Effects of 17β-estradiol on responses of viscerosomatic convergent thalamic neurons in the ovariectomized female rat

Journal of Neurophysiology

Volumn 102, Issue 2, 2009, Pages 1062-1074

  Reed, William R ^a   Chadha, Harpreet K ^a   Hubscher, Charles H ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; ESTROGEN;

ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; COLON; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ESTRUS CYCLE; FEMALE; HORMONE ACTION; NERVE STIMULATION; NEUROPATHIC PAIN; NOCICEPTIVE STIMULATION; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; RAT; SOMATOSENSORY CORTEX; THALAMUS NUCLEUS; TRUNK; VAGINA; VISCERAL PAIN; ACTION POTENTIAL; ANIMAL; DRUG EFFECT; ELECTROSTIMULATION; HINDLIMB; NERVE CELL; PERCEPTIVE THRESHOLD; PHYSIOLOGY; PRESSURE; STIMULATION; THALAMUS; THORAX; TOUCH; UTERINE CERVIX; WISTAR RAT;

ACTION POTENTIALS; ANIMALS; CERVIX UTERI; COLON; ELECTRIC STIMULATION; ESTRADIOL; ESTROGENS; FEMALE; HINDLIMB; NEURONS; OVARIECTOMY; PHYSICAL STIMULATION; PRESSURE; RATS; RATS, WISTAR; SENSORY THRESHOLDS; THALAMUS; THORAX; TOUCH PERCEPTION; VAGINA;

EID: 68149181454     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00165.2009     Document Type: Article

References (165)

1. Adler NT, Davis PG, Komisaruk BR. Variation in the size and sensitivity of a genital sensory field in relation to the estrous cycle in rats. Horm Behav 9: 334-344, 1977.
2. Albert DJ, Jonik RH, Gorzalka BB, Newlove T, Webb B, Walsh ML. Serum estradiol concentration required to maintain body weight, attractivity, proceptivity, and receptivity in the ovariectomized female rat. Physiol Behav 49: 225-231, 1991.
3. Aloisi AM, Bonifazi M. Sex hormones, central nervous system and pain. Horm Behav 50: 1-7, 2006.
4. Aloisi AM, Ceccarelli I. Role of gonadal hormones in formalin-induced pain responses of male rats: modulation by estradiol and naloxone administration. Neuroscience 95: 559-566, 2000.
5. Amandusson A, Hallbeck M, Hallbeck AL, Hermanson O, Blomqvist A. Estrogen-induced alterations of spinal cord enkephalin gene expression. Pain 83: 243-248, 1999.
6. Andersson JL, Lilja A, Hartvig P, Langstrom B, Gordh T, Handwerker H, Torebjork E. Somatotopic organization along the central sulcus, for pain localization in humans, as revealed by positron emission tomography. Exp Brain Res 117: 192-199, 1997.
7. Atkinson RM, Davis B, Pratt MA, Sharpe HM, Tomich EG. Action of some steroids on the central nervous system of the mouse. II. Pharmacology. J Med Chem 8: 426-432, 1965.
8. Beatty WW. Gonadal hormones and sex differences in nonreproductive behaviors in rodents: organizational and activational influences. Horm Behav 12: 112-163, 1979.
9. Beatty WW. Gonadal hormones and sex differences in nonreproductive behaviors. In: Handbook of Behavioral Neurobiology: Sexual Differentiation, edited by Gerall AA, Moltz H, Ward IL. New York: Plenum Press, 1992, vol. 11, p. 85-128.
10. Becker JB, Arnold AP, Berkley KJ, Blaustein JD, Eckel LA, Hampson E, Herman JP, Marts S, Sadee W, Steiner M, Taylor J, Young E. Strategies and methods for research on sex differences in brain and behavior. Endocrinology 146: 1650-1673, 2005.
11. Bereiter DA, Cioffi JL, Bereiter DF. Oestrogen receptor-immunoreactive neurons in the trigeminal sensory system of male and cycling female rats. Arch Oral Biol 50: 971-979, 2005.
12. Berkley KJ. Sex differences in pain. Behav Brain Sci 20: 371-380, 1997.
13. Berkley KJ, Benoist JM, Gautron M, Guilbaud G. Responses of neurons in the caudal intralaminar thalamic complex of the rat to stimulation of the uterus, vagina, cervix, colon and skin. Brain Res 695: 92-95, 1995.
