Effects of developmental hyperserotonemia on juvenile play behavior, oxytocin and serotonin receptor expression in the hypothalamus are age and sex dependent

Physiology and Behavior

Volumn 128, Issue , 2014, Pages 260-269

  Madden, Amanda M K ^a   Zup, Susan L ^a  

^a UNIVERSITY OF MASSACHUSETTS BOSTON   (United States)

Author keywords

Autism; Hypothalamus; Juvenile play behavior; Oxytocin; Serotonin receptor; Sex difference

Indexed keywords

5 METHOXYTRYPTAMINE; OXYTOCIN; SEROTONIN 1A RECEPTOR; SEROTONIN 2A RECEPTOR; OXYTOCIN RECEPTOR; SEROTONIN; SEROTONIN RECEPTOR;

AGE; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR CHANGE; BRAIN NUCLEUS; CELL COUNT; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; DEVELOPMENTAL HYPERSEROTONEMIA; FEMALE; HYPOTHALAMUS; JUVENILE; LOCOMOTION; MALE; MEDIAL PARAVENTRICULAR NUCLEUS; NONHUMAN; PERINATAL DEVELOPMENT; PERINATAL PERIOD; PLAY; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SEROTONIN BLOOD LEVEL; SEX DIFFERENCE; SOCIAL BEHAVIOR; ANIMAL; ANIMAL BEHAVIOR; BIOSYNTHESIS; BLOOD; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; METABOLISM; PHYSIOLOGY; RECREATION; SPRAGUE DAWLEY RAT;

AGE FACTORS; ANIMALS; BEHAVIOR, ANIMAL; FEMALE; HYPOTHALAMUS; MALE; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PLAY AND PLAYTHINGS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, SEROTONIN, 5-HT2A; RECEPTORS, OXYTOCIN; RECEPTORS, SEROTONIN; SEROTONIN; SEX FACTORS;

EID: 84896876048     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2014.01.036     Document Type: Article

References (88)

