Morphological and functional features of the sex steroid-responsive posterodorsal medial amygdala of adult rats

Mini-Reviews in Medicinal Chemistry

Volumn 12, Issue 11, 2012, Pages 1090-1106

  Rasia Filho, A A ^a,b   Haas, D ^a   de Oliveira, A P ^b   de Castilhos, J ^b   Frey, R ^b   Stein, D ^b   Lazzari, V M ^a   Back, F ^a   Pires, G N ^a   Pavesi, E ^c   Winkelmann Duarte, E C ^c   Giovenardi, M ^a,b  

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

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

^c FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

Author keywords

Anxiety; Extended amygdala; Fos immunoreacitivity; Ibotenic acid; Innate fear; Neuronal morphology; Sexual behavior; Sexual dimorphism

Indexed keywords

GLUTAMIC ACID; HISTAMINE; SEX HORMONE;

ARTICLE; BRAIN DAMAGE; BRAIN FUNCTION; IMMOBILIZATION STRESS; IMMUNOREACTIVITY; MAZE TEST; MEDIAL AMYGDALA; MORPHOLOGY; NONHUMAN; RAT; SEX DIFFERENCE; SEXUAL BEHAVIOR; SOCIAL BEHAVIOR;

AGGRESSION; AMYGDALA; ANIMALS; FEAR; FEMALE; GONADAL STEROID HORMONES; MALE; RATS; SEXUAL BEHAVIOR, ANIMAL;

EID: 84864939638     PISSN: 13895575     EISSN: 18755607     Source Type: Journal    
DOI: 10.2174/138955712802762211     Document Type: Article

References (201)

