Prenatal stress generates deficits in rat social behavior: Reversal by oxytocin

Brain Research

Volumn 1156, Issue 1, 2007, Pages 152-167

  Lee, Paul R ^a,b   Brady, Dana L ^b   Shapiro, Robert A ^c   Dorsa, Daniel M ^c   Koenig, James I ^a,b  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b MARYLAND PSYCHIATRIC RESEARCH CENTER   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Amygdala; Hypothalamus; Oxytocin; Prenatal stress; Rat; Schizophrenia; Social interaction

Indexed keywords

MESSENGER RNA; OXYTOCIN; VASOPRESSIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; CONTROLLED STUDY; DISEASE MODEL; MALE; MATERNAL STRESS; NEGATIVE SYNDROME; NERVE CELL DIFFERENTIATION; NONHUMAN; PRENATAL EXPOSURE; PRENATAL STRESS; PRIORITY JOURNAL; PROGENY; PSYCHOSOCIAL WITHDRAWAL; RAT; RISK FACTOR; SOCIAL BEHAVIOR; SOCIAL INTERACTION; SOCIOPATHY; THALAMUS MIDLINE NUCLEUS;

AMYGDALA; ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; HYPOTHALAMUS; OXYTOCIN; PREGNANCY; PREGNANCY COMPLICATIONS; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; SCHIZOPHRENIC PSYCHOLOGY; SOCIAL BEHAVIOR; STRESS;

ANIMALIA; RATTUS;

EID: 34250315706     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2007.04.042     Document Type: Article

References (96)

