Influence of sex, estrous cycle and motherhood on dendritic spine density in the rat medial amygdala revealed by the Golgi method

Neuroscience

Volumn 126, Issue 4, 2004, Pages 839-847

  Rasia Filho, A A ^a,b   Fabian, C ^b   Rigoti, K M ^c   Achaval, M ^c  

^a UNIVERSIDADE FEDERAL DE CIÊNCIAS DA SAÚDE DE PORTO ALEGRE   (Brazil)

^b UNIVERSIDADE DO VALE DO RIO DOS SINOS   (Brazil)

^c FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

Author keywords

amygdaloid complex; anteroventral periventricular nucleus of the hypothalamus; AVPV; ER ; ER ; estrogen receptor ; estrogen receptor ; Fos immunoreactivity; Fos ir; gonadal hormones; plasticity; pregnancy; sex steroids; sexual dimorphism

Indexed keywords

ANDROGEN RECEPTOR; ESTROGEN RECEPTOR;

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; BRAIN REGION; CELL DENSITY; CONTROLLED STUDY; DENDRITIC SPINE; DIESTRUS; ENDOCRINE FUNCTION; ESTRUS; ESTRUS CYCLE; FEMALE; GOLGI STAIN; MALE; METESTRUS; MOTHER; NONHUMAN; PRIORITY JOURNAL; PROESTRUS; PUERPERIUM; RAT; SEX DIFFERENCE; VEGETATION DYNAMICS;

AMYGDALA; ANALYSIS OF VARIANCE; ANIMALS; DENDRITES; ESTROUS CYCLE; FEMALE; MALE; NEURONS; PREGNANCY; RATS; RATS, WISTAR; SEX CHARACTERISTICS; SILVER STAINING;

EID: 2942659582     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2004.04.009     Document Type: Article

References (84)