1. Nelson, R.J. An Introduction to Behavioral Endocrinology; Sinauer Associates: Sunderland, 2000.
2. Rasia-Filho, A.A.; Brusco, J.; Moreira, J.E. Spine plasticity in the rat medial amygdala. In: Dendritic Spines: Biochemistry, Modeling and Properties, Baylog, L.R. Ed.; Nova Science Publishers: Hauppauge, 2009; pp. 67-90.
3. Swanson, L. W.; Petrovich, G. D. What is the amygdala? Trends. Neurosci.,1998, 21, 323-331.
4. Alheid, G. F.; de Olmos, J. S.; Beltramino, C. A. Amygdala and extended amygdala.Paxinos, G., editor. 1995; pp. 495-578.
5. McDonald, A.J. Cortical pathways to the mammalian amygdala. Prog. Neurobiol.,1998, 55, 257-332.
6. Pitkänen, A. Connectivity of the rat amygdaloid complex. In: The amygdala: a functional analysis, Aggleton, J.P. Ed.; Oxford University Press: Oxford, 2000; pp 31-115.
7. Petrovich, G.D.; Canteras, N.S.; Swanson, L.W. Combinatorial amygdalar inputs to hippocampal domains and hypothalamic behavior systems. Brain Res. Rev., 2001, 38, 247-289.
8. de Olmos, J.S.; Beltramino, C.A.; Alheid, G. Amygdala and extended amygdala of the rat: a cytoarchitectonical, fibroarchitectonical, and chemoarchitectonical survey. Paxinos, G., editor; 2004: pp. 509-603.
9. Newman, S. W. The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network. Ann. NY Acad. Sci., 1999, 877, 242-257.
10. Alheid, G.F. Extended amygdala and basal forebrain. Ann. N.Y. Acad. Sci, 2003 985, 185-205.
11. Swanson, L.W. The amygdala and its place in the cerebral hemisphere. Ann. N.Y. Acad. Sci., 2003, 985, 174-184.
12. Bian, X.; Yanagawa, Y.; Chen, W.R.; Luo, M. Cortical-like functional organization of the pheromone-processing circuits in the medial amygdala. J. Neurophysiol.,2008, 99, 77-86.
13. García-López, M.; Abellán, A.; Legaz, I.; Rubenstein, J.L.R.; Puelles, L.; Medina, L. Histogenetic compartments of the Mouse centromedial and extended amygdala base on gene expression patterns during development. J. Comp. Neurol., 2008, 506, 46-74.
14. Bupesh, M.; Legaz, I.; Abellán, A.; Medina, L. Multiple telencephalic and extratelencephalic embryonic domains contribute neurons to the medial extended amygdala. J. Comp. Neurol., 2011, 519, 1505-1525.
15. 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., 1995, 360, 213-245.
16. Carrillo, B.; Pinos, H.; Guillamón, A.; Panzica, G.; Collado, P. Morphometrical and neurochemical changes in the anteroventral subdivision of the rat medial amygdala during estrous cycle. Brain. Res., 2007, 1150, 83-93.
17. Dall'Oglio, A.; Gehlen, G.; Achaval, M.; Rasia-Filho, A.A. Dendritic branching features of posterodorsal medial amygdala neurons of adult male and female rats: Further data based on the Golgi method. Neurosci. Lett., 2008, 430, 151-156.
18. Dall'Oglio, A.; Gehlen, G.; Achaval, M.; Rasia-Filho, A.A. Dendritic branching features of Golgi-impregnated neurons from the ventral medial amygdala subnuclei of adult male and female rats. Neurosci Lett., 2008, 439, 287-292.
19. Scalia, F.; Winans, S.S. The differential projections of the olfactory bulb and accessory olfactory bulb in mammals. J. Comp. Neurol., 1975, 161, 31-55.
20. Nishizuka, M.; Arai, Y. Male-female differences in the intraamygdaloid input to the medial amygdala. Exp. Brain Res.,1983, 52, 328-332.
21. Dielenberg, R.A.; McGregor, I.S. Defensive behavior in rats towards predatory odors: a review. Neurosci. Biobehav. Rev., 2001, 25, 597-609.
22. Meredith, M.; Westberry, J.M. Distinctive responses in the medial amygdala to same-species and different-species pheromones. J. Neurosci., 2004, 24, 5719-5725.
23. Pro-Sistiaga, P.; Mohedano-Moriano, A.; Ubeda-Bañon, I.; Arroio-Jimenez, M.D.M.; Marcos, P.; Artacho-Pérula, E.; Crespo, C.; Insausti, R.; Martinez-Marcos, A. Convergence of olfactory and vomeronasal projections in the rat basal telencephalon. J. Comp. Neurol., 2007, 504, 346-362.
24. Blake, C.B.; Meredith, M. Change in number and activation of androgen receptor-immunoreactive cells in the medial amygdala in response to chemosensory input. Neuroscience, 2011, 190, 228-238.
25. Dhungel, S.; Urakawa, S.; Kondo, Y.; Sakuma, Y. Olfactory preference in the male rat depends on multiple chemosensory inputs converging on the preoptic area. Horm. Behav., 2011, 59, 193-199.
26. 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.,1991, 24, 1041-1049.
27. 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, 1997, 77, 1151-1161.
28. Coolen, L.M.; Peters, H.J.P.W.; Veening, J.G. Fos immunoreactivity in the rat brain following consummatory elements of sexual behavior: a sex comparison. Brain. Res.,1996, 738, 67-82.
29. 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., 1997, 44, 397-407.
30. de Castilhos, J.; Marcuzzo, S.; Forti, C.D.; Frey, R.M.; Stein, D.; Achaval, M.; Rasia-Filho, A.A. Further studies on the rat posterodorsal medial amygdala: Dendritic spine density and effect of 8-OH-DPAT microinjection on male sexual behavior. Brain Res. Bull., 2006, 69, 131-139.
31. Cameron, N.M.; Carey, P.; Erskine, M.S. Medullary noradrenergic neurons release norepinephrine in the medial amygdala in females in response to mating stimulation sufficient for pseudopregnancy. Brain. Res., 2004, 1022, 137-147.
32. Fleming, A.S.; Vaccarino, F.; Luebke, C. Amygdaloid inhibition of maternal behavior in the nulliparous female rat. Physiol. Behav.,1980, 25, 731-743.
