Maternal behavior as an early modulator of neurobehavioral offspring responses by Sprague-Dawley rats

Behavioural Brain Research

Volumn 237, Issue 1, 2013, Pages 63-70

  Sequeira Cordero, Andrey ^a   Masís Calvo, Marianela ^a   Mora Gallegos, Andrea ^a   Fornaguera Trías, Jaime ^a  

^a UNIVERSIDAD DE COSTA RICA   (Costa Rica)

Author keywords

5 HT neurotransmission; Anxiety; Maternal programming; TrkB

Indexed keywords

BIOGENIC AMINE; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CYCLOPHILIN A; SEROTONIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BDNF GENE; BRAIN REGION; COGNITION; CONTROLLED STUDY; CRH GENE; CRHR1 GENE; FORCED SWIMMING TEST; GENE; GENE EXPRESSION; GENETIC VARIABILITY; GROOMING; HPRT1 GEEN; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE 1 GENE; JUVENILE ANIMAL; LICKING; LOCOMOTION; MALE; MATERNAL BEHAVIOR; MATERNAL CARE; NEUROCHEMISTRY; NEUROTRANSMISSION; NONHUMAN; OPEN FIELD TEST; PEPTIDYLPROLIL ISOMERASE A GENE; PRIORITY JOURNAL; PROGENY; RAT; SPRAGUE DAWLEY RAT; TRKB GENE;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; DOPAMINE; EXPLORATORY BEHAVIOR; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIPPOCAMPUS; IMMOBILITY RESPONSE, TONIC; LOCOMOTION; MALE; MATERNAL BEHAVIOR; NEUROCHEMISTRY; NUCLEUS ACCUMBENS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, TRKB; SEROTONIN; STATISTICS, NONPARAMETRIC; SWIMMING;

EID: 84867211359     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2012.09.028     Document Type: Article

References (74)