1. Abe K. Modulation of hippocampal long-term potentiation by the amygdala A synaptic mechanism linking emotion and memory. Jpn J Pharmacol. 86:2001;18-22
2. Adamec R.E., Morgan H. The effect of kindling of different nuclei in the left and right amygdala on anxiety in the rat. Physiol Behav. 55:1994;1-12
3. ÅÅgmo A. Sexual motivation An inquiry into events determining the occurrence of sexual behavior. Behav Brain Res. 105:1999;129-150
4. Alheid GF, de Olmos J, Beltramino CA (1995) Amygdala and extended amygdala. In: The rat nervous system (Paxinos G, ed), pp 495-578. San Diego: Academic Press.
5. Bagga N., Chhina G.S., Mohan Kumar V., Singh B. Cholinergic activation of medial preoptic area by amygdala for ovulation in rat. Physiol Behav. 32:1984;45-48
6. Bolhuis J.J., Fitzgerald R.E., Dijk D.J., Koolhaas J.M. The corticomedial amygdala and learning in an agonistic situation in the rat. Physiol Behav. 32:1984;575-579
7. Bresnahan E., Routtenberg A. Memory disruption by unilateral low level, sub-seizure stimulation of the medial amygdaloid nucleus. Physiol Behav. 9:1972;513-525
8. Bressler S.C., Baum M.J. Sex comparison of neuronal Fos immunoreactivity in the rat vomeronasal projection circuit after chemosensory stimulation. Neuroscience. 71:1996;1063-1072
9. Canteras N.S., Chiavegatto S., Ribeiro do Valle L.E., Swanson L.W. Severe reduction of rat defensive behavior to a predator by discrete hypothalamic chemical lesions. Brain Res Bull. 44:1997;297-305
10. Canteras N.S., Simerly R.B., Swanson L.W. Organization of projections from the medial nucleus of the amygdala A phal study in the rat. J Comp Neurol. 360:1995;213-245
11. Calizo L.H., Flanagan-Cato L.M. Estrogen selectively regulates spine density within the dendritic arbor of rat ventromedial hypothalamic neurons. J Neurosci. 20:2000;1589-1596
12. Carrillo A.J., Rabii J., Carrer H.F., Sawyer C.H. Modulation of the proestrus surge of luteinizing hormone by electrochemical stimulation of the amygdala and hippocampus in the unanesthetized rat. Brain Res. 128:1977;81-92
13. Coopersmith C., Gans S.E., Rowe D.W., Erskine M.S. Infusions of lidocaine into the amygdala, but not the preoptic area, block pseudopregnancy in the rat. J Neuroendocrinol. 8:1996;259-266
14. Cooke B.M., Breedlove S.M., Jordan C.L. Both estrogen receptors and androgen receptors contribute to testosterone-induced changes in the morphology of the medial amygdala and sexual arousal in male rats. Horm Behav. 43:2003;336-346
15. Coolen L.M., Peters H.J.P.W., Veening J.G. Distribution of Fos immunoreactivity following mating versus anogenital investigation in the male rat brain. Neuroscience. 77:1997;1151-1161
16. Dayas C.V., Buller K.M., Day T.A. Neuroendocrine responses to an emotional stressor Evidence for involvement of the medial but not the central amygdala. Eur J Neurosci. 11:1999;2312-2322
17. De Jonge F.H., Oldenburger W.P., Louwerse A.L., Van de Poll N.E. Changes in male copulatory behavior after sexual exciting stimuli Effects of medial amygdala lesions. Physiol Behav. 52:1992;327-332
18. de Olmos J.S., Alheid G.F., Beltramino C.A. Amygdala. Paxinos G. The rat nervous system. 1985;223-334 Academic Press, Sydney
19. de Olmos J.S., Heimer L. The concepts of the ventral striatopallidal system and extended amygdala. Ann NY Acad Sci. 877:1999;1-32
20. Dielenberg R.A., Hunt G.E., McGregor I.S. When a rat smells a cat The distribution of fos immunoreactivity in rat brain following exposure to a predatory odor. Neuroscience. 104:2001;1085-1097
21. Dominguez J.M., Hull E.M. Stimulation of the medial amygdala enhances medial preoptic dopamine release Implications for male rat sexual behavior. Brain Res. 917:2001;225-229
22. Etgen A.M., Chu H.-P., Fiber J.M., Karkanias G.B., Morales J.M. Hormonal integration of neurochemical and sensory signals governing female reproductive behavior. Behav Brain Res. 105:1999;93-103
23. Federico P., Veale W.L., Pittman Q.J. Vasopressin-induced antipyresis in the medial amygdaloid nucleus of conscious rats. Am J Physiol. 262:1992;R901-R908
24. Feldman S., Conforti N., Saphier D. The preoptic area and bed nucleus of the stria terminalis are involved in the effects of the amygdala on adrenocortical secretion. Neuroscience. 37:1990;775-779
25. Ferguson J.N., Aldag J.M., Insel T.R., Young L.J. Oxytocin in the medial amygdala is essential for social recognition in the mouse. J Neurosci. 21:2001;8278-8285
26. Fleming A.S., Vaccarino F., Luebke C. Amygdaloid inhibition of maternal behavior in the nulliparous female rat. Physiol Behav. 25:1980;731-743
27. Frankfurt M., Gould E., Woolley C.S., 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
28. Giovenardi, M, Frey, RM, Azevedo, MS, Franci, CR, Lucion, AB (2002) Perfil hormonal de ratas lactantes [abstract]. Annals of the XVII Annual Meeting of FESBE; Salvador, Brazil.
