Sex differences in pain-induced effects on the septo-hippocampal system

Brain Research Reviews

Volumn 25, Issue 3, 1997, Pages 397-406

  Aloisi, Anna Maria ^a  

^a UNIVERSITY OF SIENA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; ACETYLCHOLINE; ACETYLCHOLINESTERASE; AMINE; CHOLINE ACETYLTRANSFERASE; CORTICOSTERONE; GLUCOCORTICOID; NEUROSTEROID; NORADRENALIN; OPIATE; SEROTONIN; SEX HORMONE;

ADAPTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; AVERSION; CHOLINERGIC SYSTEM; CONTROLLED STUDY; FEMALE; HIPPOCAMPUS; LIMBIC SYSTEM; MALE; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; RAT; REVIEW; SEPTUM PELLUCIDUM; SEX DIFFERENCE;

ANIMALS; BRAIN; FEMALE; HIPPOCAMPUS; HUMANS; MALE; PAIN; SEX CHARACTERISTICS;

EID: 0031418572     PISSN: 01650173     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0165-0173(97)00030-1     Document Type: Review

References (115)

1. Abercrombie E.D., Keller R.W., Zigmond M.J. Characterization of hippocampal norepinephrine release as measured by microdialysis perfusion: pharmacological and behavioral studies. Neuroscience. 3:1988;897-904.
2. A. Ahamadiani, A. Haery, Orchiectomy and androgen blockade in male rat causes analgesia via serotonergic and opioid system but not adrenergic system, 8th World Congress on Pain, Vancouver 1996, Abstr. 103, p. 360.
3. Aloisi A.M., Zimmermann M., Herdegen T. Sex-dependent effects of formalin and restraint on c-Fos expression in the septum and hippocampus of the rat. Neuroscience. 81:1997;951-958.
4. Aloisi A.M., Albonetti M.E., Carli G. Formalin-induced changes in adrenocorticotropin hormone and corticosterone plasma levels and hippocampal choline acetyltransferase activity in male and female rats. Neuroscience. 74:1996;1019-1024.
5. Aloisi A.M., Albonetti M.E., Carli G. Sex differences in the behavioral response to persistent pain in rats. Neurosci. Lett. 179:1994;79-82.
6. A.M. Aloisi, M.E. Albonetti, P. Sacerdote, G. Carli, Sex dependent effects of stress and pain on choline acetyltransferase activity levels and β-endorphin content in discrete areas of the rat brain, in: A.R. Gennazzani, F. Petraglia, R.H. Purdy (Eds.), The Brain: Source and Target for Sex Steroid Hormones, The Parthenon P.G., New York, 1996, pp. 229-242.
7. Aloisi A.M., Casamenti F., Scali C., Pepeu G., Carli G. Effects of novelty, pain and stress on hippocampal extracellular acetylcholine levels in male rats. Brain Res. 748:1997;219-226.
8. Aloisi A.M., Sacerdote P., Albonetti M.E., Carli G. Sex-related effects on behavior and b-endorphin of different intensities of formalin pain in rats. Brain Res. 699:1995;242-249.
9. Aloisi A.M., Steenbergen H.L., Van de Poll N.E., Farabollini F. Sex-dependent effects of restraint on nociception and pituitary-adrenal hormones in the rat. Physiol. Behav. 55:1994;789-793.
10. Andrews N., Hogg S., Gonzalez L.E., File S.E. 5-HT1A receptors in the median raphe nucleus and dorsal hippocampus may mediate anxiolytic and anxiogenic behaviors respectively. Eur. J. Pharmacol. 264:1994;259-264.
11. Archer J. Rodent sex differences in emotional and related behavior. Behav. Biol. 14:1975;451-479.
12. Armanini M.P., Hutchins C., Stein B.A., Sapolsky R.M. Glucocorticoid endargement of hippocampal neurons is NMDA-receptor dependent. Brain Res. 532:1990;7-12.
13. Barbaccia M.L., Roscetti G., Trabucchi M., Mostallino M.C., Concas A., Purdy R.H., Biggio G. Time-dependent changes in rat brain neuroactive steroid concentrations and GABAa receptor function after acute stress. Neuroendocrinology. 63:1996;166-172.
