Sexual behavior and dendritic spine density of posterodorsal medial amygdala neurons in oxytocin knockout female mice

Behavioural Brain Research

Volumn 256, Issue , 2013, Pages 95-100

  Becker, Roberta Oriques ^a   Lazzari, Virgínia Meneghini ^a   Menezes, Itiana Castro ^b   Morris, Mariana ^c   Rigatto, Katya ^a   Lucion, Aldo B ^b   Rasia Filho, Alberto A ^a,b   Giovenardi, Márcia ^a  

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

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

^c WRIGHT STATE UNIVERSITY   (United States)

Author keywords

Extended amygdala; OTKO mice; Ovulation; Reproductive behavior; Vasopressin

Indexed keywords

ARGIPRESSIN; OXYTOCIN;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITIC SPINE; FEMALE; HORMONE BLOOD LEVEL; LATENT PERIOD; MOUSE; NONHUMAN; OOCYTE; POSTERODORSAL MEDIAL AMYGDALA; PRIORITY JOURNAL; PROESTRUS; SEXUAL BEHAVIOR; ANIMAL; BLOOD; BLOOD ANALYSIS; C57BL MOUSE; CELL COUNT; CYTOLOGY; GENETICS; GENOTYPING TECHNIQUE; KNOCKOUT MOUSE; PHYSIOLOGY;

AMYGDALA; ANIMALS; ARGININE VASOPRESSIN; BLOOD CHEMICAL ANALYSIS; CELL COUNT; DENDRITIC SPINES; FEMALE; GENOTYPING TECHNIQUES; MICE, INBRED C57BL; MICE, KNOCKOUT; OOCYTES; OXYTOCIN; SEXUAL BEHAVIOR, ANIMAL;

EID: 84883438771     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2013.07.034     Document Type: Article

References (92)

1. Choleris E., Clipperton-Allen A.E., Phan A., Kavaliers M. Neuroendocrinology of social information processing in rats and mice. Frontiers in Neuroendocrinology 2009, 30:442-459.
2. Gimpl G., Fahrenholz F. The oxytocin receptor system: structure, function, and regulation. Physiological Reviews 2001, 81:629-682.
3. Tom N., Stephen J.A. Oxytocin in health and disease. International Journal of Biochemistry & Cell Biology 2010, 42:202-205.
4. Lim M.M., Young L.J. Neuropeptidergic regulation of affiliative behavior and social bonding in animals. Hormones and Behavior 2006, 50:506-517.
5. Argiolas A., Meles M.R., Vargiu L., Gessa G.L. D(CH2)5Tyr(Me)-[Orn8]vasotocin, a potent oxytocin antagonist, antagonizes penile erection and yawning induced by oxytocin and apomorphine, but not by ACTH-(1-24). European Journal of Pharmacology 1987, 134:221-224.
6. Lee H.J., Macbeth A.H., Pagani J.H., Young W.S. Oxytocin: the great facilitator of life. Progress in Neurobiology 2009, 88:127-151.
7. Neumann I.D. Brain oxytocin: a key regulator of emotional and social behaviours in both females and males. Journal of Endocrinology 2008, 20:858-865.
8. Achiraman S., Ponmanickam P., Ganesh D.S., Archunan G. Detection of estrus by male mice: Synergistic role of olfactory-vomeronasal system. Neuroscience Letters 2010, 477:144-148.
9. Nevison C.M., Barnard C.J., Beynon R.J., Hurst J.L. The consequences of inbreeding for recognizing competitors. Proceedings of the Royal Society B: Biological Sciences 2000, 267:687-694.
10. Kavaliers M., Colwell D.D., Choleris E., Agmo A., Muglia L.J., Ogawa S., et al. Impaired discrimination of and aversion to parasitized male odors by female oxytocin knockout mice. Genes, Brain and Behavior 2003, 2:220-230.
11. Kavaliers M., Agmos A., Choleris E., Gustafsson J.A., Korach K.S., Muglia L.J., et al. Oxytocin and estrogen receptor a and b knockout miceprovide discriminably different odor cues in behavioral assays. Genes, Brain and Behavior 2004, 3:189-195.
12. Brennan P.A., Keverne E.B. Something in the air? New insights into mammalian pheromones. Current Biology 2004, 14:81-89.
13. Keller M., Michael J.B., Brock O., Brennan P.A., Bakker J. The main and the accessory olfactory systems interact in the control of mate recognition and sexual behavior. Behavioural Brain Research 2009, 200:268-276.
14. Wacker W.D., Ludwig M. Vasopressin, oxytocin, and social odor recognition. Hormones and Behavior 2012, 61:259-265.
15. Kevetter G.A., Winans S.S. Connections of the corticomedial amygdala in the golden hamster. II. Efferents of the olfactory amygdala. Journal of Comparative Neurology 1981, 197:99-111.
16. Young L.J. The neurobiology of social recognition, approach, and avoidance. Biological Psychiatry 2002, 51:18-26.
17. Ferguson J.N., Adag J.M., Insel T.R., Young L.J. Oxytocin in the medial amygdala is essential for social recognition in the mouse. Journal of Neuroscience 2001, 21:8278-8285.
18. Samuelsen C.L., Meredith M. Oxytocin antagonist disrupts male mouse medial amygdala response to chemical-communication signals. Neuroscience 2011, 180:96-104.
19. De Olmos J., Beltramino C.A., Alheid G.F. Amydala and extended amydala of the rat: cytoarchitectonical, fibroarchitectonical and chemoarchitectonical survey. The Rat Nervous System 2004, Vol. 1:509-603. Elsevier Academic Press, Amsterdam.
20. Choi G.B., Dong H.W., Murphy A.J., Valenzuela D.M., Yancopoulos G.D., Swanson L.W., et al. Lhx6 delineates a pathway mediating innate reproductive behaviors from the amygdala to the hypothalamus. Neuron 2005, 46:647-660.
21. Dall'Oglio A., Gehlen G., Achaval M., Rasia-Filho A.A. Dendritic branching feature s of posterodorsal medial amygdala neurons of adult male and female rats: further data based on the Golgi method. Neuroscience Letters 2008, 430:151-156.
22. Newman S.W. The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network. Annals of the New York Academy of Sciences 1999, 877:242-257.
23. Sheehan T.P., Paul M., Amaral E., Numa 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.
24. Rasia-Filho A.A., Dalpian F., Menezes I.C., Brusco J., Moreira J.E., Cohen R.S. Dendritic spines of the medial amygdala: plasticity, density, shape, and subcellular modulation by sex steroids. Histology and Histopathology 2012, 27:985-1011.
25. Rasia-Filho A.A., Haas D., de Oliveira A.P., de Castilhos J., Frey R., Stein D., et al. Morphological and functional features of the sex steroid-responsive posterodorsal medial amygdala of adult rats. Mini Reviews in Medicinal Chemistry 2012, 12:1090-1106.
26. 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.
27. Johnson R.T., Breedlove S.M., Jordan C.L. Sex differences and laterality in astrocyte number and complexity in the adult rat medial amygdala. Journal of Comparative Neurology 2008, 511:599-609.
28. 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. Journal of Comparative Neurology 2008, 506:851-859.
29. Gréco B., Allegretto E.A., Tetel M.J., Blaustein J.D. Coexpression of ER beta with ER alpha and progestin receptor proteins in the female rat forebrain: effects of estradiol treatment. Endocrinology 2001, 142:5172-5181.
30. Gréco B., Blasberg M.E., Kosinski E.C., Blaustein J.D. Response of ERalpha-IR and ERbeta-IR cells in the forebrain of female rats to mating stimuli. Hormones and Behavior 2003, 43:444-453.
31. 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 Research 2008, 1240:73-81.
32. Segal M. Dendritic spines, synaptic plasticity and neuronal survival: activity shapes dendritic spines to enhance neuronal viability. European Journal of Neuroscience 2010, 31:2178-2184.
33. Nuriya M., Jiang J., Nemet B., Eisenthal K.B., Yuste R. Imaging membrane potential in dendritic spines. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:786-790.
34. Chen Y., Sabatini B.L. Signaling in dendritic spines and spine microdomains. Current Opinion in Neurobiology 2012, 22:389-396.
35. Rochefort N.L., Konnerth A. Dendritic spines: from structure to in vivo function. EMBO Reports 2012, 13:699-708.
36. 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. Experimental Brain Research 1994, 101:1-7.
37. 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.
38. Pfaus J.G., Hebb M.M. Implications of immediate-early gene induction in the brain following sexual stimulation of female and male rodents. Brain Research Bulletin 1997, 44:397-407.
39. Simerly R.B. Anatomical substrates of hypothalamic integration. The rat nervous system 2004, Vol. 1:335-369. Elsevier Academic Press, Amsterdam.
40. Meredith M., Westberry J.M. Distinctive responses in the medial amygdala to same-species and different-species pheromones. Journal of Neuroscience 2004, 24:5719-5725.
41. 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. Journal of Physiology and Biochemistry 2011, 67:71-85.
42. 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. Journal of Neuroscience 2001, 21:4104-4110.
43. Lehmann M.L., McKellar H., Erskine M.S. Coding for the initiation of pseudopregnancy by temporally patterned activation of amygdalar NMDA receptors. Journal of Neuroscience 2005, 25:8696-8703.
44. Witt D.M. Oxytocin and rodent sociosexual responses: from behavior to gene expression. Neuroscience and Biobehavioral Reviews 1995, 19:315-324.
45. Argiolas A., Collu M., Gessa G.L., Melis M.R., Serra G. The oxytocin antagonist d(CH2)5Tyr(Me)-Orn8-vasotocin inhibits male copulatory behaviour in rats. European Journal of Pharmacology 1988, 149:389-392.
46. Arletti R., Bertolini A. Oxytocin stimulates lordosis behavior in female rats. Neuropeptides 1985, 6:247-253.
47. Kow L.M., Pfaff D.W. Mapping of neural and signal transduction pathways for lordosis in the search for estrogen actions on the central nervous system. Behavioural Brain Research 1998, 92:169-180.
48. Caldwell J.D. Central oxytocin and female sexual behavior. Annals of the New York Academy of Sciences 1992, 652:166-179.
49. Lee H-J., Pagani J., Young W.S. Using transgenic mouse models to study oxytocin's role in the facilitation of species propagation. Brain Research 2010, 1364:216-224.
50. McCarthy M.M., Kleopoulous C.V., Mobbs C.V., Pfaff D.W. Infusion of antisense oligodeoxynucleotides to the oxytocin receptor in the ventromedial hypothalamus reduces estrogen-induced sexual receptivity and oxytocin receptor binding in the female rat. Neuroendocrinology 1994, 59:432-440.
51. Caligioni C.S., Oliver C., Jamur M.C., Franci C.R. Presence of oxytocin receptors in the gonadotrophin-releasing hormone (GnRH) neurones in female rats: a possible direct action of oxytocin on GnRH neurones. Journal of Neuroendocrinology 2007, 19:439-448.
52. Södersten P., DeVries G.J., Buijs R.M., Melin P. A daily rhythm in behavioural vasopressin sensitivity and brain vasopressin concentrations. Neuroscience Letters 1985, 58:37-41.
53. Caldwell J.D., Barakat A.S., Smith D.D., Hruby V.J., Pedersen C.A. A uterotonic antagonist blocks the oxytocin-induced facilitation of female sexual receptivity. Brain Research 1990, 512:291-296.
54. Antunes I.B., Da Silva A., Kawakami R., Andersen M.L. The female rat. Animal models as tools in ethical biomedical research 2010, 103-120. M.L. Andersen, S. Tufik (Eds.).
55. Rasia-Filho A.A., Lucion A.B. Effects of 8-OH-DPAT on sexual behavior of male rats castrated at different ages. Hormones and Behavior 1996, 30:251-258.
56. Young W.S., Shepard E., Amico J., Hennighausen L., Wagner K.U., Lamarca M.U., et al. Deficiency in mouse oxytocin prevents milk ejection, but not fertility or parturition. Journal of Neuroendocrinology 1996, 8:847-853.
57. Swaney W.T., Dubose B.N., Curley J.P., Champagne F.A. Sexual experience affects reproductive behavior and preoptic androgen receptors in male mice. Hormones and Behavior 2012, 61:472-478.
58. Jonhansen J.A., Clemens L.G., Nunez A.A. Characterization of copulatory behavior in female mice: evidence for paced mating. Physiology and Behavior 2008, 95:425-429.
59. Hardy D.F., DeBold J.F. Effects of mounts without intromission upon the behavior of female rats during the onset of estrogen-induced heat. Physiology and Behavior 1971, 7:643-645.
60. Gomez C.M., Frantz P.J., Sanvitto G.L., Anselmo-Franci J.A., Lucion A.B. Neonatal handling induces anovulatory estrous cycles in rats. Brazilian Journal of Medical and Biological Research 1999, 32:1239-1242.
61. Arpini M., Menezes I.T., Dall'Oglio A., Rasia-Filho A.A. The density of Golgi-impregnated dendritic spines from adult rat posterodorsal medial amygdala neurons displays no evidence of hemispheric or dorsal/ventral differences. Neuroscience Letters 2010, 469:209-221.
62. Franklin K.B.J., Paxinos G. The mouse brain in stereotaxic coordinates 1997, Academic Press, San Diego.
63. DeVries A.C., Young W.S., Nelson R.J. Reduced aggressive behaviour in mice with targeted disruption of the oxytocin gene. Journal of Neuroendocrinology 1997, 9:363-368.
64. Nishimori K., Young L.J., Guo Q., Wang Z., Insel T.R., Matzuk M.M. Oxytocin is required for nursing but not essential for parturition or reproductive behavior. Proceedings of the National Academy of Sciences of the United States of America 1996, 93:11699-11704.
65. Insel T.R., Gelhard R., Shapiro L.E. The comparative distribution of forebrain receptors for neurohypophyseal peptides inmonogamous and polygamous mice. Neuroscience 1991, 43:623-630.
66. Pedersen C.A., Caldwell J.D., Jirikowski G.F., Insel T.R. Oxytocin in maternal, sexual, and social behaviors. Annals of the New York Academy of Sciences 1992, 652:1-492.
67. Borrow A.P., Cameron N.M. The role of oxytocin in mating and pregnancy. Hormones and Behavior 2012, 61:266-276.
68. Lazzari V.M., Becker R.O., Azevedo M.S., Morris M., Rigatto K., Almeida S., et al. Oxytocin modulates social interaction but is not essential for sexual behavior in male mice. Behavioural Brain Research 2013, 244:130-136.
69. Carter C.S., Lederhendler I.I., Kirkpatrick B. The interactive neurobiology of affiliation. Annals of the New York Academy of Sciences 1997, 807:13-18.
70. Argiolas A., Melis M.R. The role of oxytocin and the paraventricular nucleus in the sexual behaviour of male mammals. Physiology and Behavior 2004, 83:309-317.
71. Ivell R., Russel J.A. Oxytocin: cellular and molecular approaches in medicine and research. Advances in Experimental Medicine and Biology 1995, 1:13-18.
72. Gorzalka BB, Lester G.L. Oxytocin-induced facilitation of lordosis behavior in rats in progesterone-dependent. Neuropeptides 1987, 10:55-56.
73. Pfaff D.W., Schwartz-Giblin S., McCarthy M.M., Kow L.M. Cellular and molecular mechanisms of female reproductive behaviors. The Physiology of Reproduction 1994, 1:107-220.
74. Segovia S., Garcia-Falgueras A., Perez-Lago C., Pinos H., Carrillo B., Collado P., et al. The effects of partial and complete masculinization on the sexual differentiation of nuclei that control lordotic behavior in the male rat. Behavioural Brain Research 2009, 196:261-267.
75. Caldwell J.D., Johns J.M., Faggin B.M., Senger M.A., Pedersen C.A. Infusion of an oxytocin antagonist into the medial preoptic area prior to progesterone inhibits sexual receptivity and increases rejection in female rats. Hormones and Behavior 1994, 28:288-302.
76. Ferri-Kolwicz S.L., Flanagan-Cato L.M. Oxytocin and dendrite remodeling in the hypothalamus. Hormones and Behavior 2012, 61:251-258.
77. Sarkar D.K., Chiappa S.A., Fink G., Sherwood N.M. Gonadotropin-releasing hormone surge in proestrous rats. Nature 1976, 264:461-463.
78. Robinson G., Evans J.J. Oxytocin has a role in gonadotrophin regulation in rats. Journal of Endocrinology 1990, 125:425-432.
79. Levine J.E., Bauer-Dantoin A.C., Besecke L.M., Conaghan L.A., Legan S.J., Meredith J.M., et al. Neuroendocrine regulation of luteinizing hormone pulse generator in the rat. Recent Progress in Hormone Research 1991, 47:97-153.
80. Freeman M.E. The neuroendocrine control of the estrous cycle in the rat. The physiology of reproduction 1994, 613-658. Raven Press, New York. 2nd ed. E. Knobil, J.D. Neill (Eds.).
81. Johnston C.A., Lopez F., Samson W.K., Negro-Vilar A. Physiologically important role for central oxytocin in the preovulatory release of luteinizing hormone. Neuroscience Letters 1990, 120:256-258.
82. Selvage D., Johnston C.A. Central stimulatory influence of oxytocin on preovulatory gonadotropin-releasing hormone requires more than the median eminence. Neuroendocrinology 2001, 74:129-134.
83. Patisaul H.B., Scordalakes E.M., Young L.J., Rissman E.F. Oxytocin, but not oxytocin receptor, is regulated by oestrogen receptor beta in the female mouse hypothalamus. Journal of Neuroendocrinology 2003, 15:787-793.
84. Clipperton-Allen A.E., Lee A.W., Reyes A., Devidze N., Phan A., Pfaff D.W., Choleris E. Oxytocin, vasopressin and estrogen receptor gene expression in relation to social recognition in female mice. Physiology and Behavior 2012, 105:915-924.
85. 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. Journal of Comparative Neurology 1990, 294:76-95.
86. Allen Mouse Brain Atlas [Internet] 2012, Allen Institute for Brain Science, Available from: http://mouse.brain-map.org/.
87. Lukas M., Veenema A.H., Neumann I.D. Oxytocin mediates rodent social memory within the lateral septum and the medial amygdala depending on the relevance of the social stimulus: male juvenile versus female adult conspecifics. Psychoneuroendocrinology 2012, 61:50-56.
88. 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 Research 1978, 142:363-367.
89. Gabor C.S., Phan A., Clipperton-Allen A.E., Kavaliers M., Choleris E. Interplay of oxytocin, vasopressin, and sex hormones in the regulation of social recognition. Behavioral Neuroscience 2012, 126:97-109.
90. Donaldson Z.R., Young L.J. Oxytocin, vasopressin and the neurogenetics of sociality. Science 2008, 322:900-904.
91. Ratty A.K., Jeong S.W., Nagle J.W., Chin H., Gainer H., Murphy D. A systematic survey of the intragenic region between the murine oxytocin- and vasopressin-encoding genes. Gene 1996, 174:71-78.
92. Ozaki Y., Nomura M., Saito J., Luedke C.E., Muglia L.J., Matsumoto T., et al. Expression of the arginine vasopressin gene in response to salt loading in oxytocin gene knockout mice. Journal of Neuroendocrinology 2004, 16:39-44.