1. Anderson J.E., Wible C.G., McCarley R.W., Jakab M., Kasai K., and Shenton M.E. An MRI study of temporal lobe abnormalities and negative symptoms in chronic schizophrenia. Schizophr. Res. 58 (2002) 123-134
2. Andreasen N.C., and Carpenter W.T. Diagnosis and classification of schizophrenia. Schizophr. Bull. 19 (1993) 199-214
3. Askew A., Gonzalez F.A., Stahl J.M., and Karom M.C. Food competition and social experience effects on V1a receptor binding in the forebrain of male Long-Evans hooded rats. Horm. Behav. 49 (2006) 328-336
4. Bale T.L., and Dorsa D.M. Regulation of oxytocin receptor messenger ribonucleic acid in the ventromedial hypothalamus by testosterone and its metabolites. Endocrinology 136 (1995) 5135-5138
5. Bales K.L., and Carter C.S. Sex differences and developmental effects of oxytocin on aggression and social behavior in prairie voles (Microtus ochrogaster). Horm. Behav. 44 (2003) 178-184
6. Bayer S.A., Altman J., Russo R.J., and Zhang X. Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology 14 (1993) 83-144
7. Beckmann H., Lang R.E., and Gattaz W.F. Vasopressin-oxytocin in cerebrospinal fluid of schizophrenic patients and normal controls. Psychoneuroendocrinology 10 (1985) 187-191
8. Bellack A.S., Schooler N.R., Marder S.R., Kane J.M., Brown C.H., and Yang Y. Do clozapine and risperidone affect social competence and problem solving?. Am. J. Psychiatry 161 (2004) 364-367
9. Bernstein H.G., Stanarius A., Baumann B., Henning H., Krell D., Danos P., Falkai P., and Bogerts B. Nitric oxide synthase-containing neurons in the human hypothalamus: reduced number of immunoreactive cells in the paraventricular nucleus of depressive patients and schizophrenics. Neuroscience 83 (1998) 867-875
10. Bhatnagar S., and Dallman M. Neuroanatomical basis for facilitation of hypothalamic-pituitary-adrenal responses to a novel stressor after chronic stress. Neuroscience 84 (1998) 1025-1039
11. Boksa P., and El-Khodor B.F. Birth insult interacts with stress at adulthood to alter dopaminergic function in animal models: possible implications for schizophrenia and other disorders. Neurosci. Biobehav. Rev. 27 (2003) 91-101
12. Borrell J., Vela J.M., Arevalo-Martin A., Molina-Holgado E., and Guaza C. Prenatal immune challenge disrupts sensorimotor gating in adult rats. Implications for the etiopathogenesis of schizophrenia. Neuropsychopharmacology 26 (2002) 204-215
13. Bowers G., Cullinan W.E., and Herman J.P. Region-specific regulation of glutamic acid decarboxylase (GAD) mRNA expression in central stress circuits. J. Neurosci. 18 (1998) 5938-5947
14. Bowman R.E., MacLusky N.J., Sarmiento Y., Frankfurt M., Gordon M., and Luine V.N. Sexually dimorphic effects of prenatal stress on cognition, hormonal responses, and central neurotransmitters. Endocrinology 145 (2004) 3778-3787
15. Breier A., Buchanan R.W., Kirkpatrick B., Davis O.R., Irish D., Summerfelt A., and Carpenter Jr. W.T. Effects of clozapine on positive and negative symptoms in outpatients with schizophrenia. Am. J. Psychiatry 151 (1994) 20-26
16. Brixey S.N., Gallagher III B.J., McFalls Jr. J.A., and Parmelee L.F. Gestational and neonatal factors in the etiology of schizophrenia. J. Clin. Psychol. 49 (1993) 447-456
17. Buchanan R.W., Breier A., Kirkpatrick B., Ball P., and Carpenter Jr. W.T. Positive and negative symptom response to clozapine in schizophrenic patients with and without the deficit syndrome. Am. J. Psychiatry 155 (1998) 751-760
18. Buijs R.M. Intra- and extrahypothalamic vasopressin and oxytocin pathways in the rat. Pathways to the limbic system, medulla oblongata and spinal cord. Cell Tissue Res. 192 (1978) 423-435
19. Buijs R.M. Immunocytochemical demonstration of vasopressin and oxytocin in the rat brain by light and electron microscopy. J. Histochem. Cytochem. 28 (1980) 357-360
20. Bujanow W. Letter: is oxytocin an anti-schizophrenic hormone?. Can. Psychiatr. Assoc. J. 19 (1974) 323
21. Caldji C., Tannenbaum B., Sharma S., Francis D., Plotsky P.M., and Meaney M.J. Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc. Natl. Acad. Sci. U. S. A. (1998) 95
22. Carpenter Jr. W.T., and Buchanan R.W. Schizophrenia. N. Engl. J. Med. 330 (1994) 681-690
23. Carter C.S., DeVries A.C., and Getz L.L. Physiological substrates of mammalian monogamy: the prairie vole model. Neurosci. Biobehav. Rev. 19 (1995) 303-314
24. Cho M.M., DeVries A.C., Williams J.R., and Carter C.S. The effects of oxytocin and vasopressin on partner preferences in male and female prairie voles (Microtus ochrogaster). Behav. Neurosci. 113 (1999) 1071-1079