14. R.E. Bartok, M. Craft, Sex differences in opioid antinociception, 8th World Congress on Pain, Vancouver 1996, Abstr. 85, p. 463.
15. Bartolini A., Ghelardini C., Fantetti L., Malcangio M., Malmberg-Aiello P., Giotti A. Role of muscarinic receptor subtypes in central antinociception. Br. J. Pharmacol. 105:1992;77-82.
16. Beatty W.W., Beatty P.A. Hormonal determinations of sex differences in avoidance behaviour and reactivity to electric shock in the rat. J. Comp. Physiol. Psychol. 73:1970;446-455.
17. Berger-Sweeney J., Arnold A., Gabeau D., Mills J. Sex differences in learning and memory in mice: effects of sequence of testing and cholinergic blockade. Behav. Neurosci. 109:1995;859-873.
18. K.J. Berkley, Sex differences in pain, Behav. Brain Sci. (1997) in press.
19. Bettini E., Pollio G., Santagati S., Maggi A. Estrogen receptor in rat brain: presence in the hippocampal formation. Neuroendocrinology. 56:1992;502-508.
20. Blanchard D.C., Griebel G., Blanchard R.J. Gender bias in the preclinical psychopharmacology of anxiety: male models for (predominantly) female disorders. J. Psychopharmacol. 9:1995;79-82.
21. Bodnar R.J., Romero M.-T., Kramer E. Organismic variables and pain inhibition roles of gender and aging. Brain Res. Bull. 21:1988;947-953.
22. K. Bon, M. Lantéri-Minet, D. Menetrey, K. Berkley, Sex, time of the day, and estrous variations in the behavioral consequences of cyclophosphamide-induced cystitis in rats, 8th World Congress on Pain, Vancouver 1996, Abstr. 100, p. 248.
23. Bosse R., Dipaolo T. The modulation of brain dopamine and GABA (A) receptors by estradiol: a clue for CNS changes occurring at menopause. Cell. Mol. Neurobiol. 16:1996;199-212.
24. H.B. Bradshaw, K.J. Berkley, Effects of estrous stage and endometriosis on escape responses to vaginal distension and vaginal tone in the awake rat, 8th World Congress on Pain, Vancouver 1996, Abstr. 97, p. 247.
25. Burgess L.H., Handa R.J. Estrogen-induced alterations in the regulation of mineralcorticoid and glucocorticoid receptor messenger RNA expression in the female rat anterior pituitary gland and brain. Mol. Cell. Neurosci. 4:1993;191-198.
26. F. Capone, F. Pavone, G. Carli, A.M. Aloisi, The muscarinic agonist oxotremorine significantly decreases the behavioral responses associated to pain induced by formalin, 8th World Congress on Pain, Vancouver 1996, Abstr. 114, p. 472.
27. J.J. Carmody, K.A. Cooper, Gender, nociception and stress analgesia in mice: paradoxical susceptibility of males to hormone treatment, 8th World Congress on Pain, Vancouver 1996, Abstr. 230, p. 506.
28. R. Chapman, Limbic processes and the affective dimension of pain, in: G. Carli, M. Zimmermann (Eds.), Progress in Brain Research, Vol. 110, Elsevier Science B.V., Amsterdam, 1996, pp. 63-84.
29. Compton D.M., Dietrich K.L., Smith J.S., Davis B.K. Spatial and non-spatial learning in the rat following lesions to the nucleus locus coeruleus. NeuroReport. 7:1995;177-182.
30. Coyle D.E., Sehlhorst S., Behbehani M.M. Intact female rats are more susceptible to the development of tactile allodynia than ovariectomized female rats following partial sciatic nerve ligation (PSNL). Neurosci. Lett. 203:1996;37-40.
31. Critchow V., Liebelt R.A., Bar-Sela M., Montcastle W., Lipscomb H.S. Sex differences in resting pituitary adrenal function in the rat. Am. J. Physiol. 205:1963;807-815.
32. Dallman M., Akana S., Scribner K.A., Bradbury M.J., Walker C.D., Strack A.M., Cascio C.S. Stress, feedback and facilitation in the hypothalamo-pituitary-adrenal axis. J. Neuroendocrinol. 4:1992;517-527.