33. 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, 2001, 106, 341-356.
34. Adamec, R. E.; Morgan, H. D. The effect of kindling of different nuclei in the left and right amygdala on anxiety in the rat. Physio.l Behav., 1994, 55, 1-12.
35. Duncan, G. E.; Knapp, D. J.; Breese, G. R. Neuroanatomical characterization of Fos induction in rat behavioral models of anxiety. Brain. Res.,1996, 713, 79-91.
36. Dayas, C.V.; Buller, K.M.; Day, T.A. Neuroendocrine responses to an emotional stressor: evidence for the involvement of the medial but not the central amygdala. Eur. J. Neurosci., 1999, 11, 2312-2322.
37. Marcuzzo, S.; Dall'Oglio, A.; Ribeiro, M.F.; Achaval, M.; Rasia-Filho, A.A. Dendritic spines in the posterodorsal medial amygdala after restraint stress and ageing in rats. Neurosci. Lett., 2007, 424, 16-21.
38. Lin, Y.; Li, X.; Lupi, M.; Kinsey-Jones, J.S.; Shao, B.; Lightman, S.L.; O'Byrne, K.T. The role of the medial and central amygdala in stress-induced suppression of pulsatile LH secretion in female rats. Endocrinology, 2011, 152, 545-555.
39. Timmer, M.; Cordero, M.I.; Sevelinges, Y.; Sandi C. Evidence for a role of oxytocin receptors in the long-term establishment of dominance hierarchies. Neuropsychopharmacol, 2011, doi: 10.1038/npp.2011.125.
40. Rasia-Filho, A.A.; Fabian, C.; Rigoti, K.; Achaval., M. Influence of sex, estrous cycle and motherhood in dendritic spine density in the rat medial amygdala revealed by the Golgi method. Neuroscience, 2004, 126, 839-847.
41. Rasia-Filho, A. A. Is there anything autonomous in the nervous system? Adv. Physiol. Educ., 2006, 30, 9-12.
42. Rasia-Filho, A.A.; Giovenardi, M.; de Almeida, R.M. Drugs and aggression. Recent Patents CNS Drug Discov., 2008, 3, 40-49.
43. Mizukami, S.; Nishizuka, M.; Arai, Y. Sexual difference in nuclear volume and its ontogeny in the rat amygdala. Exp. Neurol., 1983, 79, 569-575.
44. Johnson, R.T.; Breedlove, S.M.; Jordan, C.L. Sex differences and laterality in astrocyte number and complexity in the adult rat medial amygdala. J. Comp. Neurol., 2008, 511, 599-609.
45. Martinez, F.G.; Hermel, E.E.; Xavier, L.L.; Viola, G.G.; Riboldi, J.; Rasia-Filho, A.A.; Achaval, M. Gonadal hormone regulation of glial fibrillary acidic protein immunoreactivity in the medial amygdala subnuclei across the estrous cycle and in castrated and treated female rats. Brain. Res., 2006, 1108, 117-126.
46. Morris, J.A.; Jordan, C.L.; Breedlove, S.M. Sexual dimorphism in neuronal number of the posterodorsal medial amygdala is independent of circulating androgens and regional volume in adult rats. J. Comp. Neurol., 2008, 506, 851-859.
47. Zhou, J.; Zhang, H.; Cohen, R.S.; Pandey, S.C. Effects of estrogen treatment on expression of BDNF and CREB expression and phosphorylation in rat amygdaloid and hippocampal structures. Neuroendocrinology, 2005, 81, 294-310.
48. 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.,1990, 294, 76-95.
49. Sheridan, P. J. The nucleus interstitialis stria terminalis and the nucleus amygdaloideus medialis: Prime targets for androgen in the rat forebrain. Endocrinology, 1979, 104, 130-136.
50. 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, 1998, 67, 18-28.
51. Blake, C.B.; Meredith, M. Change in number and activation of androgen receptor-immunoreactive cells in the medial amygdala in response to chemosensory input. Neuroscience, 2011, 190, 228-238.
52. Gréco, B.; Edwards, D.A.; Michael, R.P.; Clancy, A.N. Androgen receptor immunoreactivity and mating-induced Fos expression in forebrain and midbrain structures in the male rat. Neuroscience, 1996, 75, 161-171.
53. Wagner, C. K.; Morrell, J. I. Distribution and steroid hormone regulation of aromatase mRNA expression in the forebain of adult male and female rats: A cellular-level analysis using in situ hybridization. J. Comp. Neurol., 1996, 370, 71-84.
54. Roselli, C. E.; Horton, L. E.; Resko, J. A. Distribution and regulation of aromatase activity in the rat hypothalamus and limbic system. Endocrinology, 1985, 117, 2471-2477.
55. Shughrue, P.J.; Lane, M.V.; Merchenthaler, I.J. Comparative distribution of estrogen receptor-and - mRNA in the rat central nervous system. J. Comp. Neurol., 1997, 388, 507-525.
56. 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. Neuroendocrinol., 1998, 67, 18-28.
57. Gréco, B.; Allegretto, E.A.; Tetel, M.J.; Blaustein, J.D. Coexpression of ER with ER and progestin receptor proteins in the female rat forebrain: effects of estradiol treatment. Endocrinology, 2001, 142, 5172-5181.
58. Gréco, B.; Blasberg, M.E.; Kosinski, E.C.; Blaustein, J.D. Response of ER -IR and ER -IR cells in the forebrain of female rats to mating stimuli. Horm. Behav., 2003, 43, 444-453.
59. De Vries, G.J.; Simerly, R.B. Anatomy, development, and function of sexually dimorphic neural circuits in the mammalian brain. In: Hormones, Brain and Behavio, Pfaff, D,W.; Arnold, A.P.; Etgen, A.M.; Fahrbach, S.E.; Rubin, R,.T., Eds;. Academic Press, San Diego, 2002; pp. 137-191.
60. Isgor, C.; Huang, G.C.; Akil, H.; Watson, S.J. Correlation of estrogen -receptor messenger RNA with endogenous levels of plasma estradiol and progesterone in the female rat hypothalamus, the bed nucleus of stria terminalis and the medial amygdala. Mol. Brain Res., 2002, 106, 30-41.
