Estrous cycle-dependent neural plasticity in the caudal brainstem in the female golden hamster: Ultrastructural and immunocytochemical studies of axo-dendritic relationships and dynamic remodeling

Hormones and Behavior

Volumn 54, Issue 5, 2008, Pages 627-639

  Gerrits, P O ^a   Kortekaas, R ^a   Veening, J G ^a,c,d   de Weerd, H ^a,b   Algra, A ^a,b   Mouton, L J ^a   van der Want, J J L ^b  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Brainstem; Cardiovascular regulation; Catecholamines; Estrogen; Lordosis; Mating behavior; Motoneurons; NTScom; Nucleus of the solitary tract; Sprouting

Indexed keywords

ESTROGEN RECEPTOR ALPHA;

AMBIGUUS NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN STEM; CONTROLLED STUDY; DENDRITE; ELECTRON MICROSCOPY; ESTRUS CYCLE; FEMALE; MALE; MORPHOLOGICAL TRAIT; NERVE CELL PLASTICITY; NERVE ENDING; NONHUMAN; NUCLEUS PARARETROAMBIGUUS; PRIORITY JOURNAL; SOLITARY TRACT NUCLEUS; SYRIAN HAMSTER;

ANIMALS; BRAIN STEM; CRICETINAE; DENDRITES; ESTROGEN RECEPTOR ALPHA; ESTROUS CYCLE; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; MESOCRICETUS; MODELS, BIOLOGICAL; NEURAL PATHWAYS; NEURONAL PLASTICITY; OVARIECTOMY; POSTURE; PRESYNAPTIC TERMINALS; SEXUAL BEHAVIOR, ANIMAL;

EID: 54149113118     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2008.06.006     Document Type: Article

References (76)