14. Berkley KJ, Guilbaud G, Benoist JM, Gautron M. Responses of neurons in and near the thalamic ventrobasal complex of the rat to stimulation of uterus, cervix, vagina, colon, and skin. J Neurophysiol 69: 557-568, 1993.
15. A receptors by estradiol: a clue for CNS changes occurring at menopause. Cell Mol Neurobiol 16: 199-212, 1996.
16. Bradshaw HB, Berkley KJ. Estrous changes in responses of rat gracile nucleus neurons to stimulation of skin and pelvic viscera. J Neurosci 20: 7722-7727, 2000.
17. Bradshaw HB, Berkley KJ. The influence of ovariectomy with or without estrogen replacement on responses of rat gracile nucleus neurons to stimulation of hindquarter skin and pelvic viscera. Brain Res 986: 82-90, 2003.
18. Bradshaw HB, Temple JL, Wood E, Berkley KJ. Estrous variations in behavioral responses to vaginal and uterine distention in the rat. Pain 82: 187-197, 1999.
19. Bridges RS. A quantitative analysis of the roles of dosage, sequence, and duration of estradiol and progesterone exposure in the regulation of maternal behavior in the rat. Endocrinology 114: 930-940, 1984.
20. Brobeck JR, Wheatland M, Strominger JL. Variations in regulation of energy exchange associated with estrus, diestrus, and pseudo-pregnancy in rats. Endocrinology 40: 65-72, 1947.
21. Bruggemann J, Shi T, Apkarian AV. Viscerosomatic interactions in the thalamic ventral posterolateral nucleus (VPL) of the squirrel monkey. Brain Res 787: 269-276, 1998.
22. Cairns BE, Svensson P, Wang K, Hupfeld S, Graven-Nielsen T, Sessle BJ, Berde CB, Arendt-Nielsen L. Activation of peripheral NMDA receptors contributes to human pain and rat afferent discharges evoked by injection of glutamate into the masseter muscle. J Neurophysiol 90: 2098-2105, 2003.
23. Castro-Vazquez A, Carreno NB. Estrogen but not progesterone facilitates the lordosis reaction to cervicovaginal stimulation of ovariectomized rats. Physiol Behav 35: 21-24, 1985.
24. Ceccarelli I, Fiorenzani P, Massafra C, Aloisi AM. Long-term ovariectomy changes formalin-induced licking in female rats: the role of estrogens (Abstract). Reprod Biol Endocrinol 1: 24, 2003.
25. Cervero F, Laird JM. Visceral pain. Lancet 353: 2145-2148, 1999.
26. ++ signaling in mouse dorsal root ganglion neurons. J Neurosci Res 81: 31-37, 2005.
27. Chadha HK, Hubscher CH. Convergence of nociceptive information in the forebrain of female rats: reproductive organ response variations with stage of estrus. Exp Neurol 210: 375-387, 2008.
28. Chiodo LA, Caggiula AR. Alterations in basal firing rate and autoreceptor sensitivity of dopamine neurons in the substantia nigra following acute and extended exposure to estrogen. Eur J Pharmacol 67: 165-166, 1980.
29. Choi JC, Park SK, Kim YH, Shin YW, Kwon JS, Kim JS, Kim JW, Kim SY, Lee SG, Lee MS. Different brain activation patterns to pain and pain-related unpleasantness during the menstrual cycle. Anesthesiology 105: 120-127, 2006.
30. Cimino R, Farella M, Michelotti A, Pugliese R, Martina R. Does the ovarian cycle influence the pressure-pain threshold of the masticatory muscles in symptom-free women? J Orofac Pain 14: 105-111, 2000.
31. Cliffer KD, Burstein R, Giesler GJ Jr. Distributions of spinothalamic, spinohypothalamic, and spinotelencephalic fibers revealed by anterograde transport of PHA-L in rats. J Neurosci 11: 852-868, 1991.
32. Coughlan T, Gibson C, Murphy S. Modulatory effects of progesterone on inducible nitric oxide synthase expression in vivo and in vitro. J Neurochem 93: 932-942, 2005.
33. Craft RM. Sex differences in drug- and non-drug-induced analgesia. Life Sci 72: 2675-2688, 2003a.
34. Craft RM. Sex differences in opioid analgesia: "from mouse to man." Clin J Pain 19: 175-186, 2003b.
35. Craft RM, Mogil JS, Aloisi AM. Sex differences in pain and analgesia: the role of gonadal hormones. Eur J Pain 8: 397-411, 2004.