1. Lauder J.M. Ontogeny of the serotonergic system in the rat: serotonin as a developmental signal. Ann N Y Acad Sci 1990, 600:297-313.
2. Sodhi M.S., Sanders-Bush E. Serotonin and brain development. Int Rev Neurobiol 2004, 59:111-174.
3. McNamara I.M., Borella A.W., Bialowas L.A., Whitaker-Azmitia P.M. Further studies in the developmental hyperserotonemia model (DHS) of autism: social, behavioral and peptide changes. Brain Res 2008, 1189:203-214.
4. Pino G.D., Moessner R., Lesch K.P., Lauder J.M., Persico A.M. Roles for serotonin in neurodevelopment: more than just neural transmission. Curr Neuropharmacol 2013, 2:403-417.
5. Fricker A.D., Rios C., Devi L.A., Gomes I. Serotonin receptor activation leads to neurite outgrowth and neuronal survival. Mol Brain Res 2005, 138:228-235.
6. Kesterson K.L., Lane R.D., Rhoades R.W. Effects of elevated serotonin levels on patterns of GAP-43 expression during barrel development in rat somatosensory cortex. Dev Brain Res 2002, 139:167-174.
7. Mazer C., Muneyyirci J., Taheny K., Raio N., Borella A.W., Whitaker-Azmitia P.M. Serotonin depletion during synaptogenesis leads to decreased synaptic density and learning deficits in the adult rat: a possible model of neurodevelopmental disorders with cognitive deficits. Brain Res 1997, 760:68-73.
8. Lauder J.M., Wallace J.A., Wilkie M.B., DiNome A., Krebs H. Roles for serotonin in neurogenesis. Monogr Neural Sci 1983, 9:3-10.
9. Lauder J.M., Krebs H. Serotonin as a differentiation signal in early neurogenesis. Dev Neurosci 1978, 1:15-30.
10. Zup S.L., Forger N.G. Hormones and sexual differentiation. Encyclopedia of the human brain 2002, vol. 4:323-341. Elsevier Science.
11. Forger N.G. Control of cell number in the sexually dimorphic brain and spinal cord. J Neuroendocrinol 2009, 21:393-399.
12. Cooke B., Hegstrom C.D., Villeneuve L.S., Breedlove S.M. Sexual differentiation of the vertebrate brain: principles and mechanisms. Front Neuroendocrinol 1998, 19:323-362.
13. Ladosky W., Gaziri L.C. Brain serotonin and sexual differentiation of the nervous system. Neuroendocrinology 1970, 6:168-174.
14. Giulian D., Pohorecky L.A., McEwen B.S. Effects of gonadal steroids upon brain 5-hydroxytryptamine levels in the neonatal rat. Endocrinology 1973, 93:1329-1335.
15. Wilson C.A., Pearson J.R., Hunter A.J., Tuohy P.A., Payne A.P. The effect of neonatal manipulation of hypothalamic serotonin activity in the adult rat. Biochem Behav 1986, 24:1175-1183.
16. Gonzalez M.I., Albonetti M.E., Siddiqui A., Farabollini F., Wilson C.A. Neonatal organizational effects of the 5-HT2, and 5-HT1A subsystems on adult behavior in the rat. Pharmacol Biochem Behav 1996, 54:195-203.
17. Murray J.F., Dakin C.L., Siddiqui A., Pellatt L.J., Ahmed S., Ormerod L.J., et al. Neonatal 5HT activity antagonizes the masculinizing effect of testosterone on the luteinizing hormone release response to gonadal steroids and on brain structures in rats. Eur J Neurosci 2004, 19:387-395.
18. Centers for Disease Control and Prevention Prevalence of autism spectrum disorders-autism and developmental disabilities monitoring network, 14 sites, United States. MMWR 2012, 61(3):1-19.
19. Cook E.H., Leventhal B.L. The serotonin system in autism. Curr Opin Pediatr 1996, 8:348-354.
20. Anderson G.M., Horne W.C., Chatterjee D., Cohen D.J. The hyperserotonemia of autism. Ann N Y Acad Sci 1990, 600:331-340.
21. Hranilović D., Bujas-Petkovic Z., Vragovic R., Vuk T., Hock K., Jernej B. Hyperserotonemia in adults with autistic disorder. J Autism Dev Disord 2007, 37:1934-1940.
22. Bonnin A., Goeden N., Chen K., Wilson M.L., King J., Shih J.C., et al. A transient placental source of serotonin for the fetal forebrain. Nature 2011, 472:347-350.
23. Anderson G.M., Gutknecht L., Cohen D.J., Brailly-Tabard S., Cohen J.H., Ferrari P., et al. Serotonin transporter promoter variants in autism: functional effects and relationship to platelet hyperserotonemia. Mol Psychiatry 2002, 7:831-836.
24. Croen L.A. Antidepressant use during pregnancy and childhood autism spectrum disorders. Arch Gen Psychiatry 2011, 68:1104.