1. Attah M.Y., and Besch E.L. Estrous cycle variations of food and water intake in rats in the heat. J. Appl. Physiol. 42 (1977) 874-877
2. Bandler R., and Tork I. Midbrain periaqueductal grey region in the cat has afferent and efferent connections with solitary tract nuclei. Neurosci. Lett. 74 (1987) 1-6
3. Becker J.B., Arnold A.P., Berkley K.J., Blaustein J.D., Eckel L.A., Hampson E., Herman J.P., Marts S., Sadee W., Steiner M., Taylor J., and Young E. Strategies and methods for research on sex differences in brain and behavior. Endocrinology 146 (2005) 1650-1673
4. Blaustein J.D., Lehman M.N., Turcotte J.C., and Greene G. Estrogen receptors in dendrites and axon terminals in the guinea pig hypothalamus. Endocrinology 131 (1992) 281-290
5. Blaustein J.D., and Wade G.N. Ovarian hormones and meal patterns in rats: effects of progesterone and role of gastrointestinal transit. Physiol. Behav. 19 (1977) 23-27
6. Boers J., Gerrits P.O., Meijer E., and Holstege G. Estrogen receptor-alpha-immunoreactive neurons in the mesencephalon, pons and medulla oblongata of the female golden hamster. Neurosci. Lett. 267 (1999) 17-20
7. Calizo L.H., and Flanagan-Cato L.M. Hormonal-neural integration in the female rat ventromedial hypothalamus: triple labeling for estrogen receptor-alpha, retrograde tract tracing from the periaqueductal gray, and mating-induced Fos expression. Endocrinology 144 (2003) 5430-5440
8. Csakvari E., Hoyk Z., Gyenes A., Garcia-Ovejero D., Garcia-Segura L.M., and Parducz A. Fluctuation of synapse density in the arcuate nucleus during the estrous cycle. Neuroscience 144 (2007) 1288-1292
9. Danielsen J., and Buggy J. Depression of ad lib and angiotensin-induced sodium intake at oestrus. Brain. Res. Bull. 5 (1980) 501-504
10. Farkas E., Jansen A.S., and Loewy A.D. Periaqueductal gray matter projection to vagal preganglionic neurons and the nucleus tractus solitarius. Brain. Res. 764 (1997) 257-261
11. Findlay A.L., Fitzsimons J.T., and Kucharczyk J. Angiotensin-induced drinking fluctuates with the oestrous cycle [proceedings]. J. Physiol. 275 (1978) 29P-30P
12. Flanagan-Cato L.M., Lee B.J., and Calizo L.H. Co-localization of midbrain projections, progestin receptors, and mating-induced fos in the hypothalamic ventromedial nucleus of the female rat. Horm. Behav. 50 (2006) 52-60
13. Frank A.H., and Fraps R.M. Induction of estrous in the ovariectomized golden hamster. Endocrinology 37 (1945) 357-361
14. Frankfurt M., Gould E., Woolley C.S., and McEwen B.S. Gonadal steroids modify dendritic spine density in ventromedial hypothalamic neurons: a Golgi study in the adult rat. Neuroendocrinology 51 (1990) 530-535
15. Frye C.A., Cuevas C.A., and Kanarek R.B. Diet and estrous cycle influence pain sensitivity in rats. Pharmacol. Biochem. Behav. 45 (1993) 255-260
16. Gerrits P.O., and Holstege G. Pontine and medullary projections to the nucleus retroambiguus: a wheat germ agglutinin-horseradish peroxidase and autoradiographic tracing study in the cat. J. Comp. Neurol. 373 (1996) 173-185
17. Gerrits P.O., and Holstege G. Descending projections from the nucleus retroambiguus to the iliopsoas motoneuronal cell groups in the female golden hamster: possible role in reproductive behavior. J. Comp. Neurol. 403 (1999) 219-228
18. Gerrits P.O., Vodde C., and Holstege G. Retroambiguus projections to the cutaneus trunci motoneurons may form a pathway in the central control of mating. J. Neurophysiol. 83 (2000) 3076-3083
19. Gerrits P.O., Mouton L.J., de Weerd H., Georgiadis J.R., Krukerink M., and Holstege G. Ultrastructural evidence for a direct excitatory pathway from the nucleus retroambiguus to lateral longissimus and quadratus lumborum motoneurons in the female golden hamster. J. Comp. Neurol. 480 (2004) 352-363
20. Gerrits, P.O., de Weerd, H., Mouton, L.J., van der Want, J.J.L., 2006. Estrogen induced dendritic and axonal plasticity in the caudal brainstem in female golden hamster; ultrastructural and immunocytochemical studies of synaptic remodeling. Soc. for neurosci. Atlanta, pp. 1098.
21. Gerrits P.O., Veening J.G., Blomsma S.A., and Mouton L.J. The nucleus para-retroambiguus: a new group of estrogen receptive cells in the caudal ventrolateral medulla of the female golden hamster. Horm. Behav. 53 (2008) 329-341
22. Guevara-Guzman R., Buzo E., Larrazolo A., de la Riva C., Da Costa A.P., and Kendrick K.M. Vaginocervical stimulation-induced release of classical neurotransmitters and nitric oxide in the nucleus of the solitary tract varies as a function of the oestrus cycle. Brain. Res. 898 (2001) 303-313
23. Hardy S.G. Hypothalamic projections to cardiovascular centers of the medulla. Brain. Res. 894 (2001) 233-240
