Copulation or sensory cues from the female augment Fos expression in arginine vasopressin neurons of the posterodorsal medial amygdala of male rats

Frontiers in Zoology

Volumn 11, Issue 1, 2014, Pages

  Hari Dass, Shantala A ^a   Vyas, Ajai ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

Affiliation; Mating; Neuropeptide; Nonapeptide; Pheromone; Sexual behavior; Social behavior; Testosterone; Vasotocin

Indexed keywords

EID: 84902259536     PISSN: None     EISSN: 17429994     Source Type: Journal    
DOI: 10.1186/1742-9994-11-42     Document Type: Article

References (48)

1. Greco B, Edwards DA, Michael RP, Clancy AN. 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. 10.1159/000054294, 9485165.
2. Lehman MN, Winans SS, Powers JB. Medial nucleus of the amygdala mediates chemosensory control of male hamster sexual behavior. Science 1980, 210:557-60. 10.1126/science.7423209, 7423209.
3. Kondo Y. Lesions of the medial amygdala produce severe impairment of copulatory behavior in sexually inexperienced male rats. Physiol Behav 1992, 51:939-43. 10.1016/0031-9384(92)90074-C, 1615054.
4. Heeb MM, Yahr P. Cell-body lesions of the posterodorsal preoptic nucleus or posterodorsal medial amygdala, but not the parvicellular subparafascicular thalamus, disrupt mating in male gerbils. Physiol Behav 2000, 68:317-31. 10.1016/S0031-9384(99)00182-1, 10716541.
5. Maras PM, Petrulis A. Chemosensory and steroid-responsive regions of the medial amygdala regulate distinct aspects of opposite-sex odor preference in male Syrian hamsters. Eur J Neurosci 2006, 24:3541-52. 10.1111/j.1460-9568.2006.05216.x, 17229102.
6. Maras PM, Petrulis A. The anterior medial amygdala transmits sexual odor information to the posterior medial amygdala and related forebrain nuclei. Eur J Neurosci 2010, 32:469-82. 10.1111/j.1460-9568.2010.07289.x, 20704594.
7. Kondo Y, Sachs BD, Sakuma Y. Importance of the medial amygdala in rat penile erection evoked by remote stimuli from estrous females. Behav Brain Res 1998, 91:215-22.
8. Cooke BM. Steroid-dependent plasticity in the medial amygdala. Neuroscience 2006, 138:997-1005. 10.1016/j.neuroscience.2005.06.018, 16330154.
9. Mizukami S, Nishizuki M, Arai Y. Sexual difference in nuclear volume and its ontogeny in the rat amygdala. Exp Neurol 1983, 79:569-75. 10.1016/0014-4886(83)90235-2, 6822281.
10. Cooke BM, Tabibnia G, Breedlove SM. A brain sexual dimorphism controlled by adult circulating androgens. Proc Natl Acad Sci U S A 1999, 96:7538-40. 10.1073/pnas.96.13.7538, 22121, 10377450.
11. Wang Z, De Vries GJ. Androgen and estrogen effects on vasopressin messenger RNA expression in the medial amygdaloid nucleus in male and female rats. J Neuroendocrinol 1995, 7:827-31. 10.1111/j.1365-2826.1995.tb00722.x, 8748118.
12. DeVries GJ, Buijs RM, Van Leeuwen FW, Caffe AR, Swaab DF. The vasopressinergic innervation of the brain in normal and castrated rats. J Comp Neurol 1985, 233:236-54. 10.1002/cne.902330206, 3882778.
13. Auger CJ, Coss D, Auger AP, Forbes-Lorman RM. Epigenetic control of vasopressin expression is maintained by steroid hormones in the adult male rat brain. Proc Natl Acad Sci 2011, 108:4242-7. 10.1073/pnas.1100314108, 3053981, 21368111.
14. 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. 10.1016/j.physbeh.2011.02.003, 21315100.
15. Bialy M, Sachs BD. Androgen implants in medial amygdala briefly maintain noncontact erection in castrated male rats. Horm Behav 2002, 42:345-55. 10.1006/hbeh.2002.1821, 12460594.
16. Cooke BM, Breedlove SM, Jordan CL. 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 2003, 43:336-46. 10.1016/S0018-506X(02)00047-8, 12694644.
17. Aste N, Honda S, Harada N. Forebrain Fos responses to reproductively related chemosensory cues in aromatase knockout mice. Brain Res Bull 2003, 60:191-200. 10.1016/S0361-9230(03)00035-2, 12754080.
18. Bressler SC, Baum MJ. Sex comparison of neuronal Fos immunoreactivity in the rat vomeronasal projection circuit after chemosensory stimulation. Neuroscience 1996, 71:1063-72. 10.1016/0306-4522(95)00493-9, 8684610.
19. Paredes RG, Lopez ME, Baum MJ. Testosterone augments neuronal Fos responses to estrous odors throughout the vomeronasal projection pathway of gonadectomized male and female rats. Horm Behav 1998, 33:48-57. 10.1006/hbeh.1998.1435, 9571013.
20. Hoffman GE, Smith MS, Verbalis JG. c-Fos and related immediate early gene products as markers of activity in neuroendocrine systems. Front Neuroendocrinol 1993, 14:173-213. 10.1006/frne.1993.1006, 8349003.
21. He F, Wu R, Yu P. Study of Fos, androgen receptor and testosterone expression in the sub-regions of medial amygdala, bed nucleus of stria terminalis and medial preoptic area in male mandarin voles in response to chemosensory stimulation. Behav Brain Res 2014, 258:65-74.
22. Wood RI, Coolen LM. Integration of chemosensory and hormonal cues is essential for sexual behaviour in the male Syrian hamster: role of the medial amygdaloid nucleus. Neuroscience 1997, 78:1027-35. 10.1016/S0306-4522(96)00629-X, 9174071.
23. Wood RI, Newman SW. Integration of chemosensory and hormonal cues is essential for mating in the male Syrian hamster. J Neurosci 1995, 15:7261-9.
24. Lim MM, Hammock EA, Young LJ. The role of vasopressin in the genetic and neural regulation of monogamy. J Neuroendocrinol 2004, 16:325-32. 10.1111/j.0953-8194.2004.01162.x, 15089970.
25. Bluthe RM, Schoenen J, Dantzer R. Androgen-dependent vasopressinergic neurons are involved in social recognition in rats. Brain Res 1990, 519:150-7. 10.1016/0006-8993(90)90073-K, 1975762.
26. Ho JM, Murray JH, Demas GE, Goodson JL. Vasopressin cell groups exhibit strongly divergent responses to copulation and male-male interactions in mice. Horm Behav 2010, 58:368-77. 10.1016/j.yhbeh.2010.03.021, 20382147.
27. Choi GB, Dong H-W, Murphy AJ, Valenzuela DM, Yancopoulos GD, Swanson LW, Anderson DJ. Lhx6 delineates a pathway mediating innate reproductive behaviors from the amygdala to the hypothalamus. Neuron 2005, 46:647-60. 10.1016/j.neuron.2005.04.011, 15944132.
28. Samuelsen CL, Meredith M. The vomeronasal organ is required for the male mouse medial amygdala response to chemical-communication signals, as assessed by immediate early gene expression. Neuroscience 2009, 164:1468-76. 10.1016/j.neuroscience.2009.09.030, 2801006, 19778594.
29. Meredith M. Vomeronasal, olfactory, hormonal convergence in the brain. cooperation or coincidence?. Ann N Y Acad Sci 1998, 855:349-61. 10.1111/j.1749-6632.1998.tb10593.x, 9929627.
30. Morris JA, Jordan CL, King ZA, Northcutt KV, Breedlove SM. Sexual dimorphism and steroid responsiveness of the posterodorsal medial amygdala in adult mice. Brain Res 2008, 1190:115-21. 2258085, 18054901.
31. Blake CB, Meredith M. Change in number and activation of androgen receptor-immunoreactive cells in the medial amygdala in response to chemosensory input. Neuroscience 2011, 190:228-38. 3156313, 21684322.
32. Zhou L, Blaustein JD, De Vries GJ. Distribution of androgen receptor immunoreactivity in vasopressin- and oxytocin-immunoreactive neurons in the male rat brain. Endocrinology 1994, 134:2622-7.
33. Kondo Y, Arai Y. Functional association between the medial amygdala and the medial preoptic area in regulation of mating behavior in the male rat. Physiol Behav 1995, 57:69-73. 10.1016/0031-9384(94)00205-J, 7878127.
34. Been LE, 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 hamsters. Horm Behav 2011, 59:536-48. 10.1016/j.yhbeh.2011.02.005, 3081384, 21316366.
35. Johnston JB. Further contributions to the study of the evolution of the forebrain. J Comp Neurol 1923, 35:337-481.
36. Kabelik D, Morrison JA, Goodson JL. Cryptic regulation of vasotocin neuronal activity but not anatomy by sex steroids and social stimuli in opportunistic desert finches. Brain Behav Evol 2010, 75:71-84. 10.1159/000297522, 2914398, 20332615.
37. Baum MJ, Tobet SA, Starr MS, Bradshaw WG. Implantation of dihydrotestosterone propionate into the lateral septum or medial amygdala facilitates copulation in castrated male rats given estradiol systemically. Horm Behav 1982, 16:208-23. 10.1016/0018-506X(82)90020-4, 7118087.
38. Dluzen DE, Muraoka S, Engelmann M, Landgraf R. The effects of infusion of arginine vasopressin, oxytocin, or their antagonists into the olfactory bulb upon social recognition responses in male rats. Peptides 1998, 19:999-1005. 10.1016/S0196-9781(98)00047-3, 9700747.
39. Tobin VA, Hashimoto H, Wacker DW, Takayanagi Y, Langnaese K, Caquineau C, Noack J, Landgraf R, Onaka T, Leng G, Meddle SL, Engelmann M, Ludwig M. An intrinsic vasopressin system in the olfactory bulb is involved in social recognition. Nature 2010, 464:413-7. 10.1038/nature08826, 2842245, 20182426.
40. Wacker DW, Ludwig M. Vasopressin, oxytocin, and social odor recognition. Horm Behav 2012, 61:259-65. 10.1016/j.yhbeh.2011.08.014, 21920364.
41. Goodson JL, Kelly AM, Kingsbury MA. Evolving nonapeptide mechanisms of gregariousness and social diversity in birds. Horm Behav 2012, 61:239-50. 10.1016/j.yhbeh.2012.01.005, 3312996, 22269661.
42. Garrison JL, Macosko EZ, Bernstein S, Pokala N, Albrecht DR, Bargmann CI. Oxytocin/vasopressin-related peptides have an ancient role in reproductive behavior. Science 2012, 338:540-3. 10.1126/science.1226201, 3597094, 23112335.
43. Young LJ, Nilsen R, Waymire KG, MacGregor GR, Insel TR. Increased affiliative response to vasopressin in mice expressing the V1a receptor from a monogamous vole. Nature 1999, 400:766-8. 10.1038/23475, 10466725.
44. Raab A, Haedenkamp G. Impact of social conflict between mice on testosterone binding in the central nervous system. Neuroendocrinology 1981, 32:272-7. 10.1159/000123172, 6113558.
45. Blanchard DC, Sakai RR, McEwen B, Weiss SM, Blanchard RJ. Subordination stress: behavioral, brain, and neuroendocrine correlates. Behav Brain Res 1993, 58:113-21. 10.1016/0166-4328(93)90096-9, 8136039.
46. Cooke BM, Chowanadisai W, Breedlove SM. Post-weaning social isolation of male rats reduces the volume of the medial amygdala and leads to deficits in adult sexual behavior. Behav Brain Res 2000, 117:107-13. 10.1016/S0166-4328(00)00301-6, 11099763.
47. Van Zwieten EJ, Kos WT, Ravid R, Swaab DF. Decreased number of vasopressin immunoreactive neurons in the medial amygdala and locus coeruleus of the aged rat. Neurobiol Aging 1993, 14:245-8. 10.1016/0197-4580(93)90008-Y, 8321392.
48. Lin D, Boyle MP, Dollar P, Lee H, Lein ES, Perona P, Anderson DJ. Functional identification of an aggression locus in the mouse hypothalamus. Nature 2011, 470:221-6. 10.1038/nature09736, 3075820, 21307935.