Behavioral effects of environmental enrichment during gestation in WKY and Wistar rats

Behavioural Brain Research

Volumn 233, Issue 2, 2012, Pages 245-255

  Rosenfeld, Ateret ^a   Weller, Aron ^a  

^a BAR ILAN UNIVERSITY   (Israel)

Author keywords

Activity; Anxiety like behavior; Early programming; Maternal behavior; Prenatal environmental enrichment; Rats; WKY rats

Indexed keywords

CORTICOSTERONE;

ADULT ANIMAL; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; BEHAVIOR; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DEPRESSION; ENVIRONMENTAL ENRICHMENT; FECES ANALYSIS; FEMALE; FORCED SWIMMING TEST; GESTATION PERIOD; JUVENILE ANIMAL; LACTATION; MALE; MATERNAL BEHAVIOR; MAZE TEST; NONHUMAN; OPEN FIELD TEST; PRENATAL EXPOSURE; PRIORITY JOURNAL; RAT; SEX DIFFERENCE; WISTAR KYOTO RAT; WISTAR RAT;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; ANXIETY; BEHAVIOR, ANIMAL; CIRCADIAN RHYTHM; CORTICOSTERONE; ENVIRONMENT; ENZYME-LINKED IMMUNOSORBENT ASSAY; EXPLORATORY BEHAVIOR; FECES; FEMALE; LACTATION; MALE; MATERNAL BEHAVIOR; MAZE LEARNING; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, INBRED WKY; RATS, WISTAR; SEX CHARACTERISTICS; STATISTICS, NONPARAMETRIC; SWIMMING;

EID: 84862181146     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2012.05.006     Document Type: Article

References (100)

