differences in opioid and non-opioid mediated predator-induced analgesia in mice. Brain Res 568:173-177.
37. Kest B, Sarton E, Dahan A (2000) Gender differences in opioid-mediated analgesia: animal and human studies. Anesthesiology 93:539-547.
38. Laruelle M (2000) Imaging synaptic neurotransmission with in vivo binding competition techniques: a critical review. J Cereb Blood Flow Metab 20:423-451.
39. Logan J, Fowler JS, Volkow ND, Wang GJ, Ding YS, Alexoff DL (1996) Distribution volume ratios without blood sampling from graphical analysis of PET data. J Cereb Blood Flow Metab 16:834-840.
40. Malmberg A, Chen C, Tonegawa S, Basbaum A (1997) Preserved acute pain and reduced neuropathic pain in mice lacking PKCγ. Science 278:279-283.
41. Manning B (1998) A lateralized deficit in morphine antinociception after unilateral inactivation of the central amygdala. J Neurosci 18:9453-9470.
42. Matthes HWD, Maldonado R, Simonin F, Valverde O, Slowe S, Kitchen I, Befort K, Dierich A, LeMeur M, Dolle P, Tzavara E, Hannoune J, Roques BP, Kieffer BL (1996) Loss of morphine-induced analgesia, reward effect, and withdrawal symptoms in mice lacking the μ-opioid-receptor gene. Nature 383:819-823.
43. Melzack R, Katz J (2000) The McGill pain questionnaire: appraisal and current status. In: Handbook of pain assessment (Turk D, Melzack R, eds), pp 152-168. New York: Guilford.
44. Meyer CR, Boes JL, Kim B, Bland PH, Zasadny KR, Kison PV, Koral K, Frey KA, Wahl RL (1997) Demonstration of accuracy and clinical versatility of mutual information for automatic multimodality image fusion using affine and thin-plate spline warped geometric deformations. Med Image Anal 1:195-206.
45. Miaskowski C, Levine J (1999) Does opioid analgesia show a gender preference for females. Pain Forum 8:34-44.
46. Minoshima S, Koeppe RA, Mintun MA, Berger KL, Taylor SF, Frey KA, Kuhl DE (1993) Automated detection of the intercommissural line for stereotactic localization of functional brain images. J Nucl Med 34:322-329.
47. Mogenson G, Yang C (1991) The contribution of the basal forebrain to limbic-motor integration and the mediation of motivation to action. In: The basal forebrain: anatomy to function (Napier T, Kalivas P, Hanin I, eds), pp 267-290. New York: Plenum.
48. Mogil J, Belknap J (1997) Sex and genotype determine the selective activation of neurochemically-distinct mechanisms of swim stress-induced analgesia. Pharmacol Biochem Behav 56:61-66.
49. Mogil JS, Chesler EJ, Wilson SG, Juraska JM, Sternberg WF (2000) Sex differences in thermal nociception and morphine antinociception in rodents depend on genotype. Neurosci Biobehav Rev 24:375-389.
50. Morris J, Friston K, Büchel C, Frith C, Young A, Calder A, Dolan R (1998) A neuromodulatory role for the human amygdala in processing emotional facial expressions. Brain 121:47-57.
51. Napier T, Mitrovic I (1999) Opioid modulation of ventral pallidal inputs. Ann NY Acad Sci 877:176-201.
52. Negus S, Mello N (1999) Opioid antinociception in ovariectomized monkeys: comparison with antinociception in males and effects of estradiol replacement. J Pharmacol Exp Ther 290:1132-1140.
53. Paulson P, Minoshima S, Morrow T, Casey K (1998) Gender differences in pain perception and patterns of cerebral activation during noxious heat stimulation in humans. Pain 76:223-229.