29. Gomez D.M., Newman S.W. Medial nucleus of the amygdala in the adult Syrian hamster A quantitative golgi analysis of gonadal hormonal regulation of neuronal morphology. Anat Rec. 231:1991;498-509
30. Gréco B., Edwards D.A., Michael R.P., Clancy N.A. Androgen receptors and estrogen receptors are colocalized in male rat hypothalamic and limbic neurons that express Fos immunoreactivity induced by mating. Neuroendocrinology. 67:1998;18-28
31. Guillamón A., Segovia S. Sex differences in the vomeronasal system. Brain Res Bull. 44:1997;377-382
32. Huddleston G.G., Michael R.P., Zumpe D., Clancy A.N. Estradiol in the male rat amygdala facilitates mounting but not ejaculation. Physiol Behav. 79:2003;239-246
33. Ichikawa M. Synaptic reorganization in the medial amygdaloid nucleus after lesion of the accessory olfactory bulb of adult rat Ii. new synapse formation in the medial amygdaloid nucleus by fibers from the bed nucleus of the stria terminalis. Brain Res. 420:1987;253-258
34. Ikegaya Y., Abe K., Saito H., Nishiyama N. Medial amygdala enhances synaptic transmission and synaptic plasticity in the dentate gyrus of rats in vivo. J Neurophysiol. 74:1995;2201-2203
35. Insel T.R. Regional induction of c-fos-like protein in rat brain after estradiol administration. Endocrinology. 126:1990;1849-1853
36. Kalra P.S., McCann S.M. The stimulatory effect on gonadotropin release of implants of estradiol or progesterone in certain sites in the central nervous system. Neuroendocrinology. 19:1975;289-302
37. Kinsley C.H., Madonia L., Gifford G.W., Tureski K., Griffin G.R., Lowry C., Williams J., Collins J., McLearie H., Lambert K.G. Motherhood improves learning and memory. Nature. 402:1999;137-138
38. Kondo Y. Lesions of the medial amygdala produce severe impairment of copulatory behavior in sexually inexperienced male rats. Physiol Behav. 51:1992;939-943
39. Kondo Y., Sachs B.D., Sakuma Y. Importance of the medial amygdala in rat penile erection evoked by remote stimuli from estrous females. Behav Brain Res. 91:1998;215-222
40. Li X., Schwartz P.E., Rissman E.F. Distribution of estrogen receptor-β-like immunoreactivity in rat forebrain. Neuroendocrinology. 66:1997;63-67
41. Lonstein J.S., Gréco B., De Vries G.J., Stern J.M., Blaustein J.D. Maternal behavior stimulates c-fos activity within estrogen receptor alpha-containing receptors in lactating rats. Neuroendocrinology. 72:2000;91-101
42. Malsbury C.W., McKay K. Neurotrophic effects of testosterone on the medial nucleus of the amygdala in adult male rats. J Neuroendocrinol. 6:1994;57-69
43. Mascó D.H., Carrer H.F. Sexual receptivity in female rats after lesion or stimulation in different amygdaloid nuclei. Physiol Behav. 24:1980;1073-1080
44. McDonald A.J. Cortical pathways to the mammalian amygdala. Prog Neurobiol. 55:1998;257-332
45. McDonald A.J. Cell types and intrinsic connections of the amygdala. Aggleton J.P. The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction. 1992;67-96 Wiley-Liss, New York
46. Meisel R.L., Sachs B.D. The physiology of male sexual behavior. Knobil E., Neil J.D. The physiology of reproduction. 1994;3-105 Raven Press, New York
47. Micevych P.E., Matt D.W., Go V.L.W. Concentrations of cholecystokinin, substance P, and bombesin in discrete regions of male and female rat brain Sex differences and estrogen effects. Exp Neurol. 110:1988;416-425
48. Mizukami S., Nishizuka M., Arai Y. Sexual difference in nuclear volume and its ontogeny in the rat amygdala. Exp Neurol. 79:1983;569-575
49. Morgan H.D., Watchus J.A., Milgram N.W., Fleming A.S. The long lasting effects of electrical stimulation of the medial preoptic area and medial amygdala on maternal behavior in female rats. Behav Brain Res. 99:1999;61-73
50. Nabekura J., Oomura Y., Minami T., Mizuno Y., Fukuda A. Mechanism of the rapid effect of 17α-estradiol on medial amygdala neurons. Science. 233:1986;226-228
51. Narkiewicz O., Juraniec J., Wrzolkowa T. The distribution of axon terminals with flattened vesicles in the nuclei of the amygdaloid body of the cat. J Hirnforsch. 19:1972;133-143
52. Nelson R.J. Parental behavior. Nelson R.J. An introduction to behavioral endocrinology. 1995;289-336 Sinauer Associates, Sunderland
53. Newman S.W. The medial extended amygdala in male reproductive behavior A node in the mammalian social behavior network. Ann NY Acad Sci. 877:1999;242-257
54. Nimchinsky E.A., Sabatini B.L., Svoboda K. Structure and function of dendritic spines. Annu Rev Physiol. 64:2002;313-353
55. Nishizuka M., Arai Y. Male-female differences in the intra-amygdaloid input to the medial amygdala. Exp Brain Res. 52:1983;328-332
56. Oro A.E., Simerly R.B., Swanson L.W. Estrous cycle variations in levels of cholecystokinin immunoreactivity within cells of three interconnected sexually dimorphic forebrain nuclei. Neuroendocrinology. 47:1988;225-235