1. Szyf M., Weaver I., Meaney M. Maternal care, the epigenome and phenotypic differences in behavior. Reproductive Toxicology 2007, 24:9-19.
2. Weaver I.C. Epigenetic programming by maternal behavior and pharmacological intervention. Nature versus nurture: let's call the whole thing off. Epigenetics 2007, 2(1):22-28.
3. Korosi A., Baram T.Z. The pathways from mother's love to baby's future. Frontiers in Behavioral Neuroscience 2009, 3:1-8.
4. Liu D., Diorio J., Tannenbaum B., Caldji C., Francis D., Freedman A., et al. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 1997, 277:1659-1662.
5. 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.
6. 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.
7. Weaver I.C., Champagne F.A., Brown S.E., Dymov S., Sharma S., Meaney M.J. Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life. Journal of Neuroscience 2005, 25:11045-11054.
8. Francis D.D., Meaney M.J. Maternal care and the development of stress responses. Current Opinion in Neurobiology 1999, 9:128-134.
9. Caldji C., Tannenbaum B., Sharma S., Francis D., Plotsky P.M., Meaney M.J. Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proceedings of the National Academy of Sciences of the United States of America 1998, 95:5335-5340.
10. Zhang T.Y., Chrétien P., Meaney M.J., Gratton A. Influence of naturally occurring variations in maternal care on prepulse inhibition of acoustic startle and the medial prefrontal cortical dopamine response to stress in adult rats. Journal of Neuroscience 2005, 25(6):1493-1502.
11. Weaver I.C., Meaney J.M., Szyf M. Maternal care effects on the hippocampal transcriptome and anxiety-mediate behaviors in the offspring that are reversible in adulthood. Proceedings of the National Academy of Sciences of the United States of America 2006, 103(9):3480-3485.
12. Champagne D.L., Bagot R.C., van Hasselt F., Ramakers G., Meaney M.J., de Kloet E.R., et al. Maternal care and hippocampal plasticity: evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress. Journal of Neuroscience 2008, 28(23):6037-6045.
13. Bagot R.C., van Hasselt F.N., Champagne D.L., Meaney M.J., Krugers H.J., Joëls M. Maternal care determines rapid effects of stress mediators on synaptic plasticity in adult rat hippocampal dentate gyrus. Neurobiology of Learning and Memory 2009, 92(3):292-300.
14. Meaney M.J., Szyf M. Environmental programming of stress responses through DNA methylation: life at the interface between a dynamic environment and a fixed genome. Dialogues in Clinical Neuroscience 2005, 7(2):103-123.
15. Bredy T.W., Grant R.J., Champagne D.L., Meaney M.J. Maternal care influences neuronal survival in the hippocampus of the rat. European Journal of Neuroscience 2003, 18(10):2903-2909.
16. Monroy E., Hernández-Torres E., Flores G. Maternal separation disrupts dendritic morphology of neurons in prefrontal cortex, hippocampus, and nucleus accumbens in male rat offspring. Journal of Chemical Neuroanatomy 2010, 40(2):93-101.
17. Diorio J., Meaney M.J. Maternal programming of defensive responses through sustained effects on gene expression. Journal of Psychiatry and Neuroscience 2007, 32:275-284.
18. Liu D., Diorio J., Day J.C., Francis D.D., Meaney M.J. Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nature Neuroscience 2000, 3:799-806.
19. Branchi I. The mouse communal nest: investigating the epigenetic influences of the early social environment on brain and behavior development. Neuroscience and Biobehavioral Reviews 2009, 33:551-559.
20. Macrì S., Laviola G., Leussis M.P., Anderse S.L. Abnormal behavioral and neurotrophic development in the younger sibling receiving less maternal care in a communal nursing paradigm in rats. Psychoneuroendocrinology 2009, 35:392-402.
21. Yoshii A., Constantine-Paton M. Postsynaptic BDNF-TrkB signaling in synapse maturation, plasticity, and disease. Development Neurobiology 2010, 70(5):304-322.
22. Fumagalli F., Bedogni F., Perez J., Racagni G., Riva M.A. Corticostriatal brain-derive neurotrophic factor dysregulation in adult rats following prenatal stress. European Journal of Neuroscience 2004, 20(5):1348-1354.
23. Zoladz P.R., Park C.R., Halonen J.D., Salim S., Alzoubi K.H., Srivareerat M., et al. Differential expression of molecular markers of synaptic plasticity in the hippocampus, prefrontal cortex, and amygdala in response to spatial learning, predator exposure, and stress-induce, amnesia. Hippocampus 2011, 22(3):577-589.
24. Coppens C.M., Siripornmongcolchai T., Wibrand K., Alme M.N., Buwalda B., de Boer S.F., et al. Social defeat during adolescence and adulthood differentially induce BDNF-regulated immediate early genes. Frontiers in Behavioral Neuroscience 2011, 5:72.
25. Francis D., Diorio J., Liu D., Meaney M.J. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 1999, 286(5442):1155-1158.
26. Liapakis G., Venihaki M., Margioris A., Grigoriadis D., Gkountelias K. Members of CRF family and their receptors: from past to future. Current Medicinal Chemistry 2011, 18(17):2583-2600.
27. Ivy A.S., Rex C.S., Chen Y., Dubé C., Maras P.M., Grigoriadis D.E., et al. Hippocampal dysfunction and cognitive impairments provoked by chronic early-life stress involve excessive activation of CRF receptors. Journal of Neuroscience 2010, 30(39):13005-13015.
28. Jaferi A., Bhatnagar S. Corticotropin-releasing hormone receptors in the medial prefrontal cortex regulate hypothalamic-pituitary-adrenal activity and anxiety-related behavior regardless of prior stress experience. Brain Research 2007, 1186:212-223.
29. Stern C.M., Luoma J.I., Meitzen J., Mermelstein P.G. Corticotropin releasing factor-induced CREB activation in striatal neurons occurs via a novel Gβ signaling pathway. PLoS ONE 2011, 6(3):e18114.
30. Curtis A.L., Bethea T., Valentino R.J. Sexually dimorphic responses of the brain norepinephrine system to stress and corticotropin-releasing factor. Neuropsychopharmacology 2006, 31(3):544-554.
31. Deltheil T., Guiard B.P., Cerdan J., David D.J., Tanaka K.F., Repérant C., et al. Behavioral and serotonergic consequences of decreasing or increasing hippocampus brain-derive, neurotrophic factor protein levels in mice. Neuropharmacology 2008, 55(6):1006-1014.