36. Craft RM, Ulibarri C, Leitl MD, Sumner JE. Dose- and time-dependent estradiol modulation of morphine antinociception in adult female rats. Eur J Pain 12: 472-479, 2008.
37. Crowley WR, Jacobs R, Volpe J, Rodriguez-Sierra JF, Komisaruk BR. Analgesic effect of vaginal stimulation in rats: modulation by graded stimulus intensity and hormones. Physiol Behav 16: 483-488, 1976.
38. Cyr M, Ghribi O, Di Paolo T. Regional and selective effects of oestradiol and progesterone on NMDA and AMPA receptors in the rat brain. J Neuroendocrinol 12: 445-452, 2000.
39. D'Amico JF, Greendale GA, Lu JK, Judd HL. Induction of hypothalamic opioid activity with transdermal estradiol administration in postmenopausal women. Fertil Steril 55: 754-758, 1991.
40. Danzebrink RM, Green SA, Gebhart GF. Spinal mu and delta, but not kappa, opioid-receptor agonists attenuate responses to noxious colorectal distension in the rat. Pain 63: 39-47, 1995.
41. Dawson-Basoa M, Gintzler AR. Nociceptin (Orphanin FQ) abolishes gestational and ovarian sex steroid-induced antinociception and induces hyperalgesia. Brain Res 750: 48-52, 1997.
42. Dawson-Basoa MB, Gintzler AR. 17-Beta-estradiol and progesterone modulate an intrinsic opioid analgesic system. Brain Res 601: 241-245, 1993.
43. Dawson-Basoa ME, Gintzler AR. Estrogen and progesterone activate spinal kappa-opiate receptor analgesic mechanisms. Pain 64: 608-615, 1996.
44. Dean SA, Tan J, O'Brien ER, Leenen FH. 17β-Estradiol downregulates tissue angiotensin-converting enzyme and ANG II type 1 receptor in female rats. Am J Physiol Regul Integr Comp Physiol 288: R759-R766, 2005.
45. de Leeuw R, Albuquerque RJ, Andersen AH, Carlson CR. Influence of estrogen on brain activation during stimulation with painful heat. J Oral Maxillofac Surg 64: 158-166, 2006.
46. Detsch O, Vahle-Hinz C, Kochs E, Siemers M, Bromm B. Isoflurane induces dose-dependent changes of thalamic somatosensory information transfer. Brain Res 829: 77-89, 1999.
47. Diogenes A, Patwardhan AM, Jeske NA, Ruparel NB, Goffin V, Akopian AN, Hargreaves KM. Prolactin modulates TRPV1 in female rat trigeminal sensory neurons. J Neurosci 26: 8126-8136, 2006.
48. Dostrovsky JO, Guilbaud G. Noxious stimuli excite neurons in nucleus submedius of the normal and arthritic rat. Brain Res 460: 269-280, 1988.
49. Dostrovsky JO, Guilbaud G. Nociceptive responses in medial thalamus of the normal and arthritic rat. Pain 40: 93-104, 1990.
50. Drewett RF. Oestrous and dioestrous components of the ovarian inhibition on hunger in the rat. Anim Behav 21: 772-780, 1973.
51. Drury RA, Gold RM. Differential effects of ovarian hormones on reactivity to electric footshock in the rat. Physiol Behav 20: 187-191, 1978.
52. Feder HH. Estrous cyclicity in mammals. In: Neuroendocrinology of Reproduction, edited by Adler NT. New York: Plenum Press, 1981, p. 279-348.
53. Fillingim RB, Gear RW. Sex differences in opioid analgesia: clinical and experimental findings. Eur J Pain 8: 413-425, 2004.
54. Fillingim RB, Maixner W, Girdler SS, Light KC, Harris MB, Sheps DS, Mason GA. Ischemic but not thermal pain sensitivity varies across the menstrual cycle. Psychosom Med 59: 512-520, 1997.
55. Fillingim RB, Ness TJ. Sex-related hormonal influences on pain and analgesic responses. Neurosci Biobehav Rev 24: 485-501, 2000.