57. Österlund M., Kuiper G.G.J.M., Gustafsson J.-A., Hurd Y.L. Differential distribution and regulation of estrogen receptor-α and -β mRNA within the female rat brain. Mol Brain Res. 54:1998;175-180
58. Paxinos G., Watson C. The rat brain in stereotaxic coordinates. 1998;Academic Press, San Diego
59. Petrovich G.D., Canteras N.S., Swanson L.W. Combinatorial amygdalar inputs to hippocampal domains and hypothalamic behavior systems. Brain Res Rev. 38:2001;247-289
60. Pfaus J.G., Heeb M.M. Implications of immediate-early gene induction in the brain following sexual stimulation of female and male rodents. Brain Res Bull. 44:1997;397-407
61. Pitkänen A. Connectivity of the rat amygdaloid complex. Aggleton J.P. The amygdala: a functional analysis. 2000;31-115 Oxford University Press, Oxford
62. Rajendren G., Dudley C.A., Moss R.L. Influence of male rats on the luteinizing hormone-releasing hormone neuronal system in female rats Role of the vomeronasal organ. Neuroendocrinology. 57:1993;898-906
63. Rasia-Filho A.A., Londero R.G., Achaval M. On some functional activities of the amygdala An overview. J Psychiatry Neurosci. 25:2000;14-23
64. Rasia-Filho A.A., Londero R.G., Achaval M. Effects of gonadal hormones on the morphology of neurons from the medial amygdaloid nucleus of rats. Brain Res Bull. 48:1999;173-183
65. Rasia-Filho A.A., Peres T.M.S., Cubilla-Gutierrez F.H., Lucion A.B. Effect of estradiol implanted in the corticomedial amygdala on the sexual behavior of castrated male rats. Braz J Med Biol Res. 24:1991;1041-1049
66. Rasia-Filho A.A., Xavier L.L., Santos P., Gehlen P., Achaval M. Glial fibrillary acidic protein immunodetection and immunoreactivity in the anterior and in the posterior medial amygdala of male and female rats. Brain Res Bull. 58:2002;67-75
67. Roozendaal B., McGaugh J.L. Amygdaloid nuclei lesions differentially affect glucocorticoid-induced memory enhancement in an inhibitory avoidance task. Neurobiol Learn Mem. 65:1996;1-8
68. Rowe D.W., Erskine M.S. c-Fos proto-oncogene activity induced by mating in the preoptic area, hypothalamus and amygdala in the female rat Role of afferent input via the pelvic nerve. Brain Res. 621:1993;25-34
69. Schiess M.C., Joëls M., Shinnick-Gallagher P. Estrogen priming affects active membrane properties of medial amygdala neurons. Brain Res. 440:1988;380-385
70. Sheehan T.P., Cirrito J., Numan M.J., Numan M. Using c-fos immunohistochemistry to identify forebrain regions that may inhibit maternal behavior in rats. Behav Neurosci. 114:2000;337-352
71. Sheehan T.P., Paul M., Amaral E., Numan M.J., Numan M. Evidence that the medial amygdala projects to the anterior/ventromedial hypothalamic nuclei to inhibit maternal behavior in rats. Neuroscience. 106:2001;341-356
72. Shepherd G.M. The dendritic spine A multifunctional integrative unit. J Neurophysiol. 75:1996;2197-2210
73. Shughrue P.J., Lane M.V., Merchenthaler I.J. Comparative distribution of estrogen receptor-α and -β mRNA in the rat central nervous system. Comp Neurol. 388:1997;507-525
74. Simerly R.B. Organization and regulation of sexually dimorphic neuroendocrine pathways. Behav Brain Res. 92:1998;195-203
75. Simerly R.B., Chang C., Muramatsu M., Swanson L.W. Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain An in situ hybridization study. J Comp Neurol. 294:1990;76-95
76. Smock T., Arnold S., Albeck D., Emerson P., Garritano J., Burrows K., Derber W., Sanon C., Marrs K., Wearthearly H., Kruse K. A peptidergic circuit for reproductive behavior. Brain Res. 598:1992;138-142
77. Stark C.P., Alpern H.P., Fuhrer J., Trowbridge M.G., Wimbish H., Smock T. The medial amygdaloid nucleus modifies social behavior in male rats. Physiol Behav. 63:1998;253-259
78. Swanson L.W., Petrovich G.D. What is the amygdala? Trends Neurosci. 21:1998;323-331
79. Vochteloo J.D., Koolhaas J.M. Medial amygdala lesions in male rats reduce aggressive behavior Interference with experience. Physiol Behav. 41:1987;99-102
80. Yoshida M., Suga S., Sakuma Y. Estrogen reduces the excitability of the female rat medial amygdala afferents from the medial preoptic area but not those from the lateral septum. Exp Brain Res. 101:1994;1-7
81. A, NMDA and muscarinic receptors in induction of long-term potentiation in the medial and lateral amygdala in vitro. Neurosci Res. 21:1995;317-322
82. Wood R.I., Coolen L.M. Integration of chemosensory and hormonal cues is essential for sexual behaviour in male Syrian hamster Role of the medial amygdaloid nucleus. Neuroscience. 78:1997;1027-1035
83. Woolley C.S., Gould E., Frankfurt M., McEwen B.S. Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J Neurosci. 10:1990;4035-4039
84. Zar J.H. Biostatistical analysis. 1999;Prentice Hall, Upper Saddle River, NJ