33. Dawkins K. Gender differences in psychiatry. CNS Drugs. 3:1995;393-407.
34. De Kloet E.R., Oitzl M.S., Joëls M. Functional implications of brain corticosteroid receptor diversity. Cell. Mol. Neurobiol. 13:1993;433-455.
35. Dubrovsky B., Gijsbers K., Filipini D., Birmingham M.K. Effects of adrenocortical steroids on long-term potentiation in the limbic system: basic mechanisms and behavioral consequences. Cell. Mol. Neurobiol. 13:1993;399-414.
36. Dunbar G.L., Rylett R.J., Schmidt B.M., Sinclair R.C., Williams L.R. Hippocampal choline acetyltransferase activity correlates with spatial learning in aged rats. Brain Res. 604:1993;266-272.
37. Dutar P., Bassant M.-H., Senut M.-C., Lamour Y. The septohippocampal pathway: structure and function of a central cholinergic system. Physiol. Rev. 75:1995;393-427.
38. Dutar P., Lamour Y., Jobert A. Activation of identified septo-hippocampal neurons by noxious peripheral stimulation. Brain Res. 328:1985;15-21.
39. Endo Y., Nishimura J.-I., Kimura F. Adrenalectomy increases local cerebral blood flow in the rat hippocampus. Eur. J. Physiol. 426:1994;183-188.
40. Feldman S., Conforti N., Weidenfeld J. Limbic pathways and hypothalamic neurotransmitters mediating adrenocortical responses to neural stimuli. Neurosci. Biobehav. Rev. 19:1995;235-240.
41. Fernandez-Guasti A., Picazo O. The actions of diazepam and serotonergic anxiolytics vary according to the gender and the estrous cycle phase. Pharmacol. Biochem. Behav. 37:1990;77-81.
42. R.B. Fillingim, W. Maixner, S. Kincaid, A. Sigurdsonn, Gender differences in temporal summation of thermal pain, 8th World Congress on Pain, Vancouver 1996, Abstr. 235, p. 507.
43. Foote S.L., Bloom F.E., Aston-Jones G. Nucleus locus ceruleus: new evidence of anatomical and physiological specificity. Physiol. Rev. 63:1983;844-914.
44. M.E. Freeman, The ovarian cycle of the rat, in: E. Knobil, J. Neil (Eds.), The Physiology of Reproduction, Raven Press, New York, 1988, pp. 1893-1928.
45. Gala R.R., Westphal U. Corticosteroid-binding globulin in the rat: studies on the sex differences. Endocrinology. 77:1965;841-851.
46. A.R. Gennazzani, F. Petraglia, R.H. Purdy, (Eds.), The Brain: Source and Target for Sex Steroid Hormones, Parthenon Publishing, New York, 1996, 314 pp.
47. A.R. Gennazzani, C. Salvestroni, A.-L. Guo, M. Palumbo, V. Cela, E. Casarosa, M. Luisi, A.D. Gennazzani, F. Petraglia, Neurosteroids and regulation of neuroendocrine function, in: A.R. Gennazzani, F. Petraglia and R.H. Purdy (Eds.), The Brain: Source and Target for Sex Steroid Hormones, Parthenon Publishing, New York, 1996, pp. 83-91.
48. C. Ghelardini, N. Galeotti, A. Bartolini, Caffeine induces central cholinergic antinociception, The 2nd Meeting of European Neuroscience, Strasbourg 1996, Abstr. 53.11, p. 97.
49. M.A. Giamberardino, R. Valente, G. Affaitati, L. Vecchiet, Changes in visceral pain sensitivity as a function of time of day and estrus cycle in female rats with artificial ureteral calculosis, 8th World Congress on Pain, Vancouver 1996, Abstr. 89, p. 247.
50. Glavin G.B. Stress and brain noradrenaline: a review. Neurosci. Biobehav. Rev. 9:1985;233-243.
51. J.A. Gray (Ed.), The Neuropsychology of Anxiety, Clarendon Press, Oxford, 1982, 548 pp.
52. Guilbaud G., Kayser V., Keita H., Gautron M., Berkley K.J. Estrous and sex variations in vocalization thresholds to hindpaw and tail pressure stimulation in the rat. Brain Res. 742:1996;352-354.
