An Enriched Rearing Environment Calms Adult Male Rat Sexual Activity: Implication for Distinct Serotonergic and Hormonal Responses to Females

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2014 Feb 8

PMID 24505330

Citations 7

Authors

Susumu Urakawa

Dai Mitsushima

Michito Shimozuru

Yasuo Sakuma

Yasuhiko Kondo

Affiliations

Soon will be listed here.

Abstract

Early life events induce alterations in neural function in adulthood. Although rearing in an enriched environment (EE) has a great impact on behavioral development, the effects of enriched rearing on sociosexual behavior remain unclear. In this study, we investigated the effects of rearing in an EE on male copulatory behavior and its underlying neurobiological mechanisms in Wistar-Imamichi rats. Three-week-old, recently weaned rats were continuously subjected to a standard environment (SE) or an EE comprised of a large cage with several objects, such as toys, tunnels, ladders, and a running wheel. After 6 weeks, rats reared in an EE (EE rats) showed decreased sexual activity compared with rats reared in a SE (SE rats). This included a lower number of ejaculations and longer latencies in three consecutive copulatory tests. In addition, EE rats showed decreased emotional responsiveness and less locomotor behavior in an open field. In a runway test, on the other hand, sexual motivation toward receptive females in EE males was comparable to that of SE males. Furthermore, following exposure to a female, increases in serotonin levels in the nucleus accumbens and the striatum were significantly suppressed in EE males, whereas dopaminergic responses were similar between the groups. Female-exposure-induced increases in the levels of plasma corticosterone and testosterone were also suppressed in EE rats compared to SE rats. These data suggest that rearing in an EE decreases male copulatory behavior, and serotonin and hormonal regulating systems may regulate the differences in sociosexual interactions that result from distinct rearing environments.

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References

Chapillon P, Manneche C, Belzung C, Caston J . Rearing environmental enrichment in two inbred strains of mice: 1. Effects on emotional reactivity. Behav Genet. 1999; 29(1):41-6. DOI: 10.1023/a:1021437905913. View

Barrot M, Wallace D, Bolanos C, Graham D, Perrotti L, Neve R . Regulation of anxiety and initiation of sexual behavior by CREB in the nucleus accumbens. Proc Natl Acad Sci U S A. 2005; 102(23):8357-62. PMC: 1149417. DOI: 10.1073/pnas.0500587102. View

Giuliano F, Allard J . Dopamine and male sexual function. Eur Urol. 2002; 40(6):601-8. DOI: 10.1159/000049844. View

Barrot M, Olivier J, Perrotti L, DiLeone R, Berton O, Eisch A . CREB activity in the nucleus accumbens shell controls gating of behavioral responses to emotional stimuli. Proc Natl Acad Sci U S A. 2002; 99(17):11435-40. PMC: 123274. DOI: 10.1073/pnas.172091899. View

Lopez H, Olster D, Ettenberg A . Sexual motivation in the male rat: the role of primary incentives and copulatory experience. Horm Behav. 1999; 36(2):176-85. DOI: 10.1006/hbeh.1999.1535. View

Mitsushima D, Yamada K, Takase K, Funabashi T, Kimura F . Sex differences in the basolateral amygdala: the extracellular levels of serotonin and dopamine, and their responses to restraint stress in rats. Eur J Neurosci. 2006; 24(11):3245-54. DOI: 10.1111/j.1460-9568.2006.05214.x. View

Urakawa S, Hida H, Masuda T, Misumi S, Kim T, Nishino H . Environmental enrichment brings a beneficial effect on beam walking and enhances the migration of doublecortin-positive cells following striatal lesions in rats. Neuroscience. 2006; 144(3):920-33. DOI: 10.1016/j.neuroscience.2006.10.038. View

Greenwood B, Foley T, Day H, Burhans D, Brooks L, Campeau S . Wheel running alters serotonin (5-HT) transporter, 5-HT1A, 5-HT1B, and alpha 1b-adrenergic receptor mRNA in the rat raphe nuclei. Biol Psychiatry. 2005; 57(5):559-68. DOI: 10.1016/j.biopsych.2004.11.025. View

Urakawa S, Takamoto K, Hori E, Sakai N, Ono T, Nishijo H . Rearing in enriched environment increases parvalbumin-positive small neurons in the amygdala and decreases anxiety-like behavior of male rats. BMC Neurosci. 2013; 14:13. PMC: 3599335. DOI: 10.1186/1471-2202-14-13. View

10.

Rasmuson S, Olsson T, Henriksson B, Kelly P, Holmes M, Seckl J . Environmental enrichment selectively increases 5-HT1A receptor mRNA expression and binding in the rat hippocampus. Brain Res Mol Brain Res. 1998; 53(1-2):285-90. DOI: 10.1016/s0169-328x(97)00317-3. View

11.

Neugebauer N, Cunningham S, Zhu J, Bryant R, Middleton L, Dwoskin L . Effects of environmental enrichment on behavior and dopamine transporter function in medial prefrontal cortex in adult rats prenatally treated with cocaine. Brain Res Dev Brain Res. 2004; 153(2):213-23. DOI: 10.1016/j.devbrainres.2004.09.001. View

12.

Swanson H, McConnell P, Uylings H, Van Oyen H, Van de Poll N . Interaction between pre-weaning undernutrition and post-weaning environmental enrichment on somatic development and behaviour in male and female rats. Behav Processes. 2014; 8(1):1-20. DOI: 10.1016/0376-6357(83)90039-6. View

13.

Greenwood B, Foley T, Day H, Campisi J, Hammack S, Campeau S . Freewheel running prevents learned helplessness/behavioral depression: role of dorsal raphe serotonergic neurons. J Neurosci. 2003; 23(7):2889-98. PMC: 6742115. View

14.

Everitt B . Sexual motivation: a neural and behavioural analysis of the mechanisms underlying appetitive and copulatory responses of male rats. Neurosci Biobehav Rev. 1990; 14(2):217-32. DOI: 10.1016/s0149-7634(05)80222-2. View

15.

Fernandez-Teruel A, Escorihuela R, Castellano B, Gonzalez B, Tobena A . Neonatal handling and environmental enrichment effects on emotionality, novelty/reward seeking, and age-related cognitive and hippocampal impairments: focus on the Roman rat lines. Behav Genet. 1998; 27(6):513-26. DOI: 10.1023/a:1021400830503. View

16.

Pietropaolo S, Branchi I, Cirulli F, Chiarotti F, Aloe L, Alleva E . Long-term effects of the periadolescent environment on exploratory activity and aggressive behaviour in mice: social versus physical enrichment. Physiol Behav. 2004; 81(3):443-53. DOI: 10.1016/j.physbeh.2004.02.022. View

17.

Hull E, Dominguez J . Sexual behavior in male rodents. Horm Behav. 2007; 52(1):45-55. PMC: 1952538. DOI: 10.1016/j.yhbeh.2007.03.030. View

18.

Roy V, Belzung C, Delarue C, Chapillon P . Environmental enrichment in BALB/c mice: effects in classical tests of anxiety and exposure to a predatory odor. Physiol Behav. 2001; 74(3):313-20. DOI: 10.1016/s0031-9384(01)00561-3. View

19.

Zimmermann A, Stauffacher M, Langhans W, Wurbel H . Enrichment-dependent differences in novelty exploration in rats can be explained by habituation. Behav Brain Res. 2001; 121(1-2):11-20. DOI: 10.1016/s0166-4328(00)00377-6. View

20.

Fernandez-Guasti A, Roldan-Roldan G, Saldivar A . Pharmacological manipulation of anxiety and male rat sexual behavior. Pharmacol Biochem Behav. 1990; 35(1):263-7. DOI: 10.1016/0091-3057(90)90237-c. View