Morphometrical and neurochemical changes in the anteroventral subdivision of the rat medial amygdala during estrous cycle

Brain Research

Volumn 1150, Issue 1, 2007, Pages 83-93

  Carrillo, Beatriz ^a   Pinos, Helena ^a   Guillamón, Antonio ^a   Panzica, GianCarlo ^b   Collado, Paloma ^a  

^a UNIVERSIDAD NACIONAL DE EDUCACIÓN A DISTANCIA   (Spain)

^b UNIVERSITY OF TURIN   (Italy)

Author keywords

Anteroventral subdivision of the medial amygdala; Estrous cycle; Nicotinamide adenine dinucleotide phosphate diaphorase; Nitric oxide synthase; Rat; Sexual diergism; Sexual dimorphism

Indexed keywords

BROXURIDINE; GLIAL FIBRILLARY ACIDIC PROTEIN; NEUROTRANSMITTER; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL SUBPOPULATION; CELL TYPE; CONTROLLED STUDY; ESTRUS CYCLE; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; MORPHOMETRICS; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; RAT; SEX DIFFERENCE; VOMERONASAL ORGAN;

AMYGDALA; ANIMALS; BRAIN CHEMISTRY; BROMODEOXYURIDINE; CELL COUNT; ESTROUS CYCLE; FEMALE; GLIAL FIBRILLARY ACIDIC PROTEIN; MALE; NADPH DEHYDROGENASE; NEURONS; NITRIC OXIDE SYNTHASE TYPE I; RATS; RATS, WISTAR; SEX CHARACTERISTICS;

RATTUS;

EID: 34248225480     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2007.02.073     Document Type: Article

References (74)