54. Price D (2000) Psychological and neural mechanisms of the affective dimension of pain. Science 288:1769-1772.
55. Romero M, Bodnar R (1986) Gender differences in two forms of cold-water swim analgesia. Physiol Behav 37:893-897.
56. Rubinstein M, Mogil JS, Japon M, Chan EC, Allen RG, Low MJ (1996) Absence of opioid stress-induced analgesia in mice lacking β-endorphin by site-directed mutagenesis. Proc Natl Acad Sci USA 93:3995-4000.
57. Russchen F, Amaral D, Price J (1985) The afferent connections of the substantia innominata in the monkey, Macaca fascicularis. J Comp Neurol 242:1-27.
58. Sinchak K, Micevych P (2001) Progesterone blockade of estrogen activation of μ-opioid receptors regulates reproductive behavior. J Neurosci 21:5723-5729.
59. Smith Y, Zubieta J, Del Carmen M, Dannals R, Ravert H, Zacur H, Frost J (1998) Brain μ opioid receptor measurements by positron emission tomography in normal cycling women: relationship to LH pulsatility and gonadal steroid hormones. J Clin Endocrinol Metab 83:4498-4505.
60. Sora I, Takahashi N, Funada M, Ujike H, Revay RS, Donovan DM, Miner LL, Uhl GR (1997) Opiate receptor knockout mice define μ receptor roles in endogenous nociceptive responses and morphine-induced analgesia. Proc Natl Acad Sci USA 94:1544-1549.
61. Spooren W, Veening J, Groenewegen H, Cools A (1991) Efferent connections of the striatopallidal and amygdaloid components of the substantia innominata in the cat: projections to the nucleus accumbens and caudate nucleus. Neuroscience 44:431-447.
62. Stock H, Caldarone B, Abrahamsen G, Mongeluzi D, Wilson M, Rosellini R (2001) Sex differences in relation to conditioned fear-induced enhancement of morphine analgesia. Physiol Behav 72:439-447.
63. Stohler C, Kowalski C (1999) Spatial and temporal summation of sensory and affective dimensions of deep somatic pain. Pain 79:165-173.
64. Taylor S, Liberzon I, Koeppe R (2000) The effect of graded aversive stimuli on limbic and visual activation. Neuropsychologia 38:1415-1425.
65. Terman G, Shavit Y, Lewis J, Cannon J, Liebeskind J (1984) Intrinsic mechanisms of pain inhibition: activation by stress. Science 226:1270-1277.
66. Tershner S, Mitchell J, Fields H (2000) Brainstem pain modulating circuitry is sexually dimorphic with respect to μ and κ opioid receptor function. Pain 85:153-159.
67. Treede R-D, Kenshalo DR, Gracely RH, Jones AKP (1999) The cortical representation of pain. Pain 79:105-111.
68. Unruh A (1996) Gender variations in clinical pain experience. Pain 65:123-167.
69. Watkins L, Mayer D (1982) Organization of endogenous opiate and nonopiate pain control systems. Science 216:1185-1192.
70. Watson D, Clark LA, Tellegen A (1988) Development and validation of brief measures of positive and negative affect: the PANAS scales. J Pers Soc Psychol 54:1063-1070.
71. Worsley K, Evans A, Marrett S, Neelin P (1992) A three-dimensional statistical analysis for CBF activation studies in human brain. J Cereb Blood Flow Metab 12:900-918.
72. 2, F, and t fields. Adv Appl Prob 26:13-42.
73. Zacny J (2001) Morphine responses in humans: a retrospective analysis of sex differences. Drug Alcohol Depend 63:23-28.
74. Zhang X, Ashton-Miller JA, Stohler CS (1993) A closed-loop system for maintaining constant experimental muscle pain in man. IEEE Trans Biomed Eng 40:344-352.
75. Zubieta J, Dannals R, Frost J (1999) Gender and age influences on human brain μ opioid receptor binding measured by PET. Am J Psychiatry 156:842-848.
76. Zubieta J, Smith Y, Bueller J, Xu Y, Kilbourn M, Meyer C, Koeppe R, Stohler C (2001) Regional μ opioid receptor regulation of sensory and affective dimensions of pain. Science 293:311-315.