53. Guo A.-L., Petraglia F., Criscuolo M., Ficarra G., Nappi R.E., Palumbo M.A., Trentini G.P., Purdy R.H., Gennazzani A.R. Evidence for a role of neurosteroids in modulation of diurnal changes and acute stress-induced corticosterone secretion in rats. Gynecol. Endocrinol. 9:1995;1-4.
54. Heinsbroek R.P.W., Van Haaren F., Van de Poll N.E. Sex differences in passive avoidance behavior of rats: sex-dependent susceptibility to shock-induced behavioral depression. Physiol. Behav. 43:1988;201-206.
55. Heinsbroek R.P.W., Van Haaren F., Feenstra M.G.P., Van Galen H.H., Boer G., Van de Poll N.E. Sex differences in the effects of inescapable footshock on central catecholaminergic and seronergic activity. Pharmacol. Biochem. Behav. 37:1990;539-550.
56. Hönack D., Löscher W. Sex differences in NMDA receptor mediated responses in rats. Brain Res. 620:1993;167-170.
57. Hörtnagl H., Berger M.L., Hornykiewicz O. Glucocorticoids aggravate the cholinergic deficit induced by ethylcholine aziridinium (AF64A) in rat hippocampus. Soc. Neurosci. 17:1991;715.
58. Hörtnagl H., Hansen L., Kindel G., Shneider B., El Tamer A., Hanin I. Sex differences and estrous-cycle variations in the AF64A-induced cholinergic deficit in the rat hippocampus. Brain Res. Bull. 31:1993;129-134.
59. Jirikowski G.F., Merchenthaler I., Rieger G.E., Stumpf W.E. Estradiol target sites immunoreactive for beta-endorphin in the arcuate nucleus of the rat and mouse hypothalamus. Neurosci. Lett. 65:1986;121-126.
60. Johnston A.L., File S.E. Sex differences in animal tests of anxiety. Physiol. Behav. 49:1991;245-250.
61. Juraska J.M. Sex differences in 'cognitive' regions of the rat brain. Psychoneuroendocrinology. 16:1991;105-119.
62. Kalen P., Rosegren E., Lindvall O., Bjorkland A. Hippocampal noradrenaline and serotonin release over 24 hours as measured by the dialysis technique in freely moving rats: correlation to behavioral activity state, effect of handling and tail-pinch. Eur. J. Neurosci. 1:1989;181-188.
63. Kaufman H., Vadasz C., Lajtha A. Effect of estradiol on choline acetyltransferase activity in various brain regions. Brain Res. 453:1983;389-392.
64. Kennet G.A., Chaouloff F., Marcou M., Curzon G. Female rats are more vulnerable than males in an animal model of depression: the possible role of serotonin. Brain Res. 382:1986;416-421.
65. Kepler K.L., Standifer K.M., Paul D., Kest B., Pasternak G.W., Bodnar R.J. Differential gender effects upon central opioid analgesia. Pain. 45:1991;87-94.
66. Khanna S., Sinclair J.G. Noxious stimuli produce prolonged changes in the CA1 region of the rat hippocampus. Pain. 39:1989;337-343.
67. Khanna S., Sinclair J.G. Responses in the CA1 region of the rat hippocampus to a noxious stimulus. Exp. Neurol. 117:1992;28-35.
68. Kitay J.I. Sex differences in adrenal cortical secretion in the rat. Endocrinology. 68:1961;818-824.
69. Kus L., Handa R.J., Hautman J.M., Beitz A.J. Castration increases [125I] binding in the hippocampus of male rats. Brain Res. 683:1995;270-274.
70. Loy R., Sheldon R.A. Sexually dimorphic development of cholinergic enzymes in the rat septohippocampal system. Dev. Brain Res. 34:1987;245-251.
71. Luine V.N. Estradiol increases choline acetyltransferase activity in specific basal forebrain nuclei and projection areas of female rats. Exp. Neurol. 89:1984;484-490.
72. MacLusky N.J., Yuan H., Elliott J., Brown T.J. Sex differences in corticosteroid binding in the rat brain: an in vitro autoradiographic study. Brain Res. 708:1996;71-81.
73. Maren S., De Oca B., Fanselow M.S. Sex differences in hippocampal long-term potentiation (LTP) and Pavlovian fear conditioning in rats: positive correlation between LTP and contextual learning. Brain Res. 661:1994;25-34.
74. Matera C., Wardlaw S.L. Dopamine and sex steroid regulation of PAMC gene expression in the hypothalamus. Neuroendocrinology. 58:1993;493-500.
75. McEwen B.S. Gonadal and adrenal steroids regulate neurochemical and structural plasticity of the hippocampus via cellular mechanisms involving NMDA receptors. Cell. Mol. Neurobiol. 16:1996;103-116.
76. B.S. McEwen, E. Gould, M. Orchinik, N.G. Weiland, C.S. Wolley, Oestrogens and the structural and functional plasticity of neurons: implications for memory, ageing and neurodegenerative processes, in: Wiley, Chichester (Ciba Foundation Symposium 191), Non-Reproductive Actions of Sex Steroids, 1995, pp. 52-73.
77. Meagher M.W., Grau J.W., King R.A. Role of supraspinal systems in environmentally induced antinociception: effect of spinalization and decerebration on brief shock-induced and long shock-induced antinociception. Behav. Neurosci. 104:1990;328-338.
78. Millan M.J. Serotonin (5-HT) and pain: a reappraisal of its role in the light of receptor multiplicity. Seminar Neurosci. 7:1995;409-419.
79. Moroni F., Cheney D.L., Costa E. β-Endorphin inhibits ACh turnover in nuclei of rat brain. Nature. 267:1977;267-268.
80. Morrell J.I., Pfaff D.W. Characterization of estrogen concentrating hypothalamic neurons by their axonal projections. Science. 217:1982;1273-1276.
81. Morris B.J., Johnston H.M. A role for hippocampal opioids in long-term functional plasticity. Trends Neurosci. 18:1995;350-355.
82. Munck A., Guyre P.M., Holbrook N.J. Physiological functions of glucocorticoids in stress and their relationship to pharmacological actions. Endocr. Rev. 5:1984;25-44.
83. Munglani R., Hunt S.P. Molecular biology of pain. Br. J. Anaesth. 75:1995;186-192.
84. Muth E.A., Crowley W.R., Jacobowitz D.M. Effect of gonadal hormones on luteinizing hormone in plasma and on choline acetyltransferase activity and acetylcholine levels in discrete nuclei of the rat brain. Neuroendocrinology. 30:1980;329-336.
85. P. Negri-Cesi, A. Colciago, F. Celotti, The role of aromatase in the brain, in: A.R. Gennazzani, F. Petraglia, R.H. Purdy (Eds.), The Brain: Source and Target for Sex Steroid Hormones, Parthenon Publishing, New York, 1996, pp. 135-149.
86. Nicoll R.A., Siggins G.R., Ling N., Bloom F.E., Guillemin R. Neuronal actions of endorphins and enkephalins among brain regions: a comparative microiontophoretic study. Proc. Natl. Acad. Sci. USA. 74:1977;2584-2588.
87. O'Connor L.H., Nock B., McEwen B.S. Regional specificity of gamma-aminobutyric acid receptor regulation of estradiol. Neuroendocrinology. 47:1988;473-481.
88. Ohkura T., Isse K., Akazawa K., Hamamoto M., Yaoi Y., Hagino N. Low-dose estrogen replacement therapy for Alzheimer disease in women. Menopause. 1:1994;125-130.
89. Parducz A., Garcia-Segura L.M. Sexual differences in the synaptic connectivity in the rat dentate gyrus. Neurosci. Lett. 161:1993;53-56.
90. G. Paxinos, (Ed.), The Rat Nervous System, 2nd ed., Academic Press, San Diego, USA, 1995, 1136 pp.
91. Pennypacker K.R., Hong J.-S., McMillian M.K. Implications of prolonged expression of Fos-related antigens. Trends Pharmacol. Sci. 16:1995;317-321.
92. Pérez J., Zucchi I., Maggi A. Sexual dimorphism in the response of the GABAergic system to estrogen administration. J. Neurochem. 47:1986;1798-1803.
93. Pilgrim C., Hutchison J.B. Developmental regulation of sex differences in the brain: can the role of gonadal steroids be redefined? Neuroscience. 60:1994;843-855.
