Developmental exposure to a serotonin agonist produces subsequent behavioral and neurochemical changes in the adult male prairie vole

Physiology and Behavior

Volumn 105, Issue 2, 2012, Pages 529-535

  Martin, Melissa M ^a   Liu, Yan ^a   Wang, Zuoxin ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

Author keywords

Anxiety; Autism; Oxytocin; Serotonin; Social affiliation; Vasopressin

Indexed keywords

5 METHOXYTRYPTAMINE; NEUROTRANSMITTER; OXYTOCIN RECEPTOR; VASOPRESSIN RECEPTOR;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; AUTISM; BEHAVIOR CHANGE; BRAIN; CONTROLLED STUDY; FETUS; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; MALE; NONHUMAN; PRENATAL EXPOSURE; PRIORITY JOURNAL; VOLE;

5-METHOXYTRYPTAMINE; ANIMALS; ARGININE VASOPRESSIN; ARVICOLINAE; BEHAVIOR, ANIMAL; BRAIN; EXPLORATORY BEHAVIOR; FEMALE; MALE; MAZE LEARNING; NEUROCHEMISTRY; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SEROTONIN; SEROTONIN RECEPTOR AGONISTS; SOCIAL BEHAVIOR;

EID: 80053919893     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2011.09.015     Document Type: Article

References (70)