1. Abercrombie M. Estimation of nuclear population from microtome sections. Anat. Rec. 94 (1946) 239-247
2. Achtstätter T.R., Moll A., Anderson C., Kuhn S., Pitz K., Schwechheimer, and Franke W.W. Expression of glial filament protein (GFP) in nerve sheaths and nonneuronal cells reexamined using monoclonal antibodies, with special emphasis on the coexpression of GFP and cytokeratins in epithelial cells of human salivary gland and leomorphic adenomas. Differentiation 31 (1986) 206-227
3. Benelli A., Bertolini A., Poggioli R., Cavazzuti E., Calza L., Giardino L., and Arletti R. Nitric oxide is involved in male sexual behaviour of rats. Eur. J. Pharmacol. 294 (1995) 505-510
4. Britto J., Tannahill D., and Keynes R. A critical role for sonic hedgehog signaling in the early expansion of the developing brain. Nature Neurosci. 5 2 (2002) 103-110
5. Canteras N.S., and Swanson L.W. Projections of the ventral subiculum to the amygdala, septum, and hypothalamus: a PHAL anterograde tract-tracing study in the rat. J. Comp. Neurol. 324 (1992) 180-194
6. Canteras N.S., Simerly R.B., and 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
7. Ceccatelli S., Grandison L., Scott R.E.M., Pfaff D.W., and Kow L.M. Estradiol regulation of nitric oxide synthase mRNAs in rat hypothalamus. Neuroendocrinology 64 (1996) 357-363
8. Chu H.P., Morales J.C., and Etgen A.M. Cyclic GMP may potentiate lordosis behaviour by progesterone receptor activation. J. Neuroendocrinol. 11 (1999) 107-113
9. Collado P., Guillamón A., Pinos H., Pérez-Izquierdo M.A., García-Falgueras A., Carrillo B., Rodríguez C., and Panzica G.C. NADPH-diaphorase activity increases during estrous phase in the bed nucleus of the accessory olfactory tract in the female rat. Brain Res. 983 (2003) 223-229
10. Cooke B.M. Steroid-dependent plasticity in the medial amygdala. Neuroscience 138 (2006) 997-1005
11. Cooke B.M., and Woolley C.S. Sexually dimorphic synaptic organization of the medial amygdala. J. Neurosci. 25 (2005) 10759-10767
12. Cooke B.M., Tabibnia G., and Breedlove S.M. A brain sexual dimorphism controlled by adult circulating androgens. Proc. Natl. Acad. Sci. 96 (1999) 7538-7540
13. Debus E., Weber K., and Osborn M. Monoclonal antibodies specific for glial fibrillary acidic (GFA) protein and for each of the neurofilament triplet polypeptides. Differentiation 25 (1983) 193-203
14. De Olmos J.S., Alheid G.F., and Beltramino C.A. Amygdala. In: Paxinos G. (Ed). Forebrain and Midbrain. The Rat Nervous System vol. 1 (1985), Academic Press, Australia 223-334
15. De Olmos J.S., Beltramino C.A., and Alheid G.F. Amygdala and extended amygdala of the rat: a cytoarchitectonical, fibroarchitectonical and chemoarchitectonical survey. In: Paxinos G. (Ed). The Rat Nervous System (2004), Academic Press 509-603
16. De Vries G.J., and Simerly R.B. Anatomy, development and function of sexually dimorphic neural circuits in the mammalian brain. In: Paff D.W., Arnold A.P., Etgen A.M., Fahrbach S.E., and Rubin R.T. (Eds). Hormones, Brain and Behavior (2002), Academic Press 137-192
17. Fleming A.S., Vaccarino F., and Luebke C. Amygdaloid inhibition of maternal behavior in the nulliparous female rat. Physiol. Behav. 25 (1980) 731-743
18. Fleming A.S., Miceli M., and Moretto D. Lesions of the medial preoptic area prevent the facilitation of maternal behavior produced by amygdala lesions. Physiol. Behav. 31 (1983) 503-510
19. Fowler C.D., Freeman M.E., and Wang Z. Newly proliferated cells in the adult male amygdala are affected by gonadal steroid hormones. J. Neurobiol. 57 (2003) 257-269
20. Gahr M. How should brain nuclei be delineated? Consequences for developmental mechanism and for correlations of area size, neuron numbers and functions of brain nuclei. Trends Neurosci. 20 (1997) 58-62
21. González-Flores O., and Etgen A.M. The nitric oxide pathway participates in estrous behavior induced by progesterone and some of its ring A-reduced metabolites. Horm. Behav. 45 (2004) 50-57
22. Gotti S., Chiavegatto S., Sica M., Viglietti-Panzica C., Nelson R.J., and Panzica G.C. Alteration of NO-producing system in the basal forebrain and hypothalamus of Ts65Dn mice: an immunohistochemical and histochemical study of a murine model for Down syndrome. Neurobiol. Dis. 16 (2004) 563-571
23. Gotti S., Sica M., Viglietti-Panzica C., and Panzica G.C. Distribution of nitric oxide synthase immunoreactivity in the mouse brain. Microsc. Res. Tech. 68 (2005) 13-35
24. Gratzner H.G. Monoclonal antibody to 5-bromo- and 5-iododeoxyuridine: a new reagent for detection of DNA replication. Science 218 (1982) 474-475