61. Phillips-Farfán B.V.;Lemus, A. E.; Fernández-Guasti, E. Increased estrogen receptor alpha immunoreactivity in the forebrain of sexually satiated rats. Horm. Behav., 2007, 51, 328-334.
62. Hines, M.; Allen, L. S.; Gorski, R. A. Sex differences in subregions of the medial nucleus of the amygdala and the bed nucleus of the stria terminalis of the rat. Brain Res., 1992, 579, 321-326.
63. Hermel, E.E.; Ilha, J.; Xavier, L.L.; Rasia-Filho, A.A.; Achaval, M. Influence of sex and estrous cycle, but not laterality, on the neuronal somatic volume of the posterodorsal medial amygdala of rats. Neurosci. Lett., 2006, 405, 153-158.
64. Zehr, J.L.; Todd, B.J.; Schulz, K.M.; McCarthy, M.M.; Sisk, C.L. Dendritic pruning of the medial amygdala during pubertal development of the male Syrian hamster. J. Neurobiol., 2006, 66, 578-590.
65. de Castilhos, J.; Forti, C.D.; Achaval, M.; Rasia-Filho, A.A. Dendritic spine density of posterodorsal medial amygdala neurons can be affected by gonadectomy and sex steroid manipulations in adult rats: A Golgi study. Brain. Res., 2008, 1240, 73-81.
66. Nishizuka, M.; Arai, Y. Regional difference in sexually dimorphic synaptic organization of the medial amygdala. Exp. Brain Res.,1983, 49, 462-465.
67. Cooke, B.M.; Woolley, C.S. Sexually dimorphic synaptic organization of the medial amygdala. J. Neurosci., 2005, 25, 10759-10767.
68. Arimatsu, Y.; Seto, A.; Amano, T. Sexual dimorphism in bungarotoxin binding capacity in the mouse amygdala. Brain Res., 1981, 213, 432-437.
69. 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., 1988, 100, 416-425.
70. Oro, A.E.; Simerly, R.B.; Swanson, L.W. Estrous cycle variations in levels of cholecystokinin immunoreactivity within cells of three interconnectedsexuallydimorphicforebrainnuclei. Neuroendocrinology, 1988, 47, 225-235.
71. Wilson, M.A.; Mascagni, F.; McDonald, A.J. Sex differences in delta opioid receptor immunoreactivity in rat medial amygdala. Neurosci. Lett., 2002, 328, 160-164.
72. Stefanova, N. γ-Aminobutyric acid-immunoreactivity neurons in the amygdala of the rat - sex differences and effect of early postnatal castration. Neurosci. Lett., 1998, 255, 175-177.
73. Polston, E.K.; Heitz, M.; Barnes, W.; Cardamone, K.; Erskine, M.S. NMDA-mediated activation of the medial amygdala initiates a downstream neuroendocrine memory responsible for pseudopregnancy in the female rat. J. Neurosci., 2001, 21, 4104-4110.
74. Fergunson, 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., 2001, 21, 8278-8285.
75. Lehmann, M.L.; Erskine, M.S. Glutamatergic stimulation of the medial amygdala induces steroid dependent c-fos expression within forebrain nuclei responsive to mating stimulation. Neuroscience, 2005, 136, 55-64.
76. Malsbury, C.W.; McKay, K. Neurotrophic effects of testosterone on the medial nucleus of the amygdala in adult male rats. J. Neuroendocrinol., 1994, 6, 57-69.
77. 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., 2002, 58, 67-75.
78. 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., 1999, 48, 173-183.
79. McDonald, A.J. Cell types and intrinsic connections of the amygdala. In: The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction, Aggleton, J.P. Ed.; Wiley-Liss; NewYork; 1992; pp. 67-96.
80. Nabekura, J.; Oomura, Y.; Minami, T.; Mizuno, Y.; Fukuda, A. Mechanism of the rapid effect of 17a-estradiol on medial amygdala neurons. Science, 1986, 233, 226-228.
81. 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., 1991, 231, 498-509.
82. Choi, G.B.; Dong, H-W.; Murphy, A.J.; Valenzuela, D.M.; Yancopoulos, G.D.; Swanson, L.W.; Anderson, D.J. Lhx6 delineates a pathway mediating innate reproductive behaviors from the amygdala to the hypothalamus. Neuron, 2005, 46, 647-660.
83. Arpini, M.; Menezes, I.C.; Dall'Oglio, A.; Rasia-Filho, A.A. The density of Golgi-impregnated dendritic spines from adult rat posterodorsal medial amygdalaneurons displays no evidence of hemispheric or dorsal/ventral differences. Neurosci. Lett., 2010, 469, 209-213.
84. Brusco, J.; Dall'Oglio, A.; Rocha, L.B.; Rossi, M.A.; Moreira, J.E.; Rasia-Filho, A.A. Descriptive findings on the morphology of dendritic spines in the rat medial amygdala. Neurosci. Lett., 2010, 483, 152-156.
85. Carney, R.S.E.; Mangin, J-M.; Hayes, L.; Mansfield, K.; Sousa, V.H.; Fishell, G.; Machold, R.P.; Ahn, S.; Gallo, V.; Corbin, J.G. Sonic Hedgehog expressing and responding cells generate neuronal Diversity in the medial amygdala. Neural Develop., 2010, 5, 14.
86. Cunningham, R.L.; Clairborne, B.J.; McGinnis, M.Y. Pubertal exposure to anabolic androgenic steroids increases spine densities on neurons in the limbic system of male rats. Neuroscience, 2007, 150, 609-615.
87. Simerly, R.B. Anatomical substrates of hypothalamic integration. In: The Rat Nervous System. Paxinos, G., Ed.; Academic Press: San Diego; 2004; pp. 335-368.
88. Rasia-Filho, A.A.; Brusco, J.; Rocha, L.; Moreira, J. Dendritic spines observed by extracellular DiI dye and immunolabeling under confocal microscopy. Nature Protocols/Protocol Exchange (2010). doi:10.1038/nprot.2010.153.
89. Toni, N.; Buchs, P.A.; Nikonenko, I.; Bron, C.R.; Muller, D. LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature, 1999, 402, 421-425.
90. Shepherd, G.M. The dendritic spine: a multifunctional integrative unit. J. Neurophysiol., 1996, 75, 2197-2210.
91. Nimchinsky, E.A.; Sabatini, B.L.; Svoboda, K. Structure and function of dendritic spines. Annu. Rev. Physiol., 2002, 64, 313-353.
92. Kasai, H.; Matsuzaki, M.; Noguchi, J.; Yasumatsu, N.; Nakahara, H. Sructure-stability-function relationships of dendritic spines. Trends Neurosci., 2003, 26, 360-368.
93. Peters, A.; Palay, S.; Webster, H. The fine structure of the nervous system, Oxford University Press: New York, 1991.
94. Stuart, G.; Sprutson, N.; Häusser, M. Dendrites. Oxford University Press: New York, 1999.
95. Arellano, J.I.; Espinosa, A.; Fairén, A.; Yuste, R.; DeFelipe, J. Non-synaptic dendritic spines in neocortex. Neuroscience, 2007, 145, 464-469.
96. Harris, K.M.; Kater, S.B. Dendritic spines: Cellular specializations imparting both stability and flexibility to synaptic function. Ann. Rev. Neurosci., 1994, 17, 341-371.
97. Tsay, D.; Yuste, R. On the electrical function of dendritic spines. Trends Neurosci., 2004, 27, 77-83.
98. García-López, P.; García-Marin, V.; Freire M. Dendritic spines and development: towards a unifying model of spinogenesis. A present day review of Cajal's histological slides and drawings. Neural Plasticity, 2010, 2010:769207.
99. Peters, A.; Kaiserman-Abramof, I.R. The small pyramidal neuron of the rat cerebral cortex. The perikaryon, dendrites and spines. Am. J. Anat., 1970, 127, 321-356.
100. Cooke, B.M.; Stokas, M.R.; Woolley, C.S. Morphological sex differences and laterality in the prepubertal medial amygdala. J. Comp. Neurol., 2007, 501, 904-915.
101. Cooke, B.M. Synaptic reorganization of the medial amygdala during puberty. J. Neuroendocrinol., 2011, 23, 65-73.
102. Krebs-Kraft, D.L.; Hill, M.N.; Hillard, C.J.; McCarthy, M.M. Sex difference in cell proliferation in developing rat amygdala mediated by endocannabinoids has implications for social behavior. Proc. Natl. Acad. Sci., 2010, 107, 20535-20540.
103. Hermel, E.E.; Faccioni-Heuser, M.C.; Marcuzzo, S.; Rasia-Filho, A.A.; Achaval, M. Ultrastructural features of neurons and synaptic contacts in the posterodorsal medial amygdala of adult male rats. J. Anat., 2006, 208, 565-575.
104. Oberlander, J.G.; Erskine, M.S. Receipt of vaginal-cervical stimulation modifies synapsin content in limbic areas of the female rat. Neuroscience, 2008, 153, 581-593.
105. Rasia-Filho, A.A.; Lucion, A.B. Effects of 8-OH-DPAT on sexual behavior of male rats castrated at different ages. Horm. Behav., 1996, 30, 251-258.
106. Cooke, B.M.; Woolley, C.S. Effects of prepubertal gonadectomy on a male-typical behavior and excitatory synaptic transmission in the amygdala. Develop. Neurobiol., 2009, 69, 141-152.
107. Pereno, G.L.; Balaszczuk, V.; Beltramino, C.A. Detection of conspecific pheromones elicits fos expression in GABA and calcium-binding cells of the rat vomeronasal system-medial extended amygdala. J. Physiol. Biochem., 2011, 67, 71-85.
108. Dong, H.-W.; Petrovich, G.; Swanson, L.W. Topography of projections from amygdala to bed nuclei of the stria terminalis. Brain Res. Rev.,2001, 38, 192-246.
109. Shelley, D.N.; Meisel, R.L. The effects of mating stimulation on cfos immunoreactivity in the female hamster medial amygdala are region and context dependent. Horm. Behav.,2005, 47, 212-222.
110. Cavalcante, J.C.; Sita, L.V.; Mascaro, M.B.; Bittencourt, J.C.; Elias, C.F. Distribution of urocortin 3 neurons innervating the ventral premammillary nucleus in the rat brain. Brain Res., 2006, 1089, 116-125.
111. Polston, E.K.; Gu, G.; Simerly, R.B. Neurons in the principal nucleus of the bed nuclei of the stria terminalis provide a sexually dimorphic GABAergic input to the anteroventral periventricular nucleus of the hypothalamus. Neuroscience, 2004, 123, 793-803.
112. Dominguez, J.M.; Hull, E.M. Stimulation of the medial amygdala enhances medial preoptic dopamine release: Implications for male rat sexual behavior. Brain Res., 2001, 917, 225-229.
113. Toth, M.; Fuzesi, T.; Halász, J.; Tulodgi, A.; Haller, J. Neural inputs of the hypothalamic "aggression area" in the rat. Behav. Brain Res., 2010, 215, 7-20.
114. Been, L.E.; Petrulis, A. Chemosensory and hormone information are relayed directly between the medial amygdala, posterior bed nucleus of the stria terminalis, and medial preoptic area in male Syrian hamster. Horm. Behav., 2011, 59, 536-548.
115. Kim, J.; Semaan, S.J.; Clifton, D.K.; Steiner, R.A.; Dhamija, S.; Kauffman, A.S. Regulation of Kiss1 expression by sex steroids in the amygdala of the rat and mouse. Endocrinology, 2011, 152, 2020-2030.
116. Simmons, D.A.; Yahr, P. Nitric oxidergic cells related to ejacuilation in gerbil forebrain contain androgen receptor and respond to testosterone. J. Comp. Neurol., 2011, 519, 900-915.
117. Samuelsen, C.L.; Meredith, M. Oxytocin antagonist disrupts male mouse medial amygdala response to chemical-communication signals. Neuroscience, 2011, 180, 96-104.
118. Arakawa, H.; Arakawa, K.; Deak, T. Oxytocin and vasopressin in the medial amygdala differentially modulate approach and avoidance behavior toward illness-related social odor. Neuroscience, 2010, 171, 1141-1151.
119. Veyrac, A.; Wang, G.; Baum, M.J.; Bakker, J. The main and accessory olfactory systems of female mice are activated differentially by dominant versus subordinate male urinary odors. Brain Res., 2011, 1402, 20-29.
120. 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., 1992, 52, 327-332.
121. Stark, C.H. Behavioral effects of stimulation of the medial amygdala in the male rat are modified by prior sexual experience. J. Gen. Psychol., 2005, 132, 207-224.
122. Wood R Estradiol, but not dihydrotestosterone, in the medial amygdala facilitates male hamster sex behavior. Physiol. Behav., 1996, 59, 833-841.
123. Coolen, L.M.; Wood, R.I. Testosterone stimulation of the medial preoptic area and medial amygdala in the control of male hamster sexual behavior: redundancy without mplification. Behav. Brain Res., 1999, 98, 143-153.
124. 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., 1994, 101, 1-7.
125. 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, 1975, 19, 289-302.
126. Beltramino, C.; Taleisnik, S. Facilitatory and inhibitory effects of electrochemical stimulation of the amydala on the release of luteinizing hormone. Brain Res., 1978, 144, 95-107.
127. Gu, G.B.; Simerly, R.B. Projections of the sexually dimorphic anteroventral periventricular nucleus in the female rat. J. Comp. Neurol.,1997, 384, 142-164.
128. Carrer, H.F.; Whitmoyer, D.I.; Sawyer, C.H. Effects of hippocampal and amygdaloid stimulation on the firing of preoptic neurons in the proestrous female rat. Brain Res.,1978, 142, 363-367.
129. Bagga, N.; Chhina, G.S.; Kumar, V.M.; Singh, B. Cholinergic activation of medial preoptic area by amydala for ovulation in rat. Physiol. Behav.,1984, 32, 45-48.
130. Paterson, N.E.; Iwunze, M.; Davis, S.F.; Malekiani, S.A.; Hanania, T. Comparison of the predictive validity of the mirror chamber and elevated plus maze tests in mice. J. Neurosci. Methods, 2010, 188, 62-70.
131. Singh, K.; Bishnoi, M.; Kulkarni, S.K. Elevated zero-maze: a paradigm to evaluate anti-anxiety effects of drugs. Methods Find. Exp. Clin. Pharmacol., 2007, 29, 343-348.
132. Briones-Aranda, A.; López-Rubalcava, C.; Picazo, O. Influence of forced swimming-induced stress on the -like effect of 5-HT1A agents in mice. Psychopharmacol., 2002, 162, 147-155.
133. Brusco, J.; Wittmann, R.; de Azevedo, M.S.; Lucion, A.B.; Franci, C.R.; Giovenardi, M.; Rasia-Filho, A.A. Plasma hormonal profiles and dendritic spine density and morphology in the hippocampal CA1 stratum radiatum, evidenced by light microscopy, of virgin and postpartum female rats. Neurosci. Lett., 2008, 438, 346-350.
134. Erskine, M.S.; Lehmann, M.L.; Cameron, N.M.; Polston, E.K. Co-regulation of female sexual behavior and pregnancy induction: An exploratory synthesis. Behav. Brain Res., 2004, 153, 295-315.
135. Lehmann, M.L.; McKellar, H.; Erskine, M.S. Coding for the iniation of pseudopregnancy by temporally patterned activation of amygdalar NMDA receptors. J. Neurosci., 2005, 25, 8696-8703.
136. Rosa, C.B.; Goularte, J.F.; Trindade, N.A.; de Oliveira, A.P.; Rasia-Filho, A.A. Glutamate microinjected in the posterodorsal medial amydala induces subtle increase in the consumption of a three-choice macronutrient self-selection diet in male rats. Anat. Rec., 2011, 294, 1226-1232.
137. Meisel, R.L.; Sachs, B.D. The physiology of male sexual behavior. In: The Physiology of Reproduction, Knobil, E.; Neil, J.D., Eds., Raven Press: New York, 1994; pp. 3-105.
138. Bialy, M.; Nikolaev-Diak, A.; Kalata, U.; Nikolaev, E. Blockade of androgen receptor in the medial amygdala inhibits noncontact erections in male rats. Physiol. Behav., 2011, 103, 295-301.
139. Kondo, Y. Lesions of the medial amygdala produce severe impairment of copulatory behavior in sexually inexperienced male rats. Physiol. Behav., 1992, 51, 939-949.
140. 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., 1998, 91, 215-222.
141. 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., 1998, 63 253-259.
142. Zolman, J.F. Biostatistics; Oxford University Press: New York, 1993.
143. Majchrzak, M.; Brailowsky, S.; Will, B. Chronic infusion of GABA into the nucleus basalis magnocellularis or frontal cortex of rats: a behavioral and histological study. Exp. Brain Res., 1992, 88, 531-40.
144. Fillenz, M. Physiological release of excitatory amino acids. Behav. Brain Res., 1995, 71, 51-67.
145. Kaura, S.; Bradford, H. F.; Young, A. M.; Croucher, M. J.; Hughes, P. D. Effect of amygdaloid kindling on the content and release of amino acids from the amygdaloid complex: in vivo and in vitro studies. J. Neurochem., 1995, 65, 1240-1249.
146. Timmerman, W.; Westerink, B. H. Brain microdialysis of GABA and glutamate: what does it signify? Synapse, 1997, 27, 242-61.
147. Hagiwara, Y.; Kubo, T. Anterior hypothalamic neurons respond to blood pressure changes via gamma-aminobutyric acid and angiotensins in rats. Neurosci. Lett., 2005, 384, 250-253.
148. Kubo, T.; Hagiwara, Y. Posterior hypothalamus cholinergic stimulation-induced activation of anterior hypothalamic area neurons is enhanced in spontaneously hypertensive rats. Brain Res, 2005, 1061, 36-41.
149. Genest, S. E.; Balon, N.; Laforest, S.; Drolet, G.; Kinkead, R. Neonatal maternal separation and enhancement of the hypoxic ventilatory response in rat: the role of GABAergic modulation within the paraventricular nucleus of the hypothalamus. J. Physiol., 2007, 583, 299-314.
150. Ferreira, T. L.; Shammah-Lagnado, S. J.; Bueno, O. F.; Moreira, K. M.; Fornari, R. V.; Oliveira, M. G. The indirect amygdala-dorsal striatum pathway mediates conditioned freezing: insights on emotional memory networks. Neuroscience, 2008, 153, 84-94.
151. Quagliotto, E.; Neckel, H.; Riveiro, D. F.; Casali, K. R.; Mostarda, C.; Irigoyen, M. C.; Dall'Ago, P.; Rasia-Filho, A. A. Histamine in the posterodorsal medial amygdala modulates cardiovascular reflex responses in awake rats. Neuroscience, 2008, 157, 709-19.
152. Simmons, D. A.; Yahr, P. GABA and glutamate in matingactivated cells in the preoptic area and medial amygdala of male gerbils. J. Comp. Neurol., 2003, 459, 290-300.
153. Ben-Ari, Y.; Le Gal La Salle, G.; Barbin, G.; Schwartz, J. C.; Garbarg, M. Histamine synthesizing afferents within the amygdaloid complex and bed nucleus of the stria terminalis of the rat. Brain Res., 1977, 138, 285-294.
154. Chiavegatto, S.; Bernardi, M.M.; de Souza-Spinosa, H. Effects of prenatal diphenhydramine administration on sexual behavior in rat. Braz. J. Med. Biol. Res., 1989, 22, 729-732.
155. Silveira, M.C.L.; Sandner, G.; Graeff F.G. Induction of Fos immunoreactivity in the brain by exposure to the elevated plusmaze. Behav. Brain Res., 1993, 56, 115-118.
156. Pellow, S.; Chopin, P.; File, S.E.; Briley, M. Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J. Neurosci. Methods, 1985, 14, 149-167.
157. Cruz, A.P.M.; Frei, F.; Graeff, F.G. Ethopharmacological analysis of rat behavior on the elevated plus-maze. Pharmacol. Biochem. Behav., 1994, 49, 171-176.
158. Fernandes, C.; González, M.I.; Wilson, C.A.; File, S.E. Factor analysis shows that female rat behaviour is characterized primarily by activity, male rats are driven by sex and anxiety. Pharmacol. Biochem. Behav., 1999, 64, 731-738.
159. Lucion, A.B.; Charchat, H.; Pereira, G.A.M.; Rasia-Filho, A.A. Influence of early postnatal gonadal hormones on anxiety in adult male rats. Physiol. Behav., 1996, 60, 1419-1423.
160. 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., 1997, 44, 297-305.
161. Canteras, N.S.; Ribeiro-Barbosa, E.R.; Comoli, E. Tracing from the dorsal premammillary nucleus prosencephalic systems involved in the organization of innate fear responses. Neurosci. Biobehav. Rev., 2001, 25, 661-668.
162. Collins, D.R. Synthetic versus natural cat odorant effects on rodent behavior and medial amygdala plasticity. Behav. Neurosci., 2011, 125, 124-129.
163. Blanchard, D.C.; Canteras, N.S.; Markham, C.M.; Pentkowski, N.S.; Blanchard R.J. Lesions of structures showing Fos expression to cat presentation: effects on responsivity to a cat, cat odor, and nonpredator threat. Neurosci. Biobehav. Rev., 2005, 29, 1243-1253.
164. Takahashi, L.K.; Nakashima, B.R.; Hong, H.; Watanabe, K. The smell of danger: a behavioral and neural analysis of predator odorinduced fear. Neurosci. Biobehav. Rev., 2005, 2, 1157-1167.
165. Martinez, R.C.; Carvalho-Netto, E.F.; Ribeiro-Barbosa, É.R.; Baldo, M.V.C.; Canteras, N.S. Amygdalar roles during exposure to a live predator and to a predator-associated context. Neuroscience, 2011, 172, 314-328.
166. Rasia-Filho, A.A.; Londero, R.G.; Achaval, M. On some functional activities of the amygdala: an overview. J. Psychiatry Neurosci.,2000, 25: 14-23.
167. Nelson, R.J.; Trainor, B.C. Neural mechanisms of aggression. Nature Rev., 2007, 8, 536-546.
168. Roozendaal, B.; McGaugh, J.L. Amygdaloid nuclei lesions differentially affect glucocorticoid-induced memory enhancement in an inhibitory avoidance task. Neurobiol. Learn. Mem., 1996, 65, 1-8.
169. David, J.T.; Cervantes, M.C.; Trosky, K.A.; Salinas, J.A.; Delville, Y. A neural network underlying individual differences in emotion and aggression in male golden hamsters. Neuroscience, 2004, 126, 567-578.
170. Haller, J.; Tóth, M.; Halász, J.; De Boer, S.F. Patterns of violent aggression-induced brain c-fos expression in male mice selected for aggressiveness. Physiol. Behav., 2006, 88, 173-182.
171. Siegel, A.; Roeling, T.A.P.; Gregg, T.R.; Kruk, M.R. Neuropharmacology of brain-stimulation-evoked aggression. Neurosci. Biobehav. Rev., 1999, 23, 359-389.
172. Shaikh, M.B.; Siegel, A. Neuroanatomical and neurochemical mechanisms underlying amygdaloid control of defensive rage behavior in the cat. Braz. J. Med. Biol. Res., 1994, 27, 2759-2779.
173. Smith, D.A.; Flynn, J.P. Afferent projections to affective attack sites in cat hypothalamus. Brain Res., 1980, 194, 41-51.
174. Shibata, S.; Suwandi, D.; Yamamoto, T.; Ueki, S. Effects of medial amygdaloid lesions on the initiation and the maintenance of muricide in olfactory bulbectomized rats. Physiol. Behav., 1982, 29, 939-941.
175. Shibata, S.; Yamamoto, T.; Ueki, S. Differential effects of medial, central and basolateral amygdaloid lesions on four models of experimentally-induced aggression in rats. Physiol. Behav., 1982, 28, 289-294.
176. Halász, J.; Liposits, Z.; Kruk, M.R.; Haller, J. Neural background of glucocorticoid dysfunction-induced abnormal aggression in rats: involvement of fear-and stress-related structures. Eur. J. Neurosci., 2002, 15, 561-569.
177. Veening J.G.; Coolen, L.M.; de Jong, T.R.; Joosten, H.W.; de Boer, S.F.; Koolhaas, J.M.; Olivier, B. Do similar neural systems subserve aggressive and sexual behaviour in male rats? Insights from c-Fos and pharmacological studies. Eur. J. Pharmacol., 2005, 526, 226-239.
178. de Almeida, R.M.M.; Lucion, A.B. Role of the intruder in the aggressive behavior of colonies of wild rats (Rattus norvegicus). In: Animal Model in Psychopharmacology, Olivier, B.; Mos, J.; Slagen, J.L. Eds.; Birkhauser-Verlag: Basel, 1991; pp 347-356.
179. Kollack, S.S.; Newman, S.W. Mating behavior induces selective expression of Fos protein within the chemosensory pathways of the male Syrian hamster brain. Neurosci. Lett., 1992, 143, 223-228.
180. Kollack-Walker, S.; Newman, S.W. Mating and agonistic behavior produce different patterns of Fos immunolabeling in the male Syrian hamster brain. Neuroscience, 1995, 66, 721-736.
181. Kollack-Walker, S.; Newman, S.W. Mating-induced expression of c-fos in the male Syrian hamster brain: role of experience, pheromones, and ejaculations. J. Neurobiol., 1997, 32, 481-501.
182. Parfitt, D.B.; Newman, S.W. Fos-immunoreactivity within the extended amygdala is correlated with the onset of sexual satiety. Horm. Behav., 1998, 34, 17-29.
183. Boehm, S.; Betz, H. Somatostatin inhibits excitatory transmission at rat hippocampal synapses via presynaptic receptors. J. Neurosci., 1997, 17, 4066-4075.
184. Delfs, J.R.; Dichter, M.A. Effects of somatostatin on mammalian cortical neurons in culture: physiological actions and unusual dose response characteristics. J. Neurosci., 1983, 3, 1176-1188.
185. Lu, Y.F.; Hattori, Y.; Moriwaki, A.; Hayashi, Y.; Hori, Y. Inhibition of neurons in the rat medial amygdaloid nucleus in vitro by somatostatin. Can. J. Physiol. Pharmacol., 1995, 73, 670-674.
186. Saha, S.; Henderson, Z.; Batten, T.F. Somatostatin immunoreactivity in axon terminals in rat nucleus tractus solitarii arising from central nucleus of amygdala: coexistence with GABA and postsynaptic expression of sst2A receptor. J. Chem. Neuroanat., 2002, 24, 1-13.
187. Rakovska, A.; Kiss, J.P.; Raichev, P.; Lazarova, M.; Kalfin, R.; Milenov, K. Somatostatin stimulates striatal acetylcholine release by glutamatergic receptors: an in vivo microdialysis study. Neurochem. Int., 2002, 40, 269-275.
188. Meis, S.; Sosulina, L.; Schulz, S.; Höllt, V.; Pape HC. Mechanisms of somatostatin-evoked responses in neurons of the rat lateral amygdala. Eur. J. Neurosci., 2005, 21, 755-762.
189. Crane, J.W.; French, K.R.; Buller, K.M. Patterns of neuronal activation in the rat brain and spinal cord in response to increasing durations of restraint stress. Stress, 2005, 8, 199-211.
190. Kubo, T.; Okatani, H.; Nishigori, Y.; Hagiwara, Y.; Fukumori, R.; Goshima, Y. Involvement of the medial amygdaloid nucleus in restraint stress-induced pressor responses in rats. Neurosci. Lett., 2004, 354, 84-86.
191. Ebner, K.; Rupniak, N.M.; Saria, A.; Singewald, N. Substance P in the medial amygdala: emotional stress-sensitive release and modulation of anxiety related behavior in rats. Proc. Natl. Acad. Sci., USA, 2004, 101:4280-4285.
192. Singewald, N.; Chicchi, G.G.; Thurner, C.C.; Tsao, K.L.; Spetea, M.; Schmidhammer, H.; Sreepathi, H.K.; Ferraguti, F.; Singewald, G.M.; Ebner, K. Modulation of basal and stress-induced amygdaloid substance P release by the potent and selective NK1 receptor antagonist L-822429. J. Neurochem., 2008, 106, 2476-2488.
193. Kruk, M.R.; Westphal, K.G.; Van Erp, A.M.; van Asperen, J.; Cave, B.J.; Slater, E.; de Koning, J.; Haller, J. The hypothalamus: cross-roads of endocrine and behavioural regulation in grooming and aggression. Neurosci. Biobehav. Rev., 1998, 23, 163-177.
194. Morimoto, M.; Morita, N.; Ozawa, H.; Yokoyama, K.; Kawata, M. Distribution of glucocorticoid receptor immunoreactivity and mRNA in the rat brain: an immunohistochemical and in situ hybridization study. Neurosci. Res., 1996, 26, 235-269.
195. Herman, J.P.; Ostrander, M.M.; Mueller, N.K.; Figueiredo, H. Limbic system mechanisms of stress regulation: hypothalamopituitary-adrenocortical axis. Prog. Neuro-Psychopharmacol. Biol. Psychiatry, 2005, 29, 1201-1213.
196. Brunton, P.J.; Donadio, M.V.; Russell, J.A. Sex differences in prenatally programmed anxiety behavior in rats: Differential corticotrophin-releasing hormone receptor mRNA expression in the amygdaloid complex. Stress, 2011, PMID: 21854167.
197. Delville, Y.; De Vries, G.J.; Ferris, C.F. Neural connections of the anterior hypothalamus and agonistic behavior in golden hamsters. Brain Behav. Evol., 2000, 55, 53-76.
198. Donato Jr, J.; Cavalcante, J.C.; Silva, R.J.; Teixeira, A.S.; Bittencourt, J.C.; Elias, C.F. Male and female odors induce Fos expression in chemically defined neuronal population. Physiol. Behav., 2010, 99, 67-77.
199. Koolhaas, J.M.; Van den Brink, T.H.C.; Roozendaal, B.; Boorsma, F. Medial amygdala and aggressive behavior: interaction between testosterone and vasopressin. Aggress. Behav., 1990, 16, 223-229.
200. Paxinos, G.; Watson, C. The rat brain in stereotaxic coordinates. Academic Press: San Diego, 1998.
201. Quagliotto, E. Efeito da microinjeção de histamina e metilhistamina no núcleo póstero-dorsal da amígdala medial sobre o controle da pressão arterial em ratos. M.Sc Thesis. Federal University of Rio Grande do Sul/CAPES: Porto Alegre, 2006.