25. Chugani D.C., Muzik O., Behen M., Rothermel R., Janisse J.J., Lee J., et al. Developmental changes in brain serotonin synthesis capacity in autistic and nonautistic children. Ann Neurol 1999, 45:287-295.
26. Martin M.M., Liu Y., Wang Z. Developmental exposure to a serotonin agonist produces subsequent behavioral and neurochemical changes in the adult male prairie vole. Physiol Behav 2012, 105:529-535.
27. Kahne D., Tudorica A., Borella A.W., Shapiro L., Johnstone F., Huang W., et al. Behavioral and magnetic resonance spectroscopic studies in the rat hyperserotonemic model of autism. Physiol Behav 2002, 75:403-410.
28. Bagdy G. Role of the hypothalamic paraventricular nucleus in 5-HT1A, 5-HT2A and 5-HT2C receptor-mediated oxytocin, prolactin, and ACTH/corticosterone responses. Behav Brain Res 1996, 73:277-280.
29. Jorgensen H., Kjaer A., Knigge U., Mollers M., Warberg J. Serotonin stimulates hypothalamic mRNA expression and local release of neurohypophysial peptides. J Neuroendocrinol 2003, 15:564-571.
30. Zhang Y. Desensitization of 5-HT1A receptors by 5-HT2A receptors in neuroendocrine neurons in vivo. J Pharmacol Exp Ther 2004, 310:59-66.
31. Rodriguez-Porcel F., Green D., Khatri N., Swilley Harris S., May W.L., Lin R.C., et al. Neonatal exposure of rats to antidepressants affects behavioral reactions to novelty and social interactions in a manner analogous to autistic spectrum disorders. Anat Rec 2011, 294:1726-1735.
32. Simpson K.L., Weaver K.J., de Villers-Sidani E., Lu J.Y., Cai Z., Pang Y., et al. Perinatal antidepressant exposure alters cortical network function in rodents. Proc Natl Acad Sci 2011, 108:18465-18470.
33. Lidov H.G., Molliver M.E. An immunohistochemical study of serotonin neuron development in the rat: ascending pathways and terminal fields. Brain Res Bull 1982, 8:389-430.
34. Meaney M.J., Stewart J. A descriptive study of social development in the rat (Rattus novegicus). Anim Behav 1981, 29:34-45.
35. Lee V.W., De Kretser D.M., Hudson B., Wang C. Variations in serum FSH, LH and testosterone levels in male rats from birth to sexual maturity. J Reprod Fertil 1975, 42:121-126.
36. Olesen K.M., Jessen H.M., Auger C.J., Auger A.P. Dopaminergic activation of estrogen receptors in neonatal brain alters progestin receptor expression and juvenile social play behavior. Endocrinology 2005, 146:3705-3712.
37. Hoffman G.E., Le W.W., Sita L.V. The importance of titrating antibodies for immunocytochemical methods. Curr Protoc Neurosci 2008, 45:2.12.1-2.12.26.
38. Zhang J.-M., Konkle A.T., Zup S.L., McCarthy M.M. Impact of sex and hormones on new cells in the developing rat hippocampus: a novel source of sex dimorphism?. Eur J Neurosci 2008, 27:791-800.
39. Rhodes C.H., Morrell J.I., Pfaff D.W. Immunohistochemical analysis of magnocellular elements in rat hypothalamus: distribution and numbers of cells containing neurophysin, oxytocin, and vasopressin. J Comp Neurol 1981, 198:45-64.
40. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 2007, Academic Press. 6 ed.
41. Auger A.P., Olesen K.M. Brain sex differences and the organisation of juvenile social play behaviour. J Neuroendocrinol 2009, 21:519-525.
42. Dakin C.L., Wilson C.A., Kalló I., Coen C.W., Davies D.C. Neonatal stimulation of 5-HT 2receptors reduces androgen receptor expression in the rat anteroventral periventricular nucleus and sexually dimorphic preoptic area. Eur J Neurosci 2008, 27:2473-2480.
43. Janušonis S., Anderson G.M., Shifrovich I., Rakic P. Ontogeny of brain and blood serotonin levels in 5-HT 1A receptor knockout mice: potential relevance to the neurobiology of autism. J Neurochem 2006, 99:1019-1031.
44. Filip M., Bader M. Overview on 5-HT receptors and their role in physiology and pathology of the central nervous system. Pharmacol Rep 2009, 61:761-777.
45. Patel T.D., Zhou F.C. Ontogeny of 5-HT1A receptor expression in the developing hippocampus. Dev Brain Res 2005, 157:42-57.