25. Choleris E., Gustafsson J.A., Korach K.S., Muglia L.J., Pfaff D.W., and Ogawa S. An estrogen-dependent four-gene micronet regulating social recognition: a study with oxytocin and estrogen receptor-alpha and -beta knockout mice. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 6192-6197
26. Consiglio A.R., Borsoi A., Pereira G.A., and Lucion A.B. Effects of oxytocin microinjected into the central amygdaloid nucleus and bed nucleus of stria terminalis on maternal aggressive behavior in rats. Physiol. Behav. 85 (2005) 354-362
27. Cornblatt B.A. The New York high risk project to the Hillside recognition and prevention (RAP) program. Am. J. Med. Genet. 114 (2002) 956-966
28. Daenen E.W., Wolterink G., Gerrits M.A., and Van Ree J.M. The effects of neonatal lesions in the amygdala or ventral hippocampus on social behaviour later in life. Behav. Brain Res. 136 (2002) 571-582
29. Ferguson J.N., Young L.J., Hearn E.F., Matzuk M.M., Insel T.R., and Winslow J.T. Social amnesia in mice lacking the oxytocin gene. Nat. Genet. 25 (2000) 284-288
30. File S.E., and Hyde J.R. A test of anxiety that distinguishes between the actions of benzodiazepines and those of other minor tranquilisers and of stimulants. Pharmacol. Biochem. Behav. 11 (1979) 65-69
31. Francis D.D., Champagne F.C., and Meaney M.J. Variations in maternal behaviour are associated with differences in oxytocin receptor levels in the rat. J. Neuroendocrinol. 12 (2000) 1145-1148
32. Fride E., Dan Y., Feldon J., Halevy G., and Weinstock M. Effects of prenatal stress on vulnerability to stress on prepubertal and adult rats. Physiol. Behav. 37 (1986) 681-687
33. Fries A.B., Ziegler T.E., Kurian J.R., Jacoris S., and Pollak S.D. Early experience in humans is associated with changes in neuropeptides critical for regulating social behavior. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 17237-17240
34. Gimpl G., and Fahrenholz F. The oxytocin receptor system: structure, function, and regulation. Physiol. Rev. 81 (2001) 629-683
35. Glovinsky D., Kalogeras K.T., Kirch D.G., Suddath R., and Wyatt R.J. Cerebrospinal fluid oxytocin concentration in schizophrenic patients does not differ from control subjects and is not changed by neuroleptic medication. Schizophr. Res. 11 (1994) 273-276
36. Gur R.E., McGrath C., Chan R.M., Schroeder L., Turner T., Turetsky B.I., Kohler C., Alsop D., Maldjian J., Ragland J.D., and Gur R.C. An fMRI study of facial emotion processing in patients with schizophrenia. Am. J. Psychiatry 159 (2002) 1992-1999
37. Gurtman C.G., Morley K.C., Li K.M., Hunt G.E., and McGregor I.S. Increased anxiety in rats after 3, 4-methylenedioxymethamphetamine: association with serotonin depletion. Eur. J. Pharmacol. 446 (2002) 89-96
38. Heim C., Owens M.J., Plotsky P.M., and Nemeroff C.B. I. Endocrine factors in the pathophysiology of mental disorders. Persistent changes in corticotropin-releasing factor systems due to early life stress: relationship to the pathophysiology of major depression and post-traumatic stress disorder. Psychopharmacol. Bull. (1997) 33
39. Hempel A., Hempel E., Schonknecht P., Stippich C., and Schroder J. Impairment in basal limbic function in schizophrenia during affect recognition. Psychiatry Res. 122 (2003) 115-124
40. Henry C., Kabbaj M., Simon H., LeMoal M., and Maccari S. Prenatal stress increases the hypothalamo-pituitary-adrenal axis response in young and adult rats. J. Neuroendocrinol. 6 (1994) 341-345
41. Huber D., Veinante P., and Stoop R. Vasopressin and oxytocin excite distinct neuronal populations in the central amygdala. Science 308 (2005) 245-248
42. Insel T.R. Oxytocin-a neuropeptide for affiliation: evidence from behavioral, receptor autoradiographic, and comparative studies. Psychoneuroendocrinology 17 (1992) 3-35
43. Insel T.R. A neurobiological basis of social attachment. Am. J. Psychiatry 154 (1997) 726-735
44. Javitt D.C. Management of negative symptoms of schizophrenia. Curr. Psychiatry Rep. 3 (2001) 413-417
45. Kelley M.E., Gilbertson M., Mouton A., and van Kammen D.P. Deterioration in premorbid functioning in schizophrenia: a developmental model of negative symptoms in drug-free patients. Am. J. Psychiatry 149 (1992) 1543-1548
46. Kinnunen A.K., Koenig J.I., and Bilbe G. Repeated variable prenatal stress alters pre- and postsynaptic gene expression in the rat frontal pole. J. Neurochem. 86 (2003) 736-748
47. Kirkpatrick B., Fenton W.S., Carpenter Jr. W.T., and Marder S.R. The NIMH-MATRICS consensus statement on negative symptoms. Schizophr. Bull. 32 (2006) 214-219
48. Koehl M., Darnaudery M., Dulluc J., Van Reeth O., Le Moal M., and Maccari S. Prenatal stress alters circadian activity of hypothalamo-pituitary-adrenal axis and hippocampal corticosteroid receptors in adult rats of both gender. J. Neurobiol. 40 (1999) 302-315
49. Koenig J.I. Hippocampal-dependent cognitive function and nicotinic receptor expression is compromised by prenatal stress exposure in the rat. Soc. Neurosci. Abstr. 35 (2005) 556.15
50. Koenig J.I., Elmer G.I., Shepard P.D., Lee P.R., Mayo C., Joy B., Hercher E., and Brady D.L. Prenatal exposure to a repeated variable stress paradigm elicits behavioral and neuroendocrinological changes in the adult offspring: potential relevance to schizophrenia. Behav. Brain Res. 156 (2005) 251-261
51. Koenig J.I., Kirkpatrick B., and Lee P. Glucocorticoid hormones and early brain development in schizophrenia. Neuropsychopharmacology 27 (2002) 309-318
52. Kosfeld M., Heinrichs M., Zak P.J., Fischbacher U., and Fehr E. Oxytocin increases trust in humans. Nature 435 (2005) 673-676
53. Le Pen G., and Moreau J.L. Disruption of prepulse inhibition of startle reflex in a neurodevelopmental model of schizophrenia: reversal by clozapine, olanzapine and risperidone but not by haloperidol. Neuropsychopharmacology 27 (2002) 1-11
54. Le Pen G., Grottick A.J., Higgins G.A., Martin J.R., Jenck F., and Moreau J.L. Spatial and associative learning deficits induced by neonatal excitotoxic hippocampal damage in rats: further evaluation of an animal model of schizophrenia. Behav. Pharmacol. 11 (2000) 257-268
55. Lee P.R., Brady D., Shapiro R.A., Dorsa D.M., and Koenig J.I. Social interaction deficits caused by chronic phencyclidine administration are reversed by oxytocin. Neuropsychopharmacology 30 (2005) 1883-1894 (published online 1882/1816/1805)
56. Lehmann J.M., Stohr T., and Feldon J. Long-term effects of prenatal stress experience and postnatal maternal separation on emotionality and attentional processes. Behav. Brain Res. 107 (2000) 133-144
57. Lewis D.A., and Levitt P. Schizophrenia as a disorder of neurodevelopment. Annu. Rev. Neurosci. 25 (2002) 409-432
58. Linkowski P., Geenen V., Kerkhofs M., Mendlewicz J., and Legros J.J. Cerebrospinal fluid neurophysins in affective illness and in schizophrenia. Eur. Arch. Psychiatr. Neurol. Sci. 234 (1984) 162-165
59. Lipska B.K., and Weinberger D.R. To model a psychiatric disorder in animals: schizophrenia as a reality test. Neuropsychopharmacology 23 (2000) 223-239
60. Lipska B.K., Aultman J.M., Verma A., Weinberger D.R., and Moghaddam B. Neonatal damage of the ventral hippocampus impairs working memory in the rat. Neuropsychopharmacology 27 (2002) 47-54
61. Mai J.K., Berger K., and Sofroniew M.V. Morphometric evaluation of neurophysin-immunoreactivity in the human brain: pronounced inter-individual variability and evidence for altered staining patterns in schizophrenia. J. Hirnforsch. 34 (1993) 133-154
62. McGurk S.R. The effects of clozapine on cognitive functioning in schizophrenia. J. Clin. Psychiatry 60 Suppl 12 (1999) 24-29
63. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu. Rev. Neurosci. 24 (2001) 1161-1192
64. Moller P., and Husby R. The initial prodrome in schizophrenia: searching for naturalistic core dimensions of experience and behavior. Schizophr. Bull. 26 (2000) 217-232
65. Neumann I.D. Involvement of the brain oxytocin system in stress coping: interactions with the hypothalamo-pituitary-adrenal axis. Prog. Brain Res. 139 (2002) 147-162
66. Palmer A.A., Printz D.J., Butler P.D., Dulawa S.C., and Printz M.P. Prenatal protein deprivation in rats induces changes in prepulse inhibition and NMDA receptor binding. Brain Res. 996 (2004) 193-201
67. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (1986), Academic Press, Orlando, FL
68. Pedersen C.A., and Prange Jr. A.J. Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin. Proc. Natl. Acad. Sci. U. S. A. 76 (1979) 6661-6665
69. Pedersen C.A., Ascher J.A., Monroe Y.L., and Prange Jr. A.J. Oxytocin induces maternal behavior in virgin female rats. Science 216 (1982) 648-650
70. Prut L., and Belzung C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur. J. Pharmacol. 463 (2003) 3-33
71. Rajarethinam R., DeQuardo J.R., Miedler J., Arndt S., Kirbat R., Brunberg J.A., and Tandon R. Hippocampus and amygdala in schizophrenia: assessment of the relationship of neuroanatomy to psychopathology. Psychiatry Res. 108 (2001) 79-87
72. Rapoport J.L., Addington A.M., Frangou S., and Psych M.R. The neurodevelopmental model of schizophrenia: update 2005. Mol. Psychiatry 10 (2005) 434-449
73. Rueter L.E., Ballard M.E., Gallagher K.B., Basso A.M., Curzon P., and Kohlhaas K.L. Chronic low dose risperidone and clozapine alleviate positive but not negative symptoms in the rat neonatal ventral hippocampal lesion model of schizophrenia. Psychopharmacology (Berl) 176 (2004) 312-319
74. Sams-Dodd F. Distinct effects of d-amphetamine and phencyclidine on the social behaviour of rats. Behav. Pharmacol. 6 (1995) 55-65
75. Sams-Dodd F. Phencyclidine-induced stereotyped behaviour and social isolation in rats: a possible animal model of schizophrenia. Behav. Pharmacol. 7 (1996) 3-23
76. Sams-Dodd F., Lipska B.K., and Weinberger D.R. Neonatal lesions of the rat ventral hippocampus result in hyperlocomotion and deficits in social behaviour in adulthood. Psychopharmacology (Berl) 132 (1997) 303-310
77. Sherman T.G., Day R., Civelli O., Douglass J., Herbert E., Akil H., and Watson S.J. Regulation of hypothalamic magnocellular neuropeptides and their mRNAs in the brattleboro rat: coordinate responses to further osmotic challenge. J. Neurosci. 8 (1988) 3785-3796
78. Shi L., Fatemi S.H., Sidwell R.W., and Patterson P.H. Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring. J. Neurosci. 23 (2003) 297-302
79. Sullivan P.F. The genetics of schizophrenia. PLoS Med. 2 (2005) e212
80. Szot P., Bale T.L., and Dorsa D.M. Distribution of messenger RNA for the vasopressin V1a receptor in the CNS of male and female rats. Mol. Brain Res. 24 (1994) 1-10
81. Takahashi L.K., Haglin C., and Kalin N.H. Prenatal stress potentiates stress-induced behavior and reduces the propensity to play in juvenile rats. Physiol. Behav. 51 (1992) 319-323
82. Tanaka K., Suzuki M., Sumiyoshi T., Murata M., Tsunoda M., and Kurachi M. Subchronic phencyclidine administration alters central vasopressin receptor binding and social interaction in the rat. Brain Res. 992 (2003) 239-245
83. Uvnas-Moberg K., Alster P., and Svensson T.H. Amperozide and clozapine but not haloperidol or raclopride increase the secretion of oxytocin in rats. Psychopharmacology (Berl) 109 (1992) 473-476
84. Vallee M., Mayo W., Dellu F., LeMoal M., Simon H., and Maccari S. Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion. J. Neurosci. (1997) 17
85. Walker E.F., and Diforio D. Schizophrenia: a neural diathesis-stress model. Psychol. Rev. 104 (1997) 667-685
86. Ward H.E., Johnson E.A., Salm A.K., and Birkle D.L. Effects of prenatal stress on defensive withdrawal behavior and corticotropin releasing factor systems in rat brain. Physiol. Behav. 70 (2000) 359-366
87. Ward O.B., Ward I.L., Denning J.H., Hendricks S.E., and French J.A. Hormonal mechanisms underlying aberrant sexual differentiation in male rats prenatally exposed to alcohol, stress, or both. Arch. Sex. Behav. 31 (2002) 9-16
88. Weinberger D.R., and Lipska B.K. Cortical maldevelopment, anti-psychotic drugs and schizophrenia: a search for common ground. Schizophr. Res. 16 (1995) 87-110
89. Weinstock M. Alterations induced by gestational stress in brain morphology and behavior of the offspring. Prog. Neurobiol. 65 (2001) 427-451
90. Witt D.M., Carter C.S., and Walton D.M. Central and peripheral effects of oxytocin administration in prairie voles (Microtus ochrogaster). Pharmacol. Biochem. Behav. 37 (1990) 63-69
91. Witt D.M., Winslow J.T., and Insel T.R. Enhanced social interactions in rats following chronic, centrally infused oxytocin. Pharmacol. Biochem. Behav. 43 (1992) 855-861
92. Young L.J., and Frank A. Beach Award. Oxytocin and vasopressin receptors and species-typical social behaviors. Horm. Behav. 36 (1999) 212-221
93. Young L.J., Winslow J.T., Wang Z., Gingrich B., Guo Q., Matzuk M.M., and Insel T.R. Gene targeting approaches to neuroendocrinology: oxytocin, maternal behavior, and affiliation. Horm. Behav. 31 (1997) 221-231
94. Young L.J., Wang Z., Cooper T.T., and Albers H.E. Vasopressin (V1a) receptor binding, mRNA expression and transcriptional regulation by androgen in the Syrian hamster brain. J. Neuroendocrinol. 12 (2000) 1179-1185
95. Zak P.J., Kurzban R., and Matzner W.T. Oxytocin is associated with human trustworthiness. Horm. Behav. 48 (2005) 522-527
96. Zuckerman L., Rehavi M., Nachman R., and Weiner I. Immune activation during pregnancy in rats leads to a postpubertal emergence of disrupted latent inhibition, dopaminergic hyperfunction, and altered limbic morphology in the offspring: a novel neurodevelopmental model of schizophrenia. Neuropsychopharmacology 28 (2003) 1778-1789