An enriched rearing environment calms adult male rat sexual activity: Implication for distinct serotonergic and hormonal responses to females

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Urakawa, Susumu ^a,b   Mitsushima, Dai ^c   Shimozuru, Michito ^d,e   Sakuma, Yasuo ^a   Kondo, Yasuhiko ^a,f  

^a NIPPON MEDICAL SCHOOL   (Japan)

^b UNIVERSITY OF TOYAMA   (Japan)

^c YAMAGUCHI UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d HOKKAIDO UNIVERSITY   (Japan)

^e UNIVERSITY OF TOKYO   (Japan)

^f TEIKYO UNIVERSITY OF SCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOSTERONE; SEROTONIN; TESTOSTERONE;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; COPULATION; CORTICOSTERONE BLOOD LEVEL; DOPAMINERGIC TRANSMISSION; EJACULATION; EMOTIONALITY; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL FACTOR; FEMALE; HORMONAL REGULATION; HORMONE RESPONSE; LATENT PERIOD; LOCOMOTION; MALE; MOTIVATION; NONHUMAN; NUCLEUS ACCUMBENS; OPEN FIELD BEHAVIOR; RAT; REARING; RECEPTIVE FIELD; SEROTONIN BRAIN LEVEL; SEROTONINERGIC TRANSMISSION; TESTOSTERONE BLOOD LEVEL; WEANING;

ANIMALS; COPULATION; DOPAMINE; FEMALE; LOCOMOTION; MALE; MATING PREFERENCE, ANIMAL; NUCLEUS ACCUMBENS; RATS; SEROTONIN; TESTOSTERONE;

EID: 84895515858     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087911     Document Type: Article

References (61)