94. Roof R., Havens M.D. Testosterone improves maze performance and induces development of a male hippocampus in females. Brain Res. 572:1992;310-313.
95. Sapolsky R.M. Glucocorticoids and hippocampal damage. Trends Neurosci. 10:1987;346-349.
96. Sapolsky R.M., Krey L.C., McEwen B. Prolonged glucocorticoid exposure reduces hippocampal neuron number: implication for aging. J. Neurosci. 5:1985;1222-1227.
97. Sapolsky R.M. Stress, glucocorticoids, and damage to the nervous system: the current state of confusion. Stress. 1:1996;1-19.
98. Seeman T.E., Singer B., Charpentier P. Gender differences in patterns of HPA axis response to challenge: MacArthur studies of successful aging. Psychoneuroendocrinology. 20:1995;711-725.
99. Shimon M., Egozi Y., Kloog Y., Sokolovsky M., Cohen S. Kinetics of choline uptake into isolated rat forebrain microvessels: evidence of endocrine modulation. J. Neurochem. 50:1988;1719-1724.
100. Soulairac A., Gottesmann C.L., Charpentier J. Effects of pain and of several central analgesics on cortex, hippocampus and reticular formation of brain stem. Int. J. Neuropharmacol. 6:1967;71-81.
101. Steenbergen H.L., Farabollini F., Heinsbroek R.P.W., Van de Poll N.E. Sex-dependent effects of aversive stimulation on holeboard and elevated plus-maze behavior. Behav. Brain Res. 43:1991;159-165.
102. Stein E.A., Hiller J.M., Simon E.J. Effects of stress on opioid receptor binding in the rat central nervous system. Neuroscience. 51:1992;683-690.
103. G. Tabason, I. Johnson, Sex differences in the response to placebo transcutaneous electrical nerve stimulation (TENS) in healthy subjects, 8th World Congress on Pain, Vancouver 1996, Abstr. 234, p. 507.
104. Terman G.W., Wagner J.J., Chavkin C. Kappa opioids inhibit induction of long-term potentiation in the dentate gyrus of the guinea pig hippocampus. J. Neurosci. 14:1994;4740-4747.
105. Teyler T.J., Vardaris R.M., Lewis D., Rawitch A.B. Gonadal steroids: effects on excitability of hippocampal pyramidal cells. Science. 209:1980;1017-1018.
106. Turner B.B., Weaver D.A. Sexual dimorphism of glucorticoid binding in rat brain. Brain Res. 343:1985;16-23.
107. Turner B.B. Sex differences in the binding of Type I and Type II corticosteroid receptors in the rat hippocampus. Brain Res. 581:1992;229-236.
108. Turner J.P. Potentiation of the GABA analogue muscimol by physiologically occurring steroids. Br. J. Pharmacol. 87:1986;148P.
109. Unruh A.M. Gender variations in clinical pain experience. Pain. 65:1996;123-167.
110. Van Hareen F., Van Hest A., Heinsbroek R.P.W. Behavioral differences between male and female rats: effects of gonadal hormones on learning and memory. Neurosci. Biobehav. Rev. 14:1990;23-33.
111. Van Oyen H.G., Walg H., Van de Poll N.E. Discriminated lever-press avoidance conditioning in male and female rats. Physiol. Behav. 26:1981;313-317.
112. Van Oyen H.G., Van de Poll N.E., De Bruin J.P.C. Sex, age and shock-intensity as factors in passive avoidance. Physiol. Behav. 23:1979;915-918.
113. O.M. Wolkowitz, V.I. Reus, Dehydroepiandrosterone treatment of depression and memory disorders, in: A.R. Gennazzani, F. Petraglia, R.H. Purdy (Eds.), The Brain: Source and Target for Sex Steroid Hormones, Parthenon Publishing, New York, 1996, pp. 243-256.
114. Wu D., Hersh L.B. Choline acetyltransferase: celebrating its fiftieth year. J. Neurochem. 62:1994;1653-1663.
115. Zimmermann M., Herdegen T. Control of gene transcription by Jun and Fos proteins in the nervous system. Beneficial or harmful molecular mechanisms of neuronal responses to noxious stimulation? Am. Pain Soc. J. 3:1994;33-48.