1. American Psychiatric Association Task Force on DSM-IV. Diagnostic and statistical manual of mental disorders: DSM-IV 1994, American Psychiatric Association, Washington, DC. 4th ed.
2. Ansorge M.S., Zhou M., Lira A., Hen R., Gingrich J.A. Early-life blockade of the 5-HT transporter alters emotional behavior in adult mice. Science 2004, 306:879-881.
3. Brune C.W., Kim S.-J., Salt J., Leventhal B.L., Lord C., Cook E.H. 5-HTTLPR genotype-specific phenotype in children and adolescents with autism. Am J Psychiatry 2006, 163:2148-2156.
4. Whitaker-Azmitia P.M. Behavioral and cellular consequences of increasing serotonergic activity during brain development: a role in autism?. Int J Dev Neurosci 2005, 23:75-83.
5. Cook E.H., Leventhal B.L. The serotonin system in autism. Curr Opin Pediatr 1996, 8:348-354.
6. Whitaker-Azmitia P.M. Serotonin and brain development: role in human developmental diseases. Brain Res Bull 2001, 56:479-485.
7. Shemer A.V., Azmitia E.C., Whitaker-Azmitia P.M. Dose-related effects of prenatal 5-methoxytryptamine (5-MT) on development of serotonin terminal density and behavior. Dev Brain Res 1991, 59:59-63.
8. Lauder J.M., Krebs H. Effects of p-chlorophenylalanine on time of neuronal origin during embryo-genesis in the rat. Brain Res 1976, 107:638-644.
9. Boylan C.B., Blue M.E., Hohmann C.F. Modeling early cortical serotonergic deficits in autism. Behav Brain Res 2007, 176:94-108.
10. Hohmann C.F., Walker E.M., Boylan C.B., Blue M.E. Neonatal serotonin depletion alters behavioral responses to spatial change and novelty. Brain Res 2007, 1139:163-177.
11. 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.
12. Young K.A., Gobrogge K.L., Liu Y., Wang Z. The neurobiology of pair bonding: insights from a socially monogamous rodent. Front Neuroendocrin 2011, 32:53-69.
13. Winslow J.T., Hastings N., Carter C.S., Harbaugh C.R., Insel T.R. A role for central vasopressin in pair bonding in monogamous prairie voles. Nature 1993, 365:545-548.
14. Williams J., Catania K., Carter C. Development of partner preferences in female prairie voles (Microtus ochrogaster): the role of social and sexual experience. Horm Behav 1992, 26:339-349.
15. Insel T.R., Hulihan T. A gender-specific mechanism for pair bonding: oxytocin and partner preference formation in monogamous voles. Behav Neurosci 1995, 109:782-789.
16. Williams J.R., Insel T.R., Harbaugh C.R., Carter C.S. Oxytocin administered centrally facilitates formation of a partner preference in female prairie voles (Microtus ochrogaster). J Neuroendocrinol 1994, 6:247-250.
17. Young L.J., Nilsen R., Waymire K.G., MacGregor G.R., Insel T.R. Increased affiliative response to vasopressin in mice expressing the V1a receptor from a monogamous vole. Nature 1999, 400:766-768.
18. Young L.J., Wang Z. The neurobiology of pair bonding. Nat Neurosci 2004, 7:1048-1054.
19. Aragona B.J., Liu Y., Yu Y.J., Curtis J.T., Detwiler J.M., Insel T.R., et al. Nucleus accumbens dopamine differentially mediates the formation and maintenance of monogamous pair bonds. Nat Neurosci 2006, 9:133-139.
20. Villalba C., Boyle P.A., Caliguri E.J., De Vries G.J. Effects of the selective serotonin reuptake inhibitor fluoxetine on social behaviors in male and female prairie voles (Microtus ochrogaster). Horm Behav 1997, 32:184-191.
21. Rutter M. Diagnosis and definition of childhood autism. J Autism Dev Disorders 1978, 8:139-161.
22. Roberts R.L., Wolf K.N., Sprangel M.E., Rall W.F., Wildt D.E. Prolonged mating in prairie voles (Microtus ochrogaster) increases likelihood of ovulation and embryo number. Biol Reprod 1999, 60:756-762.
23. Lauder J.M. Ontogeny of the serotonergic system in the rat: serotonin as a developmental signal. Ann NY Acad Sci 1990, 600:297-313.
24. Whitaker P.M., Seeman P. High-affinity 3H-serotonin binding to caudate: Inhibition by hallucinogens and serotoninergic drugs. Psychopharmacology 1978, 59. (1-5-5).
25. Aghajanian G.K., Bloom F.E. The formation of synaptic junctions in developing rat brain: a quantitative electron microscopic study. Brain Res 1967, 6:716-727.