24. Herbert H., and Saper C.B. Organization of medullary adrenergic and noradrenergic projections to the periaqueductal gray matter in the rat. J. Comp. Neurol. 315 (1992) 34-52
25. Herbert H., Moga M.M., and Saper C.B. Connections of the parabrachial nucleus with the nucleus of the solitary tract and the medullary reticular formation in the rat. J. Comp. Neurol. 293 (1990) 540-580
26. Holstege G. Anatomical study of the final common pathway for vocalization in the cat. J. Comp. Neurol. 284 (1989) 242-252
27. Holstege G., Kerstens L., Moes M.C., and VanderHorst V.G. Evidence for a periaqueductal gray-nucleus retroambiguus-spinal cord pathway in the rat. Neuroscience 80 (1997) 587-598
28. Huang Z.G., Subramanian S.H., Balnave R.J., Turman A.B., and Moi Chow C. Roles of periaqueductal gray and nucleus tractus solitarius in cardiorespiratory function in the rat brainstem. Respir. Physiol. 120 (2000) 185-195
29. Hubscher C.H., and Berkley K.J. Responses of neurons in caudal solitary nucleus of female rats to stimulation of vagina, cervix, uterine horn and colon. Brain. Res. 664 (1994) 1-8
30. Jennings W.A. Estrous cycle and temporal pattern of feeding in female rats. Psychol. Rep. 34 (1974) 87-98
31. Johnston R.E. Sexual excitation function of hamster vaginal secretion. Anim. Learn. Behav. 3 (1975) 161-166
32. Johnston R.E., and Rasmussen K. Individual recognition of female hamsters by males: role of chemical cues and of the olfactory and vomeronasal systems. Physiol. Behav. 33 (1984) 95-104
33. Kent G.C. Physiology of reproduction. In: Hoffman R.,A., Robinson P.F., and Magalhaes H. (Eds). The Golden Hamster (1968), Iowa State University, Ames
34. Korte S.M., Jaarsma D., Luiten P.G., and Bohus B. Mesencephalic cuneiform nucleus and its ascending and descending projections serve stress-related cardiovascular responses in the rat. J. Auton. Nerv. Syst. 41 (1992) 157-176
35. Krukerink, M., Gerrits, P.O., Mouton, L.J.,Holstege, G., 2003. Two separate cell groups in the PAG project to two separate cell groups in the caudal ventrolateral medulla in the female hamster, Soc. for Neuroscience, New Orleans, p. 78.5
36. Laflamme N., Nappi R.E., Drolet G., Labrie C., and Rivest S. Expression and neuropeptidergic characterization of estrogen receptors (ERalpha and ERbeta) throughout the rat brain: anatomical evidence of distinct roles of each subtype. J. Neurobiol. 36 (1998) 357-378
37. Langub Jr. M.C., Maley B.E., and Watson Jr. R.E. Estrous cycle-associated axosomatic synaptic plasticity upon estrogen receptive neurons in the rat preoptic area. Brain. Res. 641 (1994) 303-310
38. Li H.Y., Blaustein J.D., De Vries G.J., and Wade G.N. Estrogen-receptor immunoreactivity in hamster brain: preoptic area, hypothalamus and amygdala. Brain Res. 631 2 (1993) 304-312
39. Lisk R.D. The Estrous Cycle (1985), Plenum Press, New York
40. Luckman S.M. Fos expression within regions of the preoptic area, hypothalamus and brainstem during pregnancy and parturition. Brain. Res. 669 (1995) 115-124
41. McCormick C.M., Smith C., and Mathews I.Z. Effects of chronic social stress in adolescence on anxiety and neuroendocrine response to mild stress in male and female rats. Behav. Brain. Res. 187 (2008) 228-238
42. Meisel R.L., and Luttrell V.R. Estradiol increases the dendritic length of ventromedial hypothalamic neurons in female Syrian hamsters. Brain. Res. Bull. 25 (1990) 165-168
43. Milner T.A., McEwen B.S., Hayashi S., Li C.J., Reagan L.P., and Alves S.E. Ultrastructural evidence that hippocampal alpha estrogen receptors are located at extranuclear sites. J. Comp. Neurol. 429 (2001) 355-371
44. Mora S., Dussaubat N., and Diaz-Veliz G. Effects of the estrous cycle and ovarian hormones on behavioral indices of anxiety in female rats. Psychoneuroendocrinology 21 (1996) 609-620
45. Murphy A.Z., and Hoffman G.E. Distribution of gonadal steroid receptor-containing neurons in the preoptic-periaqueductal gray-brainstem pathway: a potential circuit for the initiation of male sexual behavior. J. Comp. Neurol. 438 (2001) 191-212
46. Norgren R. Gustatory System. In: Paxinos G. (Ed). The Rat Nervous System (1995), Academic Press, San Diego 751-771
47. Norgren R., and Leonard C.M. Ascending central gustatory pathways. J. Comp. Neurol. 150 (1973) 217-237
48. Orsini M.W. The external vaginal phenomena characterizing the stages of the estrous cycle, pregnancy, pseudopregnancy, lactation and the anestrous hamster Mesocricetus auratus Waterhouse. Proc. Anim. Care. Panel. 11 (1961) 193-206
49. Osterlund M., Kuiper G.G., Gustafsson J.A., and Hurd Y.L. Differential distribution and regulation of estrogen receptor-alpha and -beta mRNA within the female rat brain. Brain. Res. Mol. Brain. Res. 54 (1998) 175-180