1. van Praag H, Kempermann G, Gage FH (2000) Neural consequences of environmental enrichment. Nat Rev Neurosci 1: 191-198.
2. Nithianantharajah J, Hannan AJ (2006) Enriched environments, experence-dependent plasticity and disorders of the nervous system. Nat Rev Neurosci 7: 697-709. (Pubitemid 44267494)
3. Sale A, Berardi N, Maffei L (2009) Enrich the environment to empower the brain. Trends Neurosci 32: 233-239.
4. Ohlsson AL, Johansson BB (1995) Environmental influences functional outcome of cerebral infarction in rats. Stroke 26: 644-649.
5. Urakawa S, Hida H, Masuda T, Misumi S, Kim TS, et al. (2007) Environmental enrichment brings a beneficial effect on beam walking and enhances the migration of doublecortin-positive cells following striatal lesions in rats. Neurosci 144: 920-933. (Pubitemid 46013998)
6. Moser MB, Trommald M, Egeland T, Andersen P (1997) Spatial training in a complex environment and isolation alter the spine distribution differently in rat CA 1 pyramidal cells. J Comp Neurol 380: 373-381. (Pubitemid 27161327)
7. Schrijver NC, Bahr NI, Weiss IC, Würbel H (2002) Dissociable effects of isolation rearing and environmental enrichment on exploration, spatial learning and HPA activity in adult rats. Pharmacol Biochem Behav 73: 209-224. (Pubitemid 34667033)
8. Chapillon P, Manneche C, Belzung C, Caston J (1999) Rearing environmental enrichment in two inbred strains of mice: 1. Effects on emotional reactivity. Behav Genet 29: 41-46. (Pubitemid 29265765)
9. Roy V, Belzung C, Delarue C, Chapillon P (2001) Environmental enrichment in BALB/c mice: effects in classical tests of anxiety and exposure to a predatory odor. Physiol Behav 74: 313-320. (Pubitemid 33070404)
10. Benaroya-Milshtein N, Hollander N, Apter A, Kukulansky T, Raz N, et al. (2004) Environmental enrichment in mice decreases anxiety, attenuates stress responses and enhances natural killer cell activity. Eur J Neurosci 20: 1341-1347. (Pubitemid 39236447)
11. Urakawa S, Takamoto K, Hori E, Sakai N, Ono T, et al. (2013) Rearing in enriched environment increases parvalbumin-positive small neurons in the amygdala and decreases anxiety-like behavior of male rats. BMC Neurosci 14:13.
12. Valzelli L (1973) Isolation syndrome in mice. Psychopharmacologia 31: 305-320.
13. Panksepp J (1981) The ontogeny of play in rats. Dev Psychobiol 14: 327-332.
14. Varlinskaya E, Spear L, Spear N (1999) Social behavior and social motivation in adolescent rats: role of housing conditions and partner's activity. Physiol Behav 67: 475-482. (Pubitemid 29488525)
15. Kalnichev M, Easterling KW, Plotsky PM, Holtzman SG (2002) Long-lasting changes in stress-induced corticosterone response and anxiety-like behaviors as a consequence of neonatal maternal separation in Long-Evans rats. Pharmacol Biochem Behav 73: 131-140. (Pubitemid 34667025)
16. Veenema AH, Blume A, Beiderbeck DI, Neumann ID (2006) Effects of early life stress on adult male aggression and hypothalamic vasopressin and serotonin. Eur J Neurosci 24: 1711-1720. (Pubitemid 44427540)
17. Neugebauer NM, Chunningham T, Zhu J, Bryant RI, Middleton LS, et al. (2004) Effects of environmental enrichment on behavior and dopamine transporter function in medial prefrontal cortex in adult rats prenatally treated with cocaine. Dev Brain Res 153: 213-223. (Pubitemid 39441037)
18. Magalhães A, Summavielle T, Tavares MA, De Sousa L (2007) Postnatal exposure to cocaine in rats housed in an enriched environment: effects on social interactions. Human Exp Toxicol 26: 303-309.
19. Lowry CA, Hale MW, Evans AK, Heerkens J, Staub DR, et al. (2008) Serotonergic systems, anxiety, and affective disorder: focus on the dorsomedial part of the dorsal raphe nucleus. Ann N Y Acad Sci 1148:86-94.
20. Dell'Osso B, Buoli M, Baldwin DS, Altamura AC (2010) Serotonin norepinephrine reuptake inhibitors (SNRIs) in anxiety disorders: a comprehensive review of their clinical efficacy. Hum Psychopharmacol 25:17-29.