26. Shemer A., Whitaker-Azmitia P.M., Azmitia E.C. Effects of prenatal 5-methoxytryptamine and parachlorophenylalanine on serotonergic uptake and behavior in the neonatal rat. Pharm Biochem Behav 1988, 30:847-851.
27. Pitkow L.J., Sharer C.A., Ren X., Insel T.R., Terwilliger E.F., Young L.J. Facilitation of affiliation and pair-bond formation by vasopressin receptor gene transfer into the ventral forebrain of a monogamous vole. J Neurosci 2001, 21:7392-7396.
28. Devries A.C., Johnson C.L., Carter C.S. Familiarity and gender influence social preferences in prairie voles (Microtus ochrogaster). Can J Zool 1997, 75:295-301.
29. Pan Y., Liu Y., Young K.A., Zhang Z., Wang Z. Post-weaning social isolation alters anxiety-related behavior and neurochemical gene expression in the brain of male prairie voles. Neurosci Lett 2009, 454:67-71.
30. Witt D.M., Winslow J.T., Insel T.R. Enhanced social interactions in rats following chronic, centrally infused oxytocin. Pharmacol Biochem Behav 1992, 43:855-861.
31. Insel T.R., Preston S., Winslow J.T. Mating in the monogamous male: behavioral consequences. Physiol Behav 1995, 57:615-627.
32. Stowe J.R., Liu Y., Curtis J.T., Freeman M.E., Wang Z. Species differences in anxiety-related responses in male prairie and meadow voles: the effects of social isolation. Physiol Behav 2005, 86:369-378.
33. Gobrogge K.L., Liu Y., Jia X., Wang Z. Anterior hypothalamic neural activation and neurochemical associations with aggression in pair-bonded male prairie voles. J Comp Neurol 2007, 502:1109-1122.
34. Wang Z.X., Zhou L., Hulihan T.J., Insel T.R. Immunoreactivity of central vasopressin and oxytocin pathways in microtine rodents: a quantitative comparative study. J Comp Neurol 1996, 366:726-737.
35. Ferguson J.N., Aldag J.M., Insel T.R., Young L.J. Oxytocin in the medial amygdala is essential for social recognition in the mouse. J Neurosci 2001, 21:8278-8285.
36. Davis M. The role of the amygdala in fear and anxiety. Ann Rev 1992, ETATS-UNIS, Palo Alto, CA.
37. Neumann, Wigger, Torner, Holsboer, Landgraf Brain oxytocin inhibits basal and stress-induced activity of the hypothalamo-pituitary-adrenal axis in male and female rats: partial action within the paraventricular nucleus. J Neuroendocrinol 2000, 12:235-243.
38. Petrov T., Krukoff T.L., Jhamandas J.H. Chemically defined collateral projections from the pons to the central nucleus of the amygdala and hypothalamic paraventricular nucleus in the rat. Cell Tissue Res 1994, 277:289-295.
39. Kahne D., Tudorica A., Borella A., 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.
40. Jamain S., Radyushkin K., Hammerschmidt K., Granon S., Boretius S., Varoqueaux F., et al. Reduced social interaction and ultrasonic communication in a mouse model of monogenic heritable autism. Proc Natl Acad Sci U S A 2008, 105:1710-1715.
41. Moy S.S., Nadler J.J., Young N.B., Nonneman R.J., Grossman A.W., Murphy D.L., et al. Social approach in genetically engineered mouse lines relevant to autism. Genes Brain Behav 2009, 8:129-142.
42. Moy S.S., Nadler J.J., Young N.B., Perez A., Holloway L.P., Barbaro R.P., et al. Mouse behavioral tasks relevant to autism: phenotypes of 10 inbred strains. Behav Brain Res 2007, 176:4-20.
43. Balemans M.C.M., Huibers M.M.H., Eikelenboom N.W.D., Kuipers A.J., van Summeren R.C.J., Pijpers M.M.C.A., et al. Reduced exploration, increased anxiety, and altered social behavior: autistic-like features of euchromatin histone methyltransferase 1 heterozygous knockout mice. Behav Brain Res 2010, 208:47-55.
44. Whitaker-Azmitia P.M., Druse M., Walker P., Lauder J.M. Serotonin as a developmental signal 1995, Elsevier, Shannon, IRLANDE.
45. Whitaker-Azmitia P.M., Shemer A.V., Caruso J., Molino L., Azmitia E.C. Role of high affinity serotonin receptors in neuronal growth. Ann N Y Acad Sci 1990, 600:315-330.
46. 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.
47. Hitchcock J.M., Davis M. Efferent pathway of the amygdala involved in conditioned fear as measured with the fear-potentiated startle paradigm. Behav Neurosci 1991, 105:826-842.