56. Flores CA, Shughrue P, Petersen SL, Mokha SS. Sex-related differences in the distribution of opioid receptor-like 1 receptor mRNA and colocalization with estrogen receptor mRNA in neurons of the spinal trigeminal nucleus caudalis in the rat. Neuroscience 118: 769-778, 2003.
57. Foy MR, Xu J, Xie X, Brinton RD, Thompson RF, Berger TW. 17β-Estradiol enhances NMDA receptor-mediated EPSPs and long-term potentiation. J Neurophysiol 81: 925-929, 1999.
58. Frye CA, Bock BC, Kanarek RB. Hormonal milieu affects tailflick latency in female rats and may be attenuated by access to sucrose. Physiol Behav 52: 699-706, 1992.
59. Frye CA, Cuevas CA, Kanarek RB. Diet and estrous cycle influence pain sensitivity in rats. Pharmacol Biochem Behav 45: 255-260, 1993.
60. A receptor complex, attenuate pain sensitivity in rats. Brain Res 643: 194-203, 1994.
61. Giamberardino MA, Affaitati G, Valente R, Iezzi S, Vecchiet L. Changes in visceral pain reactivity as a function of estrous cycle in female rats with artificial ureteral calculosis. Brain Res 774: 234-238, 1997a.
62. Giamberardino MA, Berkley KJ, Iezzi S, de Bigontina P, Vecchiet L. Pain threshold variations in somatic wall tissues as a function of menstrual cycle, segmental site and tissue depth in non-dysmenorrheic women, dysmenorrheic women and men. Pain 71: 187-197, 1997b.
63. Giesler GJ Jr, Spiel HR, Willis WD. Organization of spinothalamic tract axons within the rat spinal cord. J Comp Neurol 195: 243-252, 1981a.
64. Giesler GJ Jr, Yezierski RP, Gerhart KD, Willis WD. Spinothalamic tract neurons that project to medial and/or lateral thalamic nuclei: evidence for a physiologically novel population of spinal cord neurons. J Neurophysiol 46: 1285-1308, 1981b.
65. Gingold SI, Greenspan JD, Apkarian AV. Anatomic evidence of nociceptive inputs to primary somatosensory cortex: relationship between spinothalamic terminals and thalamocortical cells in squirrel monkeys. J Comp Neurol 308: 467-490, 1991.
66. Gintzler AR, Bohan MC. Pain thresholds are elevated during pseudopregnancy. Brain Res 507: 312-316, 1990.
67. Greenspan JD, Craft RM, LeResche L, Arendt-Nielsen L, Berkley KJ, Fillingim RB, Gold MS, Holdcroft A, Lautenbacher S, Mayer EA, Mogil JS, Murphy AZ, Traub RJ. Studying sex and gender differences in pain and analgesia: a consensus report. Pain 132, Suppl. 1: S26-S45, 2007.
68. Gu Q, Moss RL. 17β-Estradiol potentiates kainate-induced currents via activation of the cAMP cascade. J Neurosci 16: 3620-3629, 1996.
69. Gupta DS, von Gizycki H, Gintzler AR. Sex-/ovarian steroid-dependent release of endomorphin 2 from spinal cord. J Pharmacol Exp Ther 321: 635-641, 2007.
70. Hargraves WA, Hentall ID. Analgesic effects of dietary caloric restriction in adult mice. Pain 114: 455-461, 2005.
71. Haskins JT, Moss RL. Action of estrogen and mechanical vaginocervical stimulation on the membrane excitability of hypothalamic and midbrain neurons. Brain Res Bull 10: 489-496, 1983.
72. Hellstrom B, Anderberg UM. Pain perception across the menstrual cycle phases in women with chronic pain. Percept Mot Skills 96: 201-211, 2003.
73. Hicks TP, Metherate R, Landry P, Dykes RW. Bicuculline-induced alterations of response properties in functionally identified ventroposterior thalamic neurones. Exp Brain Res 63: 248-264, 1986.
74. Hitt JC, Gerall AA, Giantonio GW. Detection of estrous activity cycle by 1-hour samples of running behavior. Psychonom Sci 10: 159-160, 1968.
75. Hubscher CH. Estradiol-associated variation in responses of rostral medullary neurons to somatovisceral stimulation. Exp Neurol 200: 227-239, 2006.
76. Hubscher CH, Brooks DL, Johnson JR. A quantitative method for assessing stages of the rat estrous cycle. Biotech Histochem 80: 79-87, 2005.
77. Hubscher CH, Johnson RD. Responses of medullary reticular formation neurons to input from the male genitalia. J Neurophysiol 76: 2474-2482, 1996.
78. Hubscher CH, Johnson RD. Changes in neuronal receptive field characteristics in caudal brain stem following chronic spinal cord injury. J Neurotrauma 16: 533-541, 1999.
79. Hubscher CH, Johnson RD. Differential effects of chronic spinal hemisection on somatic and visceral inputs to caudal brainstem. Brain Res 947: 234-242, 2002.
80. Hubscher CH, Johnson RD. Responses of thalamic neurons to input from the male genitalia. J Neurophysiol 89: 2-11, 2003.
81. Hubscher CH, Johnson RD. Chronic spinal cord injury induced changes in the responses of thalamic neurons. Exp Neurol 197: 177-188, 2006.
82. Hubscher CH, Kaddumi EG, Johnson RD. Brain stem convergence of pelvic viscerosomatic inputs via spinal and vagal afferents. Neuroreport 15: 1299-1302, 2004.
83. Ji Y, Traub RJ. Spinal NMDA receptors contribute to neuronal processing of acute noxious and nonnoxious colorectal stimulation in the rat. J Neurophysiol 86: 1783-1791, 2001.
84. Joh HD, Searles RV, Selmanoff M, Alkayed NJ, Koehler RC, Hurn PD, Murphy SJ. Estradiol alters only GAD67 mRNA levels in ischemic rat brain with no consequent effects on GABA. J Cereb Blood Flow Metab 26: 518-526, 2006.
85. Johnson RD, Hubscher CH. Brainstem microstimulation differentially inhibits pudendal motoneuron reflex inputs. Neuroreport 9: 341-345, 1998.
86. Johnson RD, Murray FT. Reduced sensitivity of penile mechanoreceptors in aging rats with sexual dysfunction. Brain Res Bull 28: 61-64, 1992.
87. Kaddumi EG, Hubscher CH. Convergence of multiple pelvic organ inputs in the rat rostral medulla. J Physiol 572: 393-405, 2006.
88. Kaddumi EG, Hubscher CH. Changes in rat brainstem responsiveness to somatovisceral inputs following acute bladder irritation. Exp Neurol 203: 349-357, 2007a.
89. Kaddumi EG, Hubscher CH. Urinary bladder irritation alters efficacy of vagal stimulation on rostral medullary neurons in chronic T8 spinalized rats. J Neurotrauma 24: 1219-1228, 2007b.
90. Kawakita K, Dostrovsky JO, Tang JS, Chiang CY. Responses of neurons in the rat thalamic nucleus submedius to cutaneous, muscle and visceral nociceptive stimuli. Pain 55: 327-338, 1993.
91. Kawakita K, Sumiya E, Murase K, Okada K. Response characteristics of nucleus submedius neurons to colo-rectal distension in the rat. Neurosci Res 28: 59-66, 1997.
92. Kayser V, Berkley KJ, Keita H, Gautron M, Guilbaud G. Estrous and sex variations in vocalization thresholds to hindpaw and tail pressure stimulation in the rat. Brain Res 742: 352-354, 1996.
93. Kevetter GA, Willis WD. Collaterals of spinothalamic cells in the rat. J Comp Neurol 215: 453-464, 1983.
94. Khasar SG, Miao FJ, Janig W, Levine JD. Vagotomy-induced enhancement of mechanical hyperalgesia in the rat is sympathoadrenal-mediated. J Neurosci 18: 3043-3049, 1998.
95. Kow LM. Sensory requirements for the lordosis reflex in female rats. Brain Res 101: 47-66, 1976.
96. Kow LM, Malsbury CW, Pfaff DW. Lordosis in the male golden hamster elicited by manual stimulation: characteristics and hormonal sensitivity. J Comp Physiol Psychol 90: 26-40, 1976.
97. Kow LM, Montgomery MO, Pfaff DW. Triggering of lordosis reflex in female rats with somatosensory stimulation: quantitative determination of stimulus parameters. J Neurophysiol 42: 195-202, 1979.
98. Kow LM, Pfaff DW. Effects of estrogen treatment on the size of receptive field and response threshold of pudendal nerve in the female rat. Neuroendocrinology 13: 299-313, 1973.
99. Ma W, Peschanski M, Besson JM. The overlap of spinothalamic and dorsal column nuclei projections in the ventrobasal complex of the rat thalamus: a double anterograde labeling study using light microscopy analysis. J Comp Neurol 245: 531-540, 1986.
100. Maggi A, Perez J. Progesterone and estrogens in rat brain: modulation of GABA (gamma-aminobutyric acid) receptor activity. Eur J Pharmacol 103: 165-168, 1984.
101. Mannino CA, South SM, Quinones-Jenab V, Inturrisi CE. Estradiol replacement in ovariectomized rats is antihyperalgesic in the formalin test. J Pain 8: 334-342, 2007.
102. Martin VT, Behbehani M. Ovarian hormones and migraine headache: understanding mechanisms and pathogenesis - part I. Headache 46: 3-23, 2006a.
103. Martin VT, Behbehani M. Ovarian hormones and migraine headache: understanding mechanisms and pathogenesis - part 2. Headache 46: 365-386, 2006b.
104. Martinez V, Wang L, Tache Y. Proximal colon distention induces Fos expression in the brain and inhibits gastric emptying through capsaicin-sensitive pathways in conscious rats. Brain Res 1086: 168-180, 2006.
105. Martinez-Gomez M, Cruz Y, Salas M, Hudson R, Pacheco P. Assessing pain threshold in the rat: changes with estrus and time of day. Physiol Behav 55: 651-657, 1994.
106. Massey JM, Hubscher CH, Wagoner MR, Decker JA, Amps J, Silver J, Onifer SM. Chondroitinase ABC digestion of the perineuronal net promotes functional collateral sprouting in the cuneate nucleus after cervical spinal cord injury. J Neurosci 26: 4406-4414, 2006.
107. Mayer EA, Berman S, Chang L, Naliboff BD. Sex-based differences in gastrointestional pain. Eur J Pain 8: 451-463, 2004.
108. McEwen B. Estrogen actions throughout the brain. Recent Prog Horm Res 57: 357-384, 2002.
109. McEwen BS, Alves SE, Bulloch K, Weiland NG. Ovarian steroids and the brain: implications for cognition and aging. Neurology 48: S8-S15, 1997.
110. McKenna KE, Chung SK, McVary KT. A model for the study of sexual function in anesthetized male and female rats. Am J Physiol Regul Integr Comp Physiol 261: R1276-R1285, 1991.
111. Melzack R. From the gate to the neuromatrix. Pain Suppl 6: S121-S126, 1999.
112. Meyerson BJ. Relationship between the anesthetic and gestagenic action and estrous behavior-inducing activity of different progestins. Endocrinology 81: 369-374, 1967.
113. Monconduit L, Bourgeais L, Bernard JF, Villanueva L. Convergence of cutaneous, muscular and visceral noxious inputs onto ventromedial thalamic neurons in the rat. Pain 103: 83-91, 2003.
114. Monks DA, Getsios S, MacCalman CD, Watson NV. N-cadherin is regulated by gonadal steroids in the adult hippocampus. Proc Natl Acad Sci USA 98: 1312-1316, 2001.
115. Nakamura NH, Rosell DR, Akama KT, McEwen BS. Estrogen and ovariectomy regulate mRNA and protein of glutamic acid decarboxylases and cation-chloride cotransporters in the adult rat hippocampus. Neuroendocrinology 80: 308-323, 2004.
116. Nequin LG, Alvarez J, Schwartz NB. Measurement of serum steroid and gonadotropin levels and uterine and ovarian variables throughout 4 day and 5 day estrous cycles in the rat. Biol Reprod 20: 659-670, 1979.
117. Nishii H, Nomura M, Fujimoto N, Matsumoto T. Thalamic neural activation in the cyclophosphamide-induced visceral pain model in mice. Neurosci Res 60: 219-227, 2008.
118. Nishikawa Y, Koyama N, Yoshida Y, Yokota T. Activation of ascending antinociceptive system by vagal afferent input as revealed in the nucleus ventralis posteromedialis. Brain Res 833: 108-111, 1999.
119. Olson ME, Bruce J. Ovariectomy, ovariohysterectomy and orchidectomy in rodents and rabbits. Can Vet J 27: 523-527, 1986.
120. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. San Diego, CA: Academic Press, 1998.
121. Ploner M, Freund HJ, Schnitzler A. Pain affect without pain sensation in a patient with a postcentral lesion. Pain 81: 211-214, 1999.
122. Quadagno DM, Shryne J, Anderson C, Gorski RA. Influence of gonadal hormones on social, sexual, emergence, and open field behaviour in the rat (Rattus norvegicus). Anim Behav 20: 732-740, 1972.
123. Rainville P. Brain mechanisms of pain affect and pain modulation. Curr Opin Neurobiol 12: 195-204, 2002.
124. Rainville P, Duncan GH, Price DD, Carrier B, Bushnell MC. Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science 277: 968-971, 1997.
125. Ren K, Wei F, Dubner R, Murphy A, Hoffman GE. Progesterone attenuates persistent inflammatory hyperalgesia in female rats: involvement of spinal NMDA receptor mechanisms. Brain Res 865: 272-277, 2000.
126. Riley JL 3rd, 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.
127. Riley JL 3rd, Robinson ME, Wise EA, Price DD. A meta-analytic review of pain perception across the menstrual cycle. Pain 81: 225-235, 1999.
128. Robbins A, Berkley KJ, Sato Y. Estrous cycle variation of afferent fibers supplying reproductive organs in the female rat. Brain Res 596: 353-356, 1992.
129. Robbins MT, Uzzell TW, Aly S, Ness TJ. Visceral nociceptive input to the area of the medullary lateral reticular nucleus ascends in the lateral spinal cord. Neurosci Lett 381: 329-333, 2005.
130. Robichaud M, Debonnel G. Oestrogen and testosterone modulate the firing activity of dorsal raphe nucleus serotonergic neurones in both male and female rats. J Neuroendocrinol 17: 179-185, 2005.
131. Rodrigues AC, Nicholas Verne G, Schmidt S, Mauderli AP. Hypersensitivity to cutaneous thermal nociceptive stimuli in irritable bowel syndrome. Pain 115: 5-11, 2005.
132. Roesch DM. Effects of selective estrogen receptor agonists on food intake and body weight gain in rats. Physiol Behav 87: 39-44, 2006.
133. Rosas-Arellano MP, Solano-Flores LP, Ciriello J. Co-localization of estrogen and angiotensin receptors within subfornical organ neurons. Brain Res 837: 254-262, 1999.
134. Salt TE. Gamma-aminobutyric acid and afferent inhibition in the cat and rat ventrobasal thalamus. Neuroscience 28: 17-26, 1989.
135. Sanoja R, Cervero F. Estrogen-dependent abdominal hyperalgesia induced by ovariectomy in adult mice: a model of functional abdominal pain. Pain 118: 243-253, 2005.
136. Sapsed-Byrne S, Ma D, Ridout D, Holdcroft A. Estrous cycle phase variations in visceromotor and cardiovascular responses to colonic distension in the anesthetized rat. Brain Res 742: 10-16, 1996.
137. Selye H. Anesthetic effects of steroid hormones. Proc Soc Exp Biol Med 46: 116-121, 1941.
138. Serova LI, Maharjan S, Huang A, Sun D, Kaley G, Sabban EL. Response of tyrosine hydroxylase and GTP cyclohydrolase I gene expression to estrogen in brain catecholaminergic regions varies with mode of administration. Brain Res 1015: 1-8, 2004.
139. Sikes RW, Vogt BA. Nociceptive neurons in area 24 of rabbit cingulate cortex. J Neurophysiol 68: 1720-1732, 1992.
140. Simpkins JW, Anderson WR, Dawson R Jr, Bodor N. Effects of a brain-enhanced chemical delivery system for estradiol on body weight and food intake in intact and ovariectomized rats. Pharm Res 6: 592-600, 1989.
141. Simpkins JW, Anderson WR, Dawson R Jr, Seth A, Brewster M, Estes KS, Bodor N. Chronic weight loss in lean and obese rats with a brain-enhanced chemical delivery system for estradiol. Physiol Behav 44: 573-580, 1988.
142. Smith SS. Sensorimotor-correlated discharge recorded from ensembles of cerebellar Purkinje cells varies across the estrous cycle of the rat. J Neurophysiol 74: 1095-1108, 1995.
143. Smith SS. Estrous hormones enhance coupled, rhythmic olivary discharge in correlation with facilitated limb stepping. Neuroscience 82: 83-95, 1998.
144. Smith SS, Waterhouse BD, Woodward DJ. Sex steroid effects on extrahypothalamic CNS. I. Estrogen augments neuronal responsiveness to iontophoretically applied glutamate in the cerebellum. Brain Res 422: 40-51, 1987.