46. Lauder J.M. Ontogeny of neurotransmitter systems: substrates for developmental disabilities?. Ment Retard Dev Disabil Res Rev 1995, 1:151-168.
47. Whitaker-Azmitia P.M. Serotonin and brain development: role in human developmental diseases. Brain Res Bull 2001, 56:479-485.
48. Li Q.-H., Nakadate K., Tanaka-Nakadate S., Nakatsuka D., Cui Y., Watanabe Y. Unique expression patterns of 5-HT2A and 5-HT2C receptors in the rat brain during postnatal development: Western blot and immunohistochemical analyses. J Comp Neurol 2004, 469:128-140.
49. Nuñez J.L., McCarthy M.M. Evidence for an extended duration of GABA-mediated excitation in the developing male versus female hippocampus. Dev Neurosci 2007, 67:1879-1890.
50. Nuñez J.L., McCarthy M.M. Androgens predispose males to GABAA-mediated excitotoxicity in the developing hippocampus. Exp Neurol 2008, 210:699-708.
51. Konishi M., Akutagawa E. Neuronal growth, atrophy and death in a sexually dimorphic song nucleus in the zebra finch brain. Nature 1985, 315:145-147.
52. Mooney R., Rao M. Waiting periods versus early innervation: the development of axonal connections in the zebra finch song system. J Neurosci 1994, 14:6532-6543.
53. Herrmann K., Arnold A.P. Lesions of HVc block the developmental masculinizing effects of estradiol in the female zebra finch song system. J Neurobiol 1991, 22:29-39.
54. Shatz C.J., Ghosh A., McConnell S.K., Allendoerfer K.L., Friauf E., Antonini A. Pioneer neurons and target selection in cerebral cortical development. Cold Spring Harb Symp Quant Biol 1990, 55:469-480.
55. Allendoerfer K.L., Shatz C.J. The subplate, a transient neocortical structure: its role in the development of connections between thalamus and cortex. Annu Rev Neurosci 1994, 17:185-218.
56. Supèr H., Martínez A., Del Río J.A., Soriano E. Involvement of distinct pioneer neurons in the formation of layer-specific connections in the hippocampus. J Neurosci 1998, 18:4616-4626.
57. Aujla P.K., Bora A., Monahan P., Sweedler J.V., Raetzman L.T. Dev Biol 2011, 353:61-71.
58. Li Q., Wichems C., Heils A., Lesch K.P., Murphy D.L. Reduction in the density and expression, but not G-protein coupling, of serotonin receptors (5-HT1A) in 5-HT transporter knock-out mice: gender and brain region differences. J Neurosci 2000, 20:7888-7895.
59. Whitaker-Azmitia P.M., Azmitia E.C. Autoregulation of fetal serotonergic neuronal development: role of high affinity serotonin receptors. Neurosci Lett 1986, 67:307-312.
60. Whitaker-Azmitia P.M., Druse M., Walker P., Lauder J.M. Serotonin as a developmental signal. Behav Brain Res 1996, 73:19-29.
61. Wilson C.A., Gonzalez M.I., Albonetti M.E., Farabollini F. The involvement of neonatal 5HT receptor mediated effects on sexual dimorphism of adult behavior in the rat. Males, females, and behavior; toward biological understanding 1998, 109-127.
62. Wilson C.A., Dakin C.L., Rico J.A., Golmohamad A., Ahmad-Jauhari Y., Davies D.C. The anti-dopaminergic agent, haloperidol, antagonises the feminising effect of neonatal serotonin on sexually dimorphic hypothalamic nuclei and tyrosine hydroxylase immunoreactive neurones. J Neuroendocrinol 2009, 21:648-656.
63. Hollander E., Novotny S., Hanratty M., Yaffe R., DeCaria C.M., Aronowitz B.R., et al. Oxytocin infusion reduces repetitive behaviors in adults with autistic and Asperger's disorders. Neuropsychopharmacology 2003, 28:193-198.
64. Hollander E., Bartz J., Chaplin W., Phillips A., Sumner J., Soorya L., et al. Oxytocin increases retention of social cognition in autism. Biol Psychiatry 2007, 61:498-503.
65. Guastella A.J., Einfeld S.L., Gray K.M., Rinehart N.J., Tonge B.J., Lambert T.J., et al. Intranasal oxytocin improves emotion recognition for youth with autism spectrum disorders. Biol Psychiatry 2010, 67:692-694.
66. de Vries G.J. Minireview: sex differences in adult and developing brains: compensation, compensation, compensation. Endocrinology 2004, 145:1063-1068.
67. Armstrong W.E., Warach S., Hatton G.I., McNeill T.H. Subnuclei in the rat hypothalamic paraventricular nucleus: a cytoarchitectural, HRP, and immunocytochemical analysis. Neuroscience 1980, 5:1931-1958.