48. Hitchcock J.M., Davis M. Fear-potentiated startle using an auditory conditioned stimulus: effect of lesions of the amygdala. Physiol Behav 1987, 39:403-408.
49. Wang R.Y., Aghajanian G.K. Inhibition of neurons in the amygdala by dorsal raphe stimulation: mediation through a direct serotonergic pathway. Brain Res 1977, 120:85-102.
50. Stutzmann G.E., McEwen B.S., LeDoux J.E. Serotonin modulation of sensory inputs to the lateral amygdala: dependency on corticosterone. J Neurosci 1998, 18:9529-9538.
51. Phelps E.A., O'Connor K.J., Gatenby J.C., Gore J.C., Grillon C., Davis M. Activation of the left amygdala to a cognitive representation of fear. Nat Neurosci 2001, 4:437-441.
52. Adolphs R., Tranel D., Hamann S., Young A.W., Calder A.J., Phelps E.A., et al. Recognition of facial emotion in nine individuals with bilateral amygdala damage. Neuropsychologia 1999, 37:1111-1117.
53. Birbaumer N., Grodd W., Diedrich O., Klose U., Erb M., Lotze M., et al. fMRI reveals amygdala activation to human faces in social phobics. Neuroreport 1998, 9:1223-1226.
54. Carter C.S., Williams J.R., Witt D.M., Insel T.R. Oxytocin and social bonding. Ann N Y Acad Sci 1992, 652:204-211.
55. Windle R.J., Shanks N., Lightman S.L., Ingram C.D. Central oxytocin administration reduces stress-induced corticosterone release and anxiety behavior in rats. Endocrinolgy 1997, 138:2829-2834.
56. Sofroniew M.V. Projections from vasopressin, oxytocin, and neurophysin neurons to neural targets in the rat and human. J Histochem Cytochem 1980, 28:475-478.
57. Swanson L.W., Kuypers H.G. The paraventricular nucleus of the hypothalamus: cytoarchitectonic subdivisions and organization of projections to the pituitary, dorsal vagal complex, and spinal cord as demonstrated by retrograde fluorescence double-labeling methods. J Comp Neurol 1980, 194:555-570.
58. Kramer K.M., Cushing B.S., Carter C.S. Developmental effects of oxytocin on stress response: single versus repeated exposure. Physiol Behav 2003, 79:775-782.
59. Grippo A.J., Trahanas D.M., Zimmerman Ii R.R., Porges S.W., Carter C.S. Oxytocin protects against negative behavioral and autonomic consequences of long-term social isolation. Psychoneuroendocrinology 2009, 34:1542-1553.
60. Modahl C., Green L.A., Fein D., Morris M., Waterhouse L., Feinstein C., et al. Plasma oxytocin levels in autistic children. Biol Psychiatry 1998, 43:270-277.
61. Green L.A., Fein D., Modahl C., Feinstein C., Waterhouse L., Morris M. Oxytocin and autistic disorder: alteration in peptide forms. Biol Psychiatry 2001, 50:609-613.
62. 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 2002, 28:193-198.
63. 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.
64. Wotjak C.T., Kubota M., Liebsch G., Montkowski A., Holsboer F., Neumann I., et al. Release of vasopressin within the rat paraventricular nucleus in response to emotional stress: a novel mechanism of regulating adrenocorticotropic hormone secretion?. J Neurosci 1996, 16:7725-7732.
65. Pitkow L.J. Facilitation of affiliation and pair-bond formation by vasopressin receptor gene transfer into the ventral forebrain of a monogamous vole. J Neurosci 2001, 21:7392-7396.
66. Kim S.J., Young L.J., Gonen D., Veenstra-VanderWeele J., Courchesne R., Lord C., et al. Transmission disequilibrium testing of arginine vasopressin receptor 1A (AVPR1A) polymorphisms in autism. Mol Psychiatry 2002, 7:503.
67. Wassink T.H., Piven J., Vieland V.J., Pietila J., Goedken R.J., Folstein S.E., et al. Examination of AVPR1a as an autism susceptibility gene. Mol Psychiatry 2004, 9:968-972.
68. Yirmiya N., Rosenberg C., Levi S., Salomon S., Shulman C., Nemanov L., et al. Association between the arginine vasopressin 1a receptor (AVPR1a) gene and autism in a family-based study: mediation by socialization skills. Mol Psychiatry 2006, 11:488-494.
69. Lim M.M., Bielsky I.F., Young L.J. Neuropeptides and the social brain: potential rodent models of autism. Int J Dev Neurosci 2005, 23:235-243.
70. Hammock E.A.D., Young L.J. Oxytocin, vasopressin and pair bonding: implications for autism. Philos Trans R Soc B: Biol Sci 2006, 361:2187-2198.