145. Smith SS, Waterhouse BD, Woodward DJ. Locally applied estrogens potentiate glutamate-evoked excitation of cerebellar Purkinje cells. Brain Res 475: 272-282, 1988.
146. Smith YR, Stohler CS, Nichols TE, Bueller JA, Koeppe RA, Zubieta JK. Pronociceptive and antinociceptive effects of estradiol through endogenous opioid neurotransmission in women. J Neurosci 26: 5777-5785, 2006.
147. Stoffel EC, Ulibarri CM, Craft RM. Gonadal steroid hormone modulation of nociception, morphine antinociception and reproductive indices in male and female rats. Pain 103: 285-302, 2003.
148. Talbot JD, Marrett S, Evans AC, Meyer E, Bushnell MC, Duncan GH. Multiple representations of pain in human cerebral cortex. Science 251: 1355-1358, 1991.
149. Tang B, Ji Y, Traub RJ. Estrogen alters spinal NMDA receptor activity via a PKA signaling pathway in a visceral pain model in the rat. Pain 137: 540-549, 2008.
150. Torres-Hernandez AR, Gonzalez-Vegas JA. Effects of 17β-estradiol on the spontaneous activity of substantia nigra neurons: evidence for a nongenomic mechanism. Brain Res 1049: 1-7, 2005.
151. Unruh AM. Gender variations in clinical pain experience. Pain 65: 123-167, 1996.
152. Vahle-Hinz C, Gottshaldt KM. Principal differences in the organization of the thalamic face representation in rodents and felids. In: Somatosensory Integration in the Thalamus, edited by Macchi G, Rustioni A, Spreafico R. Amsterdam: Elsevier, 1983, p. 125-145.
153. Vahle-Hinz C, Hicks TP. Temporal shaping of phasic neuronal responses by GABA- and non-GABA-mediated mechanisms in the somatosensory thalamus of the rat. Exp Brain Res 221: 310-321, 2003.
154. Vogt BA, Sikes RW. The medial pain system, cingulate cortex, and parallel processing of nociceptive information. Prog Brain Res 122: 223-235, 2000.
155. Wade GN, Schneider JE. Metabolic fuels and reproduction in female mammals. Neurosci Biobehav Rev 16: 235-272, 1992.
156. Willis WD, Coggeshall RE. Sensory Mechanisms of the Spinal Cord. New York: Plenum, 2004.
157. Woolf CJ. Long term alterations in the excitability of the flexion reflex produced by peripheral tissue injury in the chronic decerebrate rat. Pain 18: 325-343, 1984.
158. Woolf CJ, Thompson SW. The induction and maintenance of central sensitization is dependent on N-methyl-D-aspartic acid receptor activation; implications for the treatment of post-injury pain hypersensitivity states. Pain 44: 293-299, 1991.
159. Xu S, Cheng Y, Keast JR, Osborne PB. 17β-Estradiol activates estrogen receptor β-signaling and inhibits transient receptor potential vanilloid receptor 1 activation by capsaicin in adult rat nociceptor neurons. Endocrinology 149: 5540-5548, 2008.
160. Yang SW, Follett KA, Piper JG, Ness TJ. The effect of morphine on responses of mediodorsal thalamic nuclei and nucleus submedius neurons to colorectal distension in the rat. Brain Res 779: 41-52, 1998.
161. Yang SW, Follett KA, Piper JG, Ness TJ. The effect of morphine on responses of nucleus ventroposterolateralis neurons to colorectal distension in the rat. Brain Res Bull 48: 609-614, 1999.
162. Yezierski RP, Sorkin LS, Willis WD. Response properties of spinal neurons projecting to midbrain or midbrain-thalamus in the monkey. Brain Res 437: 165-170, 1987.
163. Young W, Boling J, Blandau R. The vaginal smear picture, sexual receptivity and time of ovulation in the albino rat. Anat Rec 80: 37-45, 1941.
164. Zhang DX, Carlton SM, Sorkin LS, Willis WD. Collaterals of primate spinothalamic tract neurons to the periaqueductal gray. J Comp Neurol 296: 277-290, 1990.
165. Zoubina EV, Fan Q, Smith PG. Variations in uterine innervation during the estrous cycle in rat. J Comp Neurol 397: 561-571, 1998.