50. Palkovits M., and Zaborszky L. Neuroanatomy of central cardiovascular control. Nucleus tractus solitarii: afferent and efferent neuronal connections in relation to the baroreceptor reflex arc. Prog. Brain. Res. 47 (1977) 9-34
51. Pfaff D.W. Features of a hormone-driven defined neural circuit for a mammalian behavior. Principles illustrated, neuroendocrine syllogisms, and multiplicative steroid effects. Ann. N. Y. Acad. Sci. 563 (1989) 131-147
52. Reed C.A., and Reed R. The copulatory behavior of the golden hamster. J. Comp. Psychol. 39 (1946) 7-12
53. Roder S., and Ciriello J. Caudal ventrolateral medullary projections to the nucleus of the solitary tract in the cat. Neurosci. Lett. 134 (1992) 161-164
54. Ryan S.M., and Maier S.F. The estrous cycle and estrogen modulate stress-induced analgesia. Behav. Neurosci. 102 (1988) 371-380
55. Sa S.I., and Madeira M.D. Estrogen modulates the sexually dimorphic synaptic connectivity of the ventromedial nucleus. J. Comp. Neurol. 484 (2005) 68-79
56. Saleh T.M., and Connell B.J. Central nuclei mediating estrogen-induced changes in autonomic tone and baroreceptor reflex in male rats. Brain. Res. 961 (2003) 190-200
57. Saleh M.C., Connell B.J., and Saleh T.M. Autonomic and cardiovascular reflex responses to central estrogen injection in ovariectomized female rats. Brain. Res. 879 (2000) 105-114
58. Saleh T.M., Connell B.J., and Cribb A.E. Sympathoexcitatory effects of estrogen in the insular cortex are mediated by GABA. Brain. Res. 1037 (2005) 114-122
59. Saper C.B. Central autonomic system. In: Paxinos G. (Ed). The Rat Nervous System (1995), Academic Press, San Diego 107-135
60. Sawchenko P.E. Central connections of the sensory and motor nuclei of the vagus nerve. J. Auton. Nerv. Syst. 9 (1983) 13-26
61. Schwaber J.S., Kapp B.S., Higgins G.A., and Rapp P.R. Amygdaloid and basal forebrain direct connections with the nucleus of the solitary tract and the dorsal motor nucleus. J. Neurosci 2 (1982) 1424-1438
62. Shughrue P.J., Lane M.V., and Merchenthaler I. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J. Comp. Neurol. 388 (1997) 507-525
63. Turcotte J.C., and Blaustein J.D. Projections of the estrogen receptor-immunoreactive ventrolateral hypothalamus to other estrogen receptor-immunoreactive sites in female guinea pig brain. Neuroendocrinology 69 (1999) 63-76
64. VanderHorst V.G., and Holstege G. Caudal medullary pathways to lumbosacral motoneuronal cell groups in the cat: evidence for direct projections possibly representing the final common pathway for lordosis. J. Comp. Neurol. 359 (1995) 457-475
65. VanderHorst V.G., and Holstege G. A concept for the final common pathway of vocalization and lordosis behavior in the cat. Prog. Brain. Res. 107 (1996) 327-342
66. VanderHorst V.G., and Holstege G. Estrogen induces axonal outgrowth in the nucleus retroambiguus-lumbosacral motoneuronal pathway in the adult female cat. J. Neurosci. 17 (1997) 1122-1136
67. VanderHorst V.G., and Holstege G. Nucleus retroambiguus projections to lumbosacral motoneuronal cell groups in the male cat. J. Comp. Neurol. 382 (1997) 77-88
68. VanderHorst V.G., Mouton L.J., Blok B.F., and Holstege G. Distinct cell groups in the lumbosacral cord of the cat project to different areas in the periaqueductal gray. J. Comp. Neurol. 376 (1996) 361-385
69. VanderHorst V.G., Terasawa E., and Ralston III H.J. Monosynaptic projections from the nucleus retroambiguus region to laryngeal motoneurons in the rhesus monkey. Neuroscience 107 (2001) 117-125
70. VanderHorst V.G., Terasawa E., and Ralston III H.J. Axonal sprouting of a brainstem-spinal pathway after estrogen administration in the adult female rhesus monkey. J. Comp. Neurol. 454 (2002) 82-103
71. VanderHorst V.G., Terasawa E., and Ralston III H.J. Projections from estrogen receptor-alpha immunoreactive neurons in the periaqueductal gray to the lateral medulla oblongata in the rhesus monkey. Neuroscience 125 (2004) 243-253
72. Veening J.G., Swanson L.W., and Sawchenko P.E. The organization of projections from the central nucleus of the amygdala to brainstem sites involved in central autonomic regulation: a combined retrograde transport-immunohistochemical study. Brain. Res. 303 (1984) 337-357
73. Woolley C.S., and McEwen B.S. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J. Neurosci. 12 (1992) 2549-2554
74. Woolley C.S., and McEwen B.S. Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J. Comp. Neurol. 336 (1993) 293-306
75. Woolley C.S., Gould E., Frankfurt M., and McEwen B.S. Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J. Neurosci. 10 (1990) 4035-4039
76. Yuri K., and Kawata M. The effect of estrogen on the estrogen receptor-immunoreactive cells in the rat medial preoptic nucleus. Brain Res. 548 1-2 (1991) 50-54