32. Hasbi A., Fan T., Alijaniaram M., Nguyen T., Perreault M.L., O'Dowd B.F., et al. Calcium signaling cascade links dopamine D1-D2 receptor heteromer to striatal BDNF production and neuronal growth. Proceedings of the National Academy of Sciences of the United States of America 2009, 106(50):21377-21382.
33. McEuen J.G., Semsar K.A., Lim M.A., Bale T.L. Influence of sex and corticotropin-releasing, factor pathways as determinants in serotonin sensitivity. Endocrinology 2009, 150(8):3709-3716.
34. Francis D.D., Caldji C., Champagne F., Plotsky P.M., Meaney M.J. The role of corticotropin-releasing factor-norepinephrine systems in mediating the effects of early experience on the development of behavioral and endocrine responses to stress. Biological Psychiatry 1999, 46(9):1153-1166.
35. Weaver I.C., D'Alessio A.C., Brown S.E., Hellstrom I.C., Dymov S., Sharma S., et al. The transcription factor nerve growth factor-inducible protein mediates epigenetic programming: altering epigenetic marks by immediate-early genes. Journal of Neuroscience 2007, 27(7):1756-1768.
36. Zhang T.Y., Hellstrom I.C., Bagot R.C., Wen X., Diorio J., Meaney M.J. Maternal care and DNA methylation of a glutamic acid decarboxylase 1 promoter in rat hippocampus. Journal of Neuroscience 2010, 30(39):13130-13137.
37. 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(1):125-137.
38. Marini F., Pozzato C., Andreetta V., Jansson B., Arban R., Domenici E., et al. Single exposure to social defeat increases corticotropin-releasing factor and glucocorticoid receptor mRNA expression in rat hippocampus. Brain Research 2006, 1067:25-35.
39. Rage F., Silhol M., Binamé F., Arancibia S., Tapia-Arancibia L. Effect of aging on the expression of BDNF and TrkB isoforms in rat pituitary. Neurobiology of Aging 2007, 28:1088-1098.
40. Santos A.R., Duarte C.B. Validation of internal control genes for expression studies: effects of the neurotrophin BDNF on hippocampal neurons. Journal of Neuroscience Research 2008, 86(16):3684-3692.
41. Hellemans J., Mortier G., De Paepe A., Speleman F., Vandesompele J. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biology 2007, 8(2):R19.
42. 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(1):85-93.
43. Walsh R.N., Cummins R.A. The Open-Field Test: a critical review. Psychological Bulletin 1976, 83(3):482-504.
44. Lister R.G. Ethologically-based animal models of anxiety disorders. Pharmacology Therapeutics 1990, 46:321-340.
45. Suarez S.D., Gallup G.G. An ethological analysis of open-field behavior in rats and mice. Learning and Motivation 1981, 12:342-363.
46. Markel A.L., Galaktionov Y.K., Efimov V.M. Factor analysis of rat behavior in an open field test. Neuroscience and Behavioral Physiology 1989, 19:279-286.
47. Whimbey A.E., Denenberg V.H. Two independent behavioral dimensions in open-field performance. Journal of Comparative and Physiological Psychology 1967, 63(3):500-504.
48. Ramos A., Mormède P. Stress and emotionality: a multidimensional and genetic approach. Neuroscience and Biobehavioral Reviews 1998, 22(1):33-57.
49. White D.A., Kalinichev M., Holtzman S.G. Locomotor response to novelty as a predictor of reactivity to aversive stimuli in the rat. Brain Research 2007, 1149:141-148.
50. Brenes J.C., Fornaguera J. The effect of chronic fluoxetine on social isolation-induced changes on sucrose consumption, immobility behavior, and on serotonin and dopamine function in hippocampus and ventral striatum. Behavioural Brain Research 2009, 198(1):199-205.
51. Daniels W.M., Pietersen C.Y., Carstens M.E., Stein D.J. Maternal separation in rats leads to anxiety-like behavior and a blunted ACTH response and altered neurotransmitter levels in response to a subsequent stressor. Metabolic Brain Disease 2004, 19(1-2):3-14.
52. Daniels W.M., Fairbairn L.R., van Tilburg G., McEvoy C.R., Zigmond M.J., Russell V.A., et al. Maternal separation alters nerve growth factor and corticosterone levels but not the DNA methylation status of the exon 1(7) glucocorticoid receptor promoter region. Metabolic Brain Disease 2009, 24(4):615-627.
53. Clinton S.M., Vázquez D.M., Kabbaj M., Kabbaj M.H., Watson S.J., Akil H. Individual differences in novelty-seeking and emotional reactivity correlate with variation in maternal behavior. Hormones and Behavior 2007, 51(5):655-664.
54. van Eekelen J.A., Rots N.Y., Sutanto W., de Kloet E.R. The effect of aging on stress responsiveness and central corticosteroid receptors in the brown Norway rat. Neurobiology of Aging 1992, 13(1):159-170.
55. Shoji H., Mizoguchi K. Acute and repeated stress differentially regulates behavioral, endocrine, neural parameters relevant to emotional and stress response in young and aged rats. Behavioural Brain Research 2010, 211(2):169-177.
56. Coutellier L., Friedrich A.C., Failing K., Würbel H. Variations in the postnatal maternal environment in mice: effects on maternal behaviour and behavioural and endocrine responses in the adult offspring. Physiology and Behavior 2008, 93(1-2):395-407.
57. Ramos A. Animal models of anxiety: do I need multiple tests?. Trends in Pharmacological Sciences 2008, 29(10):493-498.
58. Kaufman J., Yang B.Z., Douglas-Palumberi H., Grasso D., Lipschitz D., Houshyar S., et al. Brain-derived neurotrophic factor-5-HTTLPR gene interactions and environmental modifiers of depression in children. Biological Psychiatry 2006, 59:673-680.
59. Ren-Patterson R.F., Cochran L.W., Holmes A., Lesch K.P., Lu B., Murphy D.L. Gender-dependent modulation of brain monoamines and anxiety-like behaviors in mice with genetic serotonin transporter and BDNF deficiencies. Cellular and Molecular Neurobiology 2006, 26:755-780.
60. Koponen E., Võikar V., Riekki R., Saarelainen T., Rauramaa T., Rauvala H., et al. Transgenic mice overexpressing the full-length neurotrophin receptor trkB exhibit increased activation of the trkB-PLC gamma pathway, reduced anxiety, and facilitated learning. Molecular and Cellular Neurosciences 2004, 26(1):166-181.
61. Thome J., Sakai N., Shin K., Steffen C., Zhang Y.J., Impey S., