Activational effects of estradiol and dihydrotestosterone on social recognition and the arginine-vasopressin immunoreactive system in male mice lacking a functional aromatase gene.
Pierman, S.; Sica, M.; Allieri, F.et al.
2008 • In Hormones and Behavior, 54 (1), p. 98-106
[en] In rodents, parts of the arginine-vasopressin (AVP) neuronal system are sexually dimorphic with males having more AVP-immunoreactive cells/fibers than females. This neuropeptide neuronal system is highly sensitive to steroids and has been proposed to play an important role in the processing of olfactory cues critical to the establishment of a social memory. We demonstrate here that gonadally intact male aromatase knockout (ArKO) mice, which cannot aromatize androgens into estrogens due to a targeted mutation in the aromatase gene, showed severe deficits in social recognition as well as a reduced AVP-immunoreactivity in several brain regions. To determine whether this reduction is due to a lack of organizational or activational effects of estrogens, we assessed social recognition abilities and AVP-immunoreactivity in male ArKO and wild-type (WT) mice when treated with estradiol benzoate (EB) in association with dihydrotestosterone propionate (DHTP) in adulthood. Adult treatment with EB and DHTP restored social recognition abilities in castrated ArKO males since they showed normal female-oriented ultrasonic vocalizations and were able to recognize an unfamiliar female using a habituation-dishabituation paradigm. Furthermore, adult treatment also restored AVP-immunoreactivity in the lateral septum of ArKO males to levels observed in intact WT males. These results suggest that social recognition in adulthood and stimulation of AVP expression in the adult mouse forebrain depend predominantly on the estrogenic metabolite of testosterone. Furthermore, our results are in line with the idea that the organization of the AVP system may depend on androgen or sex chromosomes rather than estrogens.
Disciplines :
Neurosciences & behavior
Author, co-author :
Pierman, S.
Sica, M.
Allieri, F.
Viglietti-Panzica, C.
Panzica, G. C.
Bakker, Julie ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Language :
English
Title :
Activational effects of estradiol and dihydrotestosterone on social recognition and the arginine-vasopressin immunoreactive system in male mice lacking a functional aromatase gene.
Publication date :
2008
Journal title :
Hormones and Behavior
ISSN :
0018-506X
eISSN :
1095-6867
Publisher :
Academic Press, San Diego, United States - California
Allieri F., Spigolon G., Viglietti-Panzica C., Garcia-Falgueras A., Guillamon A., Collado P., and Panzica G.C. The Tfm rat, a model to study the influence of testosterone on the development of limbic vasopressinergci system. Trabajos del Instituto Cajal LXXX (2005) 198-199
Bakker J., Honda S., Harada N., and Balthazart J. Sexual partner preference requires a functional aromatase (Cyp19) gene in male mice. Horm. Behav. 42 (2002) 158-171
Bakker J., Honda S., Harada N., and Balthazart J. Restoration of male sexual behavior by adult exogenous estrogens in male aromatase knockout mice. Horm. Behav. 46 (2004) 1-10
Bakker J., De Mees C., Douhard Q., Balthazart J., Gabant P., Szpirer J., and Szpirer C. Alpha-fetoprotein protects the developing female mouse brain from masculinization and defeminization by estrogens. Nat. Neurosci. 9 (2006) 220-226
Bielsky I.F., and Young L.J. Oxytocin, vasopressin, and social recognition in mammals. Peptides 25 (2004) 1565-1574
Bielsky I.F., Hu S.B., Szegda K.L., Westphal H., and Young L.J. Profound impairment in social recognition and reduction in anxiety-like behavior in vasopressin V1a receptor knockout mice. Neuropsychopharmacology 29 (2004) 483-493
[ROMAN]Bluthe R.M., and Dantzer R. Social recognition does not involve vasopressinergic neurotransmission in female rats. Brain Res. 535 (1990) 301-304
Bluthe R.M., Schoenen J., and Dantzer R. Androgen-dependent vasopressinergic neurons are involved in social recognition in rats. Brain Res. 519 (1990) 150-157
Brown R.E. Mammalian social odors: a critical review. Adv. Study Behav. 10 (1979) 107-161
De Vries G.J., and Buijs R.M. The origin of the vasopressinergic and oxytocinergic innervation of the rat brain with special reference to the lateral septum. Brain Res. 273 (1983) 307-317
De Vries G.J., and Al Shamma H.A. Sex differences in hormonal responses of vasopressin pathways in the rat brain. J. Neurobiol. 21 (1990) 686-693
De Vries G.J., and Boyle P.A. Double duty for sex differences in the brain. Behav. Brain Res. 92 (1998) 205-213
De Vries G.J., and Miller M.A. Anatomy and function of extrahypothalamic vasopressin systems in the brain. Prog. Brain Res. 119 (1998) 3-20
De Vries G.J., and Panzica G.C. Sexual differentiation of central vasopressin and vasotocinsystems in vertebrates: different mechanisms, similar endpoints. Neuroscience 138 (2006) 947-955
De Vries G.J., Al Shamma H.A., and Zhou L. The sexually dimorphic vasopressin innervation of the brain as a model for steroid modulation of neuropeptide transmission. In: Harding C.F. (Ed). Hormonal restructuring of the adult brain. Basic and clinical perspectives. Annals vol. 743 (1994), New York Academy of Sciences, New York, USA 95-120
De Vries G.J., Wang Z., Bullock N.A., and Numan S. Sex differences in the effects of testosterone and its metabolites on vasopressin messenger RNA levels in the bed nucleus of the stria terminalis of rats. J. Neurosci. 14 (1994) 1789-1794
De Vries G.J., Rissman E.F., Simerly R.B., Yang L.Y., Scordalakes E.M., Auger C.J., Swain A., Lovell-Badge R., Burgoyne P.S., and Arnold A.P. A model system for study of sex chromosome effects on sexually dimorphic neural and behavioral traits. J. Neurosci. 22 (2002) 9005-9014
Dizinno G., Whitney G., and Nyby J. Ultrasonic vocalizations by male mice (mus musculus) in response to a female-produced pheromone: effects of experience. Behav. Biol. 22 (1978) 104-113
Engelmann M., and Landgraf R. Microdialysis administration of vasopressin into the septum improves social recognition in Brattleboro rats. Physiol. Behav. 55 (1994) 145-149
Engelmann M., Wotjak C.T., Neumann I., Ludwig M., and Landgraf R. Behavioral consequences of intracerebral vasopressin and oxytocin: focus on learning and memory. Neurosci. Biobehav. Rev. 20 (1996) 341-358
Ferris C.F., Delville Y., Miller M.A., Dorsa D.M., and De Vries G.J. Distribution of small vasopressinergic neurons in golden hamsters. J. Comp. Neurol. 360 (1995) 589-598
Fisher C.R., Graves K.H., Parlow A.F., and Simpson E.R. Characterization of mice deficient in aromatase (ArKO) because of targeted disruption of the cyp19 gene. Proc. Natl. Acad. Sci. 95 (1998) 6965-6970
Franklin K.B.J., and Paxinos G. The mouse brain in stereotaxic coordinates (1997), Academic Press, New York
Han T.M., and De Vries G.J. Organizational effects of testosterone, estradiol, and dihydrotestosterone on vasopressin mRNA expression in the bed nucleus of the stria terminalis. J. Neurobiol. 54 (2003) 502-510
Honda S., Harada N., Ito S., Takagi Y., and Maeda S. Disruption of sexual behavior in male aromatase-deficient mice lacking exons 1 and 2 of the cyp19 gene. Biochem. Biophys. Res. Commun. 252 (1998) 445-449
Maggio J.C., and Whitney G. Ultrasonic vocalizing by adult female mice (Mus musculus). J. Comp. Psychol. 99 (1985) 420-436
Nyby J.G., Dizinno G., and Whitney G. Sexual dimorphism in ultrasonic vocalizations of mice (Mus musculus): gonadal hormone regulation. J. Comp. Physiol. Psychol. 91 (1977) 1424-1431
Pierman S., Douhard Q., Balthazart J., Baum M.J., and Bakker J. Attraction thresholds and sex discrimination of urinary odorants in male and female aromatase knockout (ArKO) mice. Horm. Behav. 49 (2006) 96-104
Pierman S., Tirelli E., Douhard Q., Baum M.J., and Bakker J. Male aromatase knockout mice acquire a conditioned place preference for cocaine but not for contact with an estrous female. Behav. Brain Res. 174 (2006) 64-69
Plumari L., Viglietti-Panzica C., Allieri F., Honda S., Harada N., Absil P., Balthazar J., and Panzica G.C. Changes in the arginine-vasopressin immunoreactive systems in male mice lacking a functional aromatase gene. J. Neuroendocrinol. 14 (2002) 971-978
Sales G.D. Ultrasound and mating behavior in rodents with some observations on other behavioral situations. J. Zool. 168 (1972) 149-164
Viglietti-Panzica C., Aste N., Balthazart J., and Panzica G.C. Vasotocinergic innervation of sexually dimorphic medial preoptic nucleus of the male Japanese quail: influence of testosterone. Brain Res. 657 (1994) 171-184
Viglietti-Panzica C., Balthazart J., Fratesi S., Plumari L., Absil P., and Panzica G.C. Estradiol mediates effects of testosterone on vasotocin-immunoreactivity in the adult quail brain. Horm. Behav. 40 (2001) 445-461
Wesson D.W., Keller M., Douhard Q., Baum M.J., and Bakker J. Enhanced urinary odor discrimination in female aromatase knockout (ArKO) mice. Horm. Behav. 49 (2006) 580-586
Whitney G., Cable J.R., Stockton M.D., and Tilson E.F. Ultrasonic emissions: do they facilitate courtship of mice?. J. Comp. Physiol. Psychol. 84 (1973) 445-452
Wimersma Greidanus T.B. Disturbed behavior and memory of the Brattleboro rat. Ann. N.Y. Acad. Sci. 394 (1982) 655-662
Wimersma Greidanus T.B., van Ree J.M., and de Wied D. Vasopressin and memory. Pharmacol. Ther. 20 (1983) 437-458