1. Drake A.J., Walker B.R., Seckel J.R. Intergenerational consequences of fetal programming by in utero exposure to glucocorticoids in rats. American Journal of Physiology: Regulatory Integrative and Comparative Physiology 2005, 288:R34-R38.
2. Lau C., Rogers J.M. Embryonic and fetal programming of physiological disorders in adulthood. Birth Defects Research 2004, 72:300-312.
3. McArdle H.J., Andersen H.S., Jones H., Gambling L. Fetal programming: causes and consequences as revealed by studies of dietary manipulation in rats - a review. Placenta 2006, 27:S56-S60.
4. Newnham J.P., Ross M.G. Early life origins of human health and disease 2009, S Karger, Basel.
5. O'Donnell K., O'Connor T.G., Glover V. Prenatal stress and neurodevelopment of the child: focus on the HPA axis and role of the placenta. Developmental Neuroscience 2009, 31:285-292.
6. Van den Bergh B.R., Marcoen A. High antenatal maternal anxiety is related to ADHD symptoms, externalizing problems, and anxiety in 8- and 9-year-olds. Child Development 2004, 75:1085-1097.
7. Abrams R.M., Gerhardt K.J., Peters A.J.M. Transmission of sound and vibration to the fetus. Fetal development: a psychobiological perspective 1995, 315-330. Lawrence Erlbaum, Hillsdale, NJ. J.P. Lecanuet, W.P. Fifer, N.A. Krasnegor, W.P. Smotherman (Eds.).
8. Lecanuet J.P., Schaal B. Fetal sensory competencies. European Journal of Obstetrics, Gynecology, and Reproductive Biology 1996, 68:1-23.
9. Issel E.P. Fetal response to external mechanical stimuli. Journal of Perinatal Medicine 1983, 11:232-242.
10. Van den Bergh B.R.H., Mulder E.J.H., Mennesa M., Glover V. Antenatal maternal anxiety and stress and the neurobehavioural development of the fetus and child: links and possible mechanisms. a review. Neuroscience and Biobehavioral Reviews 2005, 29:237-258.
11. Talge N.M., Neal C., Glover V. The early stress, translational research and prevention science network: fetal and neonatal experience on child and adolescent mental health. Antenatal maternal stress and long-term effects on child neurodevelopment: how and why?. Journal of Child Psychology and Psychiatry, and Allied Disciplines 2007, 8:245-261.
12. Davis E.P., Glynn L.M., Schetter C.D., Hobel C., Chicz-Demet A., Sandman C.A. Prenatal exposure to maternal depression and cortisol influences infant temperament. Journal of the American Academy of Child and Adolescent Psychiatry 2007, 46:737-746.
13. Weinstock M. The potential influence of maternal stress hormones on development and mental health of the offspring. Brain, Behavior, and Immunity 2005, 19:296-308.
14. Kinney D.K., Munir K.M., Crowley D.J., Miller A.M. Prenatal stress and risk for autism. Neuroscience and Biobehavioral Reviews 2008, 32:1519-1532.
15. Conger R.D., Ge X., Elder G.H., Lorenz F.O., Simons R.L. Economic stress, coercive family process, and developmental problems of adolescents. Child Development 1994, 65:541-561.
16. Eisenberg L., Earls F.J. Poverty, social depreciation and child development. Handbook of psychiatry 1975, vol. 6:275-291. Basic Books, New York.
17. McLoyd V.C. The impact of economic hardship on black families and children: psychological distress, parenting, and socioemotional development. Child Development 1990, 61:311-346.
18. McLoyd V.C. Socioeconomic disadvantage and child development. American Psychologist 1998, 53:185-204.
19. Francis D.D., Meaney M.J. Maternal care and the development of stress responses. Current Opinion in Neurobiology 1999, 9:128-134.
20. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annual Review of Neuroscience 2001, 24:1161-1192.
21. Macri S., Wurbel H. Developmental plasticity of HPA and fear responses in rats: a critical review of the maternal mediation hypothesis. Hormones and Behavior 2006, 50:667-680.
22. Wadhwa P.D., Sandman C.A., Porto M., Dunkel-Schetter C., Garite T.J. The association between prenatal stress and infant birth weight and gestational age at birth: a prospective investigation. American Journal of Obstetrics and Gynecology 1993, 169:858-865.
23. Huizink A.C., Mulder E.J., Buitelaar J.K. Prenatal stress and risk for psychopathology: specific effects or induction of general susceptibility. Psychological Bulletin 2004, 130:115-142.
24. Weinstock M. The long-term behavioural consequences of prenatal stress. Neuroscience and Biobehavioral Reviews 2008, 32:1073-1086.
25. Austin M.P., Leader L.R., Reilly N. Prenatal stress, the hypothalamic-pituitary-adernal axis, and fetal and infant neurobehaviour. Early Human Development 2005, 81:917-926.
26. Weinstock M. Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Progress in Neurobiology 2001, 65:427-451.
27. Marashi V., Barnekow A., Ossendorf E., Sachser N. Effects of different forms of environmental enrichment on behavioral, endocrinological, and immunological parameters in male mice. Hormones and Behavior 2003, 43:281-292.
28. Renner M.J., Rosenzweig M.R. Enriched and impoverished environments: effects on brain and behavior 1987, Springer, New York.
29. Falkenberg T., Mohammed A.K., Henriksson B., Persson H., Winblad B., Lindefors N. Increased expression of brain-derived neurotropic factor mRNA in rat hippocampus is associated with improved spatial memory and enriched environment. Neuroscience Letters 1992, 138:153-156.
30. Paylor R., Morrison S.K., Rudy J.W., Waltrip L.T., Wehner J.M. Brief exposure to an enriched environment improves performance on the Morris water task and increases hippocampal cystolic protein kinase C activity in young rats. Behavioural Brain Research 1992, 52:49-59.
31. Brenes S'aenz J.C., Villagra O.R., Fornaguera Trias J. Factor analysis of forced swimming test, sucrose preference test and open field test on enriched, social and isolated reared rats. Behavioural Brain Research 2006, 169:57-65.
32. Klein S.L., Lambert K.G., Durr D., Schaefer T., Waring R.E. Influence of environmental enrichment and sex on predator stress response in rats. Physiology and Behavior 1994, 56:291-297.
33. Mohammed A.K., Winblad B., Ebendal T., Larkfors L. Environmental influence on behavior and nerve growth factor in the brain. Brain Research 1990, 528:62-72.
34. Brenes J.C., Rodríguez O., Fornaguera J. Differential effect of environment enrichment and social isolation on depressive-like behavior, spontaneous activity and serotonin and norepinephrine concentration in prefrontal cortex and ventral striatum. Pharmacology Biochemistry and Behavior 2008, 89:85-93.
35. Francis D.D., Diorio J., Plotsky P.M., Meaney M.J. Environmental enrichment reverses the effects of maternal separation on stress reactivity. Journal of Neuroscience 2002, 22:7840-7843.
36. Laviola G., Rea M., Morley-fletcher S., Di Carlo S., Bacosi A., De Simone R., et al. Beneficial effects of enriched environment on adolescent rats from stressed pregnancies. European Journal of Neuroscience 2004, 20:1655-1664.
37. Van Dellen A., Blakemore C., Deacon R., York D., Hannan A.J. Delaying the onset of Huntington's in mice. Nature 2000, 404:721-722.
38. McKim M., Thompson W.R. Prenatal maternal enrichment and restriction in rats: effects on biological and foster offspring. Bulletin of the Psychonomic Society 1975, 5:259-260.
39. Kiyono S., Seo M.L., Shibagaki M., Inouye M. Facilitative effects of maternal environmental enrichment on maze learning in rat offspring. Physiology and Behavior 1985, 34:431-435.
40. Koo J.W., Park C.H., Choi S.H., Kim N.J., Kim H.S., Choe J.C., et al. Postnatal environment can counteract prenatal effects on cognitive ability, cell proliferation and synaptic protein expression. FASEB Journal 2003, 17:1556-1558.
41. Welberg L., Thrivikraman K.V., Plotsky P.M. Combined pre- and postnatal environmental enrichment programs the HPA axis differentially in male and female rats. Psychoneuroendocrinology 2006, 31:553-564.
42. Bebbington P. The classification and epidemiology of unipolar depression. Mood disorders: a handbook of science and practice 2004, 3-28. Wiley, Chichester. M. Power (Ed.).
43. Heim C., Plotsky P.M., Nemeroff C.B. Importance of studying the contributions of early adverse experience to neurobiological findings in depression. Neuropsychopharmacology 2004, 29:641-648.
44. Pryce C.R., Rüedi-Bettschen D., Dettling A.C., Weston A., Russig H., Ferger B., et al. Long-term effects of early-life environmental manipulations in rodents and primates: potential animal models in depression research. Neuroscience and Biobehavioral Reviews 2005, 29:649-674.
45. Pare W.P. Hyponeophagia in Wistar Kyoto rats. Physiology and Behavior 1994, 55:975-978.
46. Malkesman O., Braw Y., Zagoory-Sharon O., Golan O., Lavi-Avnon Y., Schroeder M., et al. Reward and anxiety in genetic animal models of childhood depression. Behavioural Brain Research 2005, 164:1-10.
47. Malkesman O., Braw Y., Maayan R., Weizman A., Overstreet D.H., Shabat-Simon M., et al. Two different putative genetic animal models of childhood depression. Biological Psychiatry 2006, 59:17-23.
48. Pare W.P., Redei E. A biobehavioral profile of an ulcer susceptible rat strain. Neuroendocrinology of gastrointestinal ulceration 1995, 201-208. Plenum, New York. S. Szabo, Y. Tache (Eds.).
49. Redei E., Pare W.P., Aird F., Kluczynski J. Strain differences in hypothalamic-pituitary-adrenal activity and stress ulcer. American Journal of Physiology 1994, 266:R353-R360.
50. Braw Y., Malkesman O., Merlender A., Bercovich A., Dagan M., Maayan R., et al. Stress hormones and emotion-regulation in two genetic animal models of depression. Psychoneuroendocrinology 2006, 31:1105-1116.
51. De La Garza R., Mahoney J.J. A distinct neurochemical profile in WKY rats at baseline and in response to acute stress: implications for animal models of anxiety and depression. Brain Research 2004, 1021:209-218.
52. Jaio X., Pare W.P., Tejani-Butt S. Strain differences in the distribution of dopamine transporter sites in rat brain. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2003, 27:913-919.
53. Makesman O., Braw Y., Ram E., Maayan R., Weizman A., Kinor N., et al. Dehydroepiandrosterone and monoamines in the limbic system of a genetic animal model of childhood depression. European Neuropsychopharmacology 2008, 18:255-261.
54. Malkesman O., Shayit M., Genud R., Zangen A., Kinor N., Maayan R., et al. Dehydroepiandrosterone in the nucleus accumbens is associated with early onset of depressive-behavior: a study in an animal model of childhood depression. Neuroscience 2007, 149:573-581.
55. Solberg L.C., Olson S., Turek F.W., Redei E. Altered hormone levels and circadian rhythm of activity in the WKY rat, a putative animal model of depression. American Journal of Physiology: Regulatory Integrative and Comparative Physiology 2001, 281:R786-R794.
56. Griebel G., Moreau J.L., Jenck F., Misslin R., Martin J.R. Acute and chronic treatment with 5-HT uptake inhibitors differentially modulates emotional responses in anxiety models in rodents. Psychopharmacology 1994, 113:463-470.
57. Lahmame A., del Arco C., Pazos A., Yritia M., Armario A. Are Wistar-Kyoto rats a genetic animal model of depression resistant to antidepressants. European Journal of Pharmacology 1997, 337:115-123.
58. Lopez- Rubalcava C., Lucki I. Strain differences in the behavioral effects of antidepressant drugs in the forced swim test. Neuropsychopharmacology 2000, 22:191-199.
59. Malkesman O., Asaf T., Shbiro L., Goldstein A., Maayan R., Weizman A., et al. Monoamines, BDNF, dehydroepiandrosterone, DHEA-sulfate, and childhood depression-an animal model study. Advances in Pharmacological Science 2009, 2009:405107.
60. Pollier F., Sophie S., Aguerre S., Ebinger G. Serotonin reuptake inhibitors by citalopram in rat strains differing for their emotionality. Neuropsychopharmacology 2000, 22:64-76.
61. Tejani-Butt S., Kluczynski J., Pare W.P. Strain-dependent modification of behavior following antidepressant treatment. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2003, 27:7-14.
62. Beck K.D., Jiao X., Pang K.C., Servatius R.J. Vulnerability factors in anxiety determined through differences in active-avoidance behavior. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2010, 34:852-860.
63. Braw Y., Malkesman O., Merlender A., Bercovich A., Dagan M., Overstreet D.H., et al. Withdrawal emotion-regulation in infant rats from genetic animal models of depression. Behavioural Brain Research 2008, 193:94-100.
64. Cameron O.G. Anxious-depressive comorbidity: effects on HPA axis and CNS noradrenergic functions. Essential Psychopharmacology 2006, 7:24-34.
65. Abbey H., Howard E. Statistical procedure in developmental studies on species with multiple offspring. Developmental Psychobiology 1973, 6:329-335.
66. Pare W.P., Redei E. Sex differences and stress response of WKY rats. Physiology and Behavior 1993, 54:1179-1185.
67. Schroeder M., Lavi-Avnon Y., Dagan M., Zagoory-Sharon O., Moran T.H., Weller A. Diurnal and nocturnal nursing behavior in the OLETF rat. Developmental Psychobiology 2007, 49:323-333.
68. Schroeder M., Zagoory-Sharon O., Lavi-Avnon Y., Moran T.H., Weller A. Weight gain and maternal behavior in CCK1 deficient rats. Physiology and Behavior 2006, 89:402-409.
69. Ottoni E.B. EthoLog 2.2: a tool for the transcription and timing of behavior observation sessions. Behavior Research Methods, Instruments and Computers 2000, 32:446-449.
70. Pellow S., File S.E. Anxiolytic and anxiogenic drug effects exploratory activity in an elevated plus maze: a novel test of anxiety in the rat. Pharmacology Biochemistry and Behavior 1986, 24:525-529.
71. Abel E.L. Ontogeny of immobility and response to alarm substance in the forced swim test. Physiology and Behavior 1993, 54:713-716.
72. Abelson K.S.P., Frad S.S., Nyman J., Goldkuhl R., Hau J. Distribution of [3H]-corticosterone in urine, feces and blood of male Sprague-Dawley rats after tail vein and jugular vein injections. In vivo 2009, 23:381-386.
73. Siswanto H., Hau J., Carlsson H.E., Goldkuhl R., Abelson K.S.P. Corticosterone concentrations in blood and excretion in faeces after ACTH administration in male Sprague-Dawley rats. In vivo 2008, 22:435-440.
74. Sevenster P. A causal analysis of a displacement activity. Behavior Supplement 1961, 9:1-170.
75. Jolles J., Rompa-Barendregt J., Gispen W.H. Novelty and grooming behavior in the rat. Behavioral and Neural Biology 1979, 25:563-572.
76. Bindra D., Spinner N. Response to different degrees of novelty: the incidence of various activities. Journal of the Experimental Analysis of Behavior 1958, 341-350.
77. Westenbroek C., Ter Horst G.J., Roos M.H., Kuipers S.D., Trentani A., den Boer J.A. Gender-specific effect of social housing in rats after chronic mild stress exposure. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2003, 27:21-30.
78. Leshem M., Sherman M. Troubles shared are troubles halved: stress in rats is reduced in proportion to social propinquity. Physiology and Behavior 2006, 89:399-401.
79. Brenes J.C., Padilla M., Fornaguera J. A detailed analysis of open-field habituation and behavioral and neurochemical antidepressant-like effects in postweaning enriched rats. Behavioural Brain Research 2009, 197:125-137.
80. Magalhaes A., Summaviekke T., Tavares M.A., de Sousa L. Effects of postnatal cocaine exposure and environmental enrichment on rat behavior in a forced swim test. Annals of the New York Academy of Sciences 2004, 1025:619-629.
81. Bell R., O'Nill M. Exercise and pregnancy: a review. Birth 1994, 21:85-95.
82. DiPietro J.A., Irizarry R.A., Costigan K.A., Gurewitsch E. The psychophysiology of the maternal-fetal relationship. Psychophysiology 2004, 41:510-520.
83. Ito A., Kikusui T., Takeuchi Y., Mori Y. Effects of early weaning on anxiety and autonomic response to stress in rats. Behavioural Brain Research 2006, 171:87-93.
84. Kanari K., Kikusui T., Takeuchi Y., Mori Y. Multidimensional structure of anxiety-related behavior in early-weaned rats. Behavioural Brain Research 2005, 156:45-52.
85. Kikusui T., Nakamura K., Kakuma Y., Mori Y. Early weaning augments neuroendocrine stress response in mice. Behavioural Brain Research 2006, 175:96-103.
86. Kikusui T., Mori Y. Behavioural and neurochemical consequences of early weaning in rodents. Journal of Neuroendocrinology 2009, 21:427-431.
87. Maruoka T., Kodomari I., Yamauchi R., Wada E., Wada K. Maternal enrichment affects prenatal hippocampal proliferation and open-field behaviors in female offspring mice. Neuroscience Letters 2000, 454:28-32.
88. Götz A.A., Stefanski V. Psychosocial maternal stress during pregnancy affects serum corticosterone, blood immune parameters and anxiety behaviour in adult male rat offspring. Physiology and Behavior 2007, 90:108-115.
89. Cannizzaro C., Plescia F., Martire M., Gagliano M., Cannizzaro G., Mantia G., et al. Single, intense prenatal stress decreases emotionality and enhances learning performance in the adolescent rat offspring: interaction with a brief, daily maternal separation. Behavioural Brain Research 2006, 169:128-136.
90. Ordyan N.é., Pivina S.G. Characteristics of the behavior and stress-reactivity of the hypophyseal-adrenal system in prenatally stressed rats. Neuroscience and Behavioral Physiology 2004, 34:569-574.
91. Chin E.H., Love O.P., Verspoor J.J., Williams T.D., Rowley K., Burness G. Juveniles exposed to embryonic corticoserone have enhanced flight performance. Proceedings: Biological Sciences/The Royal Society 2009, 276:499-505.
92. DiPietro J.A., Novak M.F., Costigan K.A., Atella L.D., Reusing S.P. Maternal psychological distress during pregnancy in relation to child development at age two. Child Development 2006, 77:573-587.
93. Marin M.T., Planeta C.S. Maternal separation affects cocaine-induced locomotion and response to novelty in adolescent, but not in adult rats. Brain Research 2004, 1013:83-90.
94. Viveros M.P., Llorente R., López-Gallardo M., Suarez J., Bermúdez-Silva F., De la Fuente M., et al. Sex-dependent alterations in response to maternal deprivation in rats. Psychoneuroendocrinology 2009, 34:S217-S226.
95. Gué M., Bravard A., Meunier J., Veyrier R., Gaillet S., Recasens M., et al. Sex differences in learning deficits induced by prenatal stress in juvenile rats. Behavioural Brain Research 2004, 150:149-157.
96. Selye H. A syndrome produced by diverse noxious agents. Nature 1936, 138:32-36.
97. Heim C., Ehlert U., Hellhammer D.H. The potential role of hypocortisolosm in the pathophysiology of stress-related bodily disorders. Psychoneuroendocrinology 2000, 25:1-35.
98. Yehuda R., Levengood J., Schmeidler J., Wilson S., Guo L.S., Gerber D. Increased pituitary activation following metyrapone administration in PTSD. Psychoneuroendocrinology 1997, 21:1-16.
99. Friedman S.B., Mason J.W., Hanburg D.A. Urinary 17-hydroxycorticosteroid levels in parents of children with neoplastic disease: a study of chronic psychological stress. Psychosomatic Medicine 1963, 25:364-376.
100. Gunnar M.R., Vazquez D.A. Low cortisol and a flattening of expected daytime rhythm: potential indices of risk in human development. Development and Psychopathology 2001, 13:515-538.