21. Wise RA (2004) Dopamine, learning and motivation. Nat Rev Neurosci 5:483-494.
22. Belz EE, Kennell JS, Czambel RK, Rubin RT, Rhodes ME (2003) Environmental enrichment lowers stress-responsive hormones in singly housed male and female rats. Pharmacol Biochem Behav 76:481-486. (Pubitemid 37487904)
23. Giuliano F, Allard J (2001) Dopamine and male sexual function. Eur Urol 40: 601-608. (Pubitemid 34102525)
24. de Jong TR, Veening JG, Waldinger MD, Cools AR, Olivier B (2006) Serotonin and neurobiology of the ejaculatory threshold. Neurosci Biobehav Rev 30: 893-907.
25. Hull EM, Dominguez JM (2007) Sexual behavior in male rodents. Horm Behav 27: 2837-2845.
26. Kamel F, Mock EJ, Wright W, Frankel AI (1975) Alterations in plasma concentrations of testosterone, LH, and prolactin associated with mating in the male rat. Horm Behav 6: 277-288.
27. Bonilla-Jaime H, Vázquez-Palacios G., Arteaga-Silva M, Retana-Márquez S (2006) Hormonal responses to different sexually related conditions in male rats. Horm Behav 49: 376-382. (Pubitemid 43239606)
28. Kondo Y, Sachs BD, Sakuma Y (1997) Importance of the medial amygdala in rat penile erection evoked by remote stimuli from estrus females. Behav Brain Res 88: 153-160. (Pubitemid 27496312)
29. López HH, Olster DH, Ettenberg A (1999) Sexual motivation in the male rat: the role of primary incentives and copulatory experience. Horm Behav 36: 176-185. (Pubitemid 29480876)
30. Ahn S, Phillips AG (1999) Dopaminergic correlates of sensory-specific satiety in the medial prefrontal cortex and nucleus accumbens of the rat. J Neurosci 19:RC29: 1-6.
31. Mitsushima D, Yamada K, Takase K, Funabashi T, Kimura F (2006) Sex differences in the basolateral amygdala: the extracellular levels of serotonin and dopamine, and their responses to restraint stress in rats. Eur J Neurosci 24: 3245-354.
32. Fiorino DF, Coury A, Phillips AG (1997) Dynamic changes in nucleus accumbens dopamine efflux during the Coolidge effect in male rats. J Neurosci 17: 4849-4855. (Pubitemid 27246940)
33. Paxinos G, Watson C (1986) The Rat Brain in Stereotaxic Coordinates, 2nd Edn. Academic Press, London.
34. Shimozuru M, Kikusui T, Takeuchi Y, Mori Y (2006) Scent-marking and sexual activity may reflect social hierarchy among group-living male Mongolian gerbils (Meriones unguiculatus). Phisiol Behav 89: 644-649.
35. Swanson HH, Mcconnell P, Uylings HBM, van Oyen HG, van de Poll NE (1983a) Interaction between pre-weaning undernutrition and post-weaning environmental enrichment on somatic development and behavior in male and female rats. Behav Proc 8: 1-20.
36. Swanson HH, van de Poll NE (1983b) Effects of an isolated or enriched environment after handling on sexual maturation and behavior in male and female rats. J Reprod Fert 69: 165-171.
37. Zimmermann A, Stauffacher M, Langhans W, Würbel H (2001) Enrichment-dependent differences in novelty exploration in rats can be explain by habituation. Behav Brain Res 121: 11-20. (Pubitemid 32220132)
38. Pietropaolo S, Branchi I, Cirulli F, Chiarotti F, Aloe L, et al. (2004) Long-term effects of the periadolescent environment on exploratory activity and aggressive behaviour in mice: social versus physical enrichment. Physiol Behav 81: 443-453. (Pubitemid 38591533)
39. Brenes JC, Padilla M, Fornaguera J (2009) A detailed analysis of open-field habituation and behavioral and neurochemical antidepressant-like effects in postweaning enriched rats. Behav Brain Res 197: 125-137.
40. Fernández-Teruel A, Escorihuela RM, Castellano B, González B, Tobeña A (1997) Neonatal handling and environmental enrichment effects on emotionality, novelty/reward seeking, and age-related cognitive and hippocampal impairments: focus on Roman rat lines. Behav Genet 27: 513-526.
41. Baldini S, Restani L, Baroncelli L, Coltelli M, Franco R, et al. (2013) Enriched early life experiences reduce adult anxiety-like behavior in rats: a role for insulin-like growth factor 1. J Neurosci 33:11715-11723.
42. Fernández-Teruel A, Driscoll P, Gil L, Aguilar R, Tobeña A, et al. (2002) Enduring effects of environmental enrichment on novelty seeking, saccharin and ethanol intake in two rat lines (RHA/Verh and RLA/Verh) differing in incentive-seeking behavior. Pharmcol Biochem Behav 73: 225-231. (Pubitemid 34667034)
43. Martínez-Cué C, Baamonde C, Lumbreras M, Paz J, Davisson T, et al. (2002) Differential effects of environmental enrichment on behavioral and learning of male and female Ts65Dn mice, a model for Down syndrome. Behav Brain Res 134: 185-200. (Pubitemid 34912698)
44. Barfield RJ, Sachs BD (1968) Sexual behavior: stimulation by painful electrical schock to skin in male rats. Science 161: 392-393.
45. Fernández-Guasti A, Roldán-Roldán G, Saldívar A (1990) Pharmacological manipulation of anxiety and male rat sexual behavior. Pharm Biochem Behavi 35:263-267.
46. Morley-Fletcher S, Rea M, Maccari S, Laviola G (2003) Environmental enrichment during adolescence reverses the effects of prenatal stress on play behaviour and HPA axis reactivity in rats. Eur J Neurosci 18: 3367-3374. (Pubitemid 38031062)
47. Inoue T, Tsuchiya K, Koyama T (1994) Regional changes in dopamine and 5-hydroxytryptamine activation with various intensity of physical and psychological stress in rat brain. Pharmacol Biochem Behav 49: 911-920. (Pubitemid 24376030)
48. Rueter LE, Jacobs BL (1996) A microdialysis examination of serotonin release in the rat forebrain induced by behavioral/environmental manipulation. Brain Res 739: 57-69. (Pubitemid 26387363)
49. Giuliano F (2007) 5-hydroxytryptamine in premature ejaculation: opportunities for therapeutic intervention. Trends Neurosci 30: 79-84.
50. Patel K, Hellstrom WJ (2009) Central regulation of ejaculation and the therapeutic role of serotonergic agents in premature ejaculation. Curr Opin Investig Drugs 10: 681-690.
51. Everitt BJ (1990) Sexual motivation: a neural and behavioural analysis of the mechanisms underlying appetitive and copulatory responses of male rats. Neurosci Biobehav Rev 14: 217-232.
52. Melis MR, Argiolas A (1995) Dopamine and sexual behavior. Neurosci Biobehav Rev 19: 19-38.
53. Rasmuson S, Olsson T, Henriksson BG, Kelly PAT, Holmes MC, et al. (1998) Environmental enrichment selectively increases 5-HT1A receptor mRNA expression and binding in the rat hippocampus. Brain Res Mol Brain Res 53: 285-290. (Pubitemid 28085464)
54. MacGillivray L, Reynolds KB, Rosebush PI, Mazurek MF (2012) The comparative effects of environmental enrichment with exercise and serotonin transporter blockade on serotonergic neurons in the dorsal raphe nucleus. Synapse 66: 465-470.
55. Greenwood BN, Foley TE, Day HEW, Campisi J, Hammack SH, et al. (2003) Freewheel running prevents learned helplessness/behavioral depression: role of dorsal raphe serotonergic neurons. J Neurosci 23: 2889-2898. (Pubitemid 36418625)
56. Greenwood BN, Foley TE, Day HEW, Burhans D, Brooks L, et al. (2005) Wheel running alters serotonin (5-HT) transporter, 5-HT1A, 5-HT1B, and alpha1b-adrenergic receptor mRNA in the rat raphe nuclei. Biol Psychiatry 57: 559-568. (Pubitemid 40311992)
57. Robbins TW, Everitt BJ (1996) Neurobehavioural mechanisms of reward and motivation. Curr Opin Neurobiol 6: 228-36. (Pubitemid 26168482)
58. Kelley AE (1999) Functional specificity of ventral striatal compartments in appetitive behaviors. Ann N Y Acad Sci 877: 71-90.
59. Barrot M, Olivier JD, Perrotti LI, DiLeone RJ, Berton O, et al. (2002) CREB activity in the nucleus accumbens shell controls gating of behavioral responses to emotional stimuli. Proc Natl Acad Sci U S A 99: 11435-11440. (Pubitemid 34920943)
60. Barrot M, Wallace DL, Bolaños CA, Graham DL, et al. (2005) Regulation of anxiety and initiation of sexual behavior by CREB in the nucleus accumbens. Proc Natl Acad Sci U S A 102: 8357-8362. (Pubitemid 40800093)
61. Matsumoto J, Urakawa S, Hori E, de Araujo MF, Sakuma Y, et al. (2012) Neuronal responses in the nucleus accumbens shell during sexual behavior in male rats. J Neurosci 32: 1672-1686.