68. Hosoya Y., Matsushita M. Identification and distribution of the spinal and hypophyseal projection neurons in the paraventricular nucleus of the rat. A light and electron microscopic study with the horseradish peroxidase method. Exp Brain Res 1979, 35:315-331.
69. Buijs R.M., Velis D.N., Swaab D.F. Extrahypothalamic vasopressin and oxytocin innervation of fetal and adult rat brain. Prog Brain Res 1980, 53:159-167.
70. Vanderschuren L.J., Niesink R.J., Van Ree J.M. The neurobiology of social play behavior in rats. Neurosci Biobehav Rev 1997, 21:309-326.
71. Veenema A.H., Bredewold R., De Vries G.J. Sex-specific modulation of juvenile social play by vasopressin. Psychoneuroendocrinology 2013, 38:2554-2561.
72. Pellis S.M., Field E.F., Smith L.K., Pellis V.C. Multiple differences in the play fighting of male and female rats. Implications for the causes and functions. Neurosci Biobehav Rev 1997, 21:105-120.
73. Panksepp J. Social deprivation and play in rats. Behav Neural Biol 1980, 30:197-206.
74. Siviy S.M., Deron L.M., Kasten C.R. Serotonin, motivation, and playfulness in the juvenile rat. Dev Cogn Neurosci 2011, 1:606-616.
75. Pellis S.M., Pellis V.C. Differential rates of attack, defense, and counterattack during the developmental decrease in play fighting by male and female rats. Dev Psychobiol 1990, 23:215-231.
76. Pellis S.M., McKenna M. What do rats find rewarding in play fighting?-an analysis using drug-induced non-playful partners. Behav Brain Res 1995, 68:65-73.
77. Homberg J.R., Schiepers O.J., Schoffelmeer A.N., Cuppen E., Vanderschuren L.J. Acute and constitutive increases in central serotonin levels reduce social play behaviour in peri-adolescent rats. Psychopharmacology (Berl) 2007, 195:175-182.
78. Pellis S.M., Pellis V.C., McKenna M.M. Feminine dimension in the play fighting of rats. J Comp Psychol 1994, 108:68-73.
79. Cirulli F., Terranova M.L., Laviola G. Affiliation in periadolescent rats: behavioral and corticosterone response to social reunion with familiar or unfamiliar partners. Pharmacol Biochem Behav 1996, 54:99-105.
80. Paul M.J., Murray E.K., Ismail N.I., Kim A.M., Shah C.R., Probst C.K., de Vries G.J. Possible role for vasopressin in the regulation of sex differences in play behavior [Abstract 28]. 2013 World Congress on Neurohypophyseal Hormones 2013, Programs & Abstracts, Bristol, England.
81. Xu H., Qin S., Carrasco G.A., Dai Y., Filardo E.J., Prossnitz E.R., et al. Extra-nuclear estrogen receptor GPR30 regulates serotonin function in rat hypothalamus. Neuroscience 2009, 158:1599-1607.
82. Sumner B.E., Grant K.E., Rosie R., Hegele-Hartung C., Fritzemeier K.-H., Fink G. Effects of tamoxifen on serotonin transporter and 5-hydroxytryptamine2A receptor binding sites and mRNA levels in the brain of ovariectomized rats with or without acute estradiol replacement. Mol Brain Res 1999, 73:119-128.
83. Osterlund M.K., Halldin C., Hurd Y.L. Effects of chronic 17β-estradiol treatment on the serotonin 5-HT1A receptor mRNA and binding levels in the rat brain. Synapse 2000, 35:39-44.
84. Alves S.E., Lopez V., McEwen B.S., Weiland N.G. Differential colocalization of estrogen receptor B (ERB) with oxytocin and vasopressin in the paraventricular and supraoptic nuclei of the female rat brain: an immunocytochemical study. Proc Natl Acad Sci 1998, 95:3281-3286.
85. Osterlund M.K., Hurd Y.L. Acute 17β-estradiol treatment down-regulates serotonin 5HT1A receptor mRNA expression in the limbic system of female rats. Mol Brain Res 1998, 55:169-172.
86. Fink G., Sumner B., Rosie R., Wilson H., McQueen J. Androgen actions on central serotonin neurotransmission: relevance for mood, mental state and memory. Behav Brain Res 1999, 105:53-68.
87. Biegon A., McEwen B.S. Modulation by estradiol of serotonin1 receptors in brain. J Neurosci 1982, 2:199-205.
88. Rubinow D.R., Schmidt P.J., Roca C.A. Estrogen-serotonin interactions: implications for affective regulation. Biol Psychiatry 1998, 44:839-850.