25. Guillamón A., and Segovia S. Sexual dimorphism in the CNS and the role of steroids. In: Stone T.W. (Ed). CNS Neurotransmitters and Neuromodulators: Neuroactive Steroids (1996), CRC Press, Florida 127-152
26. Gundersen H.J.G., and Jensen E.B. The efficiency of systematic sampling in stereology and its prediction. J. Microsc. 147 (1987) 229-263
27. Gundersen H.J.G., Bagger P., Bendtsen T.F., Evans S.M., Korbo L., Marcussen N., Moller A., Nielsen K., Nyengaard J.R., Pakkenberg B., Sorensen F.B., Vesterby A., and West M.J. The new stereologicals tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS 96 (1988) 857-881
28. Gundersen H.J.G., Bendtsen T.F., Korbo L., Marcussen N., Moller A., Nielsen K., Nyengaard J.R., Pakkenberg B., Sorensen F.B., Vesterby A., and West M.J. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 96 (1988) 379-394
29. Halpern M., and Martínez-Marcos A. Structure and function of the vomeronasal system: an update. Prog. Neurobiol. 70 (2003) 245-318
30. Hines M., Allen L.S., and Gorski R.A. Sex differences in subregions of the medial nucleus of the amygdala and the bed nucleus of the stria teminalis of the rat. Brain Res. 579 (1992) 321-326
31. Kawata M. Roles of steroid hormones and their receptors in structural organization in the nervous system. Neurosci. Res. 24 (1995) 1-46
32. Kerchner M., Malsbury C.W., Ward O.B., and Ward I.L. Sexually dimorphic areas in the rat medial amygdala: resistance to the demasculinizing effect of prenatal stress. Brain Res. 672 (1995) 251-260
33. Kinsley C.H., Trainer R., Stafisso-Sandoz G., Quadros P., Marcus L.K., Hearon C., Meyer E.A.A., Hester N., Morgan M., Kozub F.J., and Lambert K.G. Motherhood and the hormones of pregnancy modify concentrations of hippocampal neuronal dendritc spines. Horm. Behav. 49 (2006) 131-142
34. Königsmark B.W. Methods for the counting of neurons. In: Nauta W.J.M., and Ebesson S.O.E. (Eds). Contemporary Research Methods in Neuroanatomy (1970), Springer, New York 315-340
35. Licht G., and Meredith M. Convergence of main and accessory olfactory pathways onto single neurons in the hamster amygdala. Exp. Brain Res. 69 (1987) 7-18
36. Madeira M.D., Ferreira-Silva L., and Paula-Barbosa M.M. Influence of sex and estrous cycle on the sexual dimorphisms of the hypothalamic ventromedial nucleus: stereological evaluation and golgi study. J. Comp. Neurol. 432 (2001) 329-345
37. Mani S.K., Allen J.M.C., Rettori V., McCann S.M., O'Malley B.W., and Clark J.H. Nitric oxide mediates sexual behavior in female rats. Proc. Natl. Acad. Sci. 91 (1994) 6468-6472
38. Martini M., Sica M., Eva C., Viglietti-Panzica C., and Panzica G.C. Dimorphism and effects of estrous cycle on the nitrergic system in mouse hypothalamus. Horm. Behav. 46 (2004) 95-96
39. McCarthy M.M., and Konkle A.T.M. When is a sex difference not a sex difference?. Front. Neuroendocrinol. 26 (2005) 85-102
40. McDonald A.J., Payne D.R., and Mascagni F. Identification of putative nitric oxide producing neurons in the rat amygdala using NADPH-diaphorase histochemistry. Neuroscience 52 (1993) 97-106
41. Meyer J.S., Nauert J., Koehm S., and Hughes J. Cell kinetics of human tumor by in vitro bromodeoxyuridine labeling. J. Histochem and Cytochem. 37 (1989) 1449-1454
42. Mizukami S., Nishizuka M., and Arai Y. Sexual difference in nuclear volume and its ontogeny in the rat amygdale. Exp. Neurol. 79 (1983) 569-575
43. Mizukawa K., Vincent S.R., McGreer P.L., and Mc Greer E.G. Distribution of reduced-nicotinamide-adenine-dinucleotide-phosphate diaphorase-positive cells and fibers in the cat central nervous system. J. Comp. Neurol. 279 (1989) 281-311
44. Naumann T., Kermer P., and Frotscher M. Fine structure of rat septohippocampal neurons: III. Recovery of choline acetyltransferase immunoreactivity after fimbria-fornix transaction. J. Comp. Neurol. 350 (1994) 161-170
45. Nishizuka M., and Arai Y. Sexual dimorphism in synaptic organization in the amygdala and its dependence on neonatal hormone environment. Brain Res. 212 (1981) 31-38
46. Nishizuka M., and Arai Y. Organizational action of estrogen on synaptic pattern in the amygdala: implications for sexual differentiation of the brain. Brain Res. 213 (1981) 422-426
47. Nishizuka M., and Arai Y. Male-female differences in the intra-amygdaloid input to the medial amygdale. Exp. Brain Res. 52 (1983) 328-332
48. Okamura H., Yokosuka M., and Hayashi S. Estrogenic induction of NADPH-diaphorase activity in the preoptic neurons containing estrogen receptor immunoreactivity in the female rat. J. Neuroendocrinol. 6 (1994) 597-601
49. Oro A.E., Simerly R.B., and Swanson L.W. Estrous cycle variations in levels of cholecystokinin immunoreactivity within cells of three interconnected sexually dimorphic forebrain nuclei. Evidence for a regulatory role for estrogen. Neuroendocrinology 47 (1988) 225-235
50. Panzica G.C., Arévalo R., Sánchez F., Alonso J.R., Aste N., Viglietti-Panzica C., Aijon J., and Vazquez R. Topographical distribution of reduced nicotinamide adenine dinucleotide phosphate-diaphorase in the brain of the Japanese quail. J. Comp. Neurol. 342 (1994) 97-114
51. Panzica G.C., Aste N., Viglietti-Panzica C., and Ottinger M.A. Structural sex differences in the brain: influence of gonadal steroids and behavioral correlates. J. Endocrinol. Invest. 18 (1995) 232-252
52. Panzica G.C., Verzè L., Viglietti-Panzica C., and Rissman E.F. Modifications of NOS-immunoreactive system in estrogen receptor alpha knock-out male mice. Abstr. - Soc. Neurosci. 26 (2000) 1275
53. Panzica G.C., Viglietti-Panzica C., Sica M., Gotti S., Martini M., Pinos H., Carrillo B., and Collado P. Effects of gonadal hormones on central nitric oxide producing systems. Neuroscience 138 (2006) 987-995
54. Paxinos G., and Watson Ch. The Rat Brain in Stereotaxic Coordinates (1998), Academic Press, Australia
55. Peters A., Palay S.L., and Webster F.H. The Fine Structure of the Nervous System (1991), Oxford Univ. Press
56. Pfaus J.G., Kleopoulos S.P., Mobbs C.V., Gibbs R.B., and Pfaff D.W. Sexual stimulation activates c-fos within estrogen concentrating regions of the female rat forebrain. Brain Res. 624 (1993) 253-267
57. Pow D.V. NADPH-diaphorase (nitric oxide synthase) staining in the rat supraoptic nucleus is activity dependent: possible functional implications. J. Neuroendocrinol. 4 (1992) 377-380
58. Rachman I.M., Unnerstall J.R., Pfaff D.W., and Cohen R.S. Regulation of neuronal nitric oxide synthase mRNA in lordosis-relevant neurons of the ventromedial hypothalamus following short-term estrogen treatment. Mol. Brain Res. 59 (1998) 105-108
59. Rakic P. Adult neurogenesis in mammals: an identity crisis. J. Neurosci. 22 (2002) 614-618
60. Rasia-Filho A.A., Xavier L.L., Dos Santos P., Huelen G., and Achaval M. Glial fibrillary acidic protein immunodetection and imunoreactivity in the anterior and posterior medial amygdala of male and female rats. Brain Res. Bull. 58 (2002) 67-75
61. Rasia-Filho A.A., Fabian C., Rigoti K.M., and Achaval M. Influence of sex, estrous cycle and motherhood on dendritic spine density in the rat medial amygdala revealed by the Golgi method. Neuroscience 126 (2004) 839-847
62. Roselli C.E., Ellinwood E.E., and Resko J.A. Regulation of brain aromatase activity in rats. Endocrinology 114 (1984) 192-200
63. 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
64. Sagar S.M., and Ferriero D. NADPH diaphorase activity in the posterior pituitary: relation to neuronal function. Brain Res. 400 (1987) 348-352
65. Scalia F., and Winans S.S. The differential projections of the olfactory bulb and accessory olfactory bulb in mammals. J. Comp. Neurol. 161 (1975) 31-56
66. Segovia S., and Guillamón A. Sexual dimorphism in the vomeronasal pathway and sex differences in reproductive behaviors. Brain Res. Rev. 18 (1993) 51-74
67. Sica M., Plumari L., Honda S., Harada N., Absil P., Viglietti Panzica C., Balthazart J., and Panzica G.C. Changes in the neuronal nitric oxide synthase immunoreactive system in male mice lacking a functional aromatase gene. Horm. Behav. 41 (2002) 490
68. Simerly R.B., Chang C., Muramatsu M., and 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
69. Sterio D.C. The unbiased estimation of number and sizes of arbitrary particles using the disector. J. Microsc. 134 (1984) 127-136
70. Tanapat P., Hastings N.B., Reeves A.J., and Gould E. Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J. Neurosci. 19 (1999) 5792-5801
71. Valero J., Weruaga E., Murias A.R., Recio J.S., and Alonso J.R. Proliferation markers in the adult rodent brain: bromodeoxyuridine and proliferating cell nuclear antigen. Brain Res. Brain Res. Protoc. 15 (2005) 127-134
72. Vincent S.R., and Kimura H. Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience 46 (1992) 755-784
73. Wolley C.S., and McEwen B.S. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult. J. Neurosci. 12 (1992) 2549-2554
74. Wolley C.S., Gould E., Frankfurt M., and McEwen B.S. Long-term and short-term electrophysiological effects of estrogen on the synaptic properties of hippocampal CA1 pyramidal neurons. J. Neurosci. 12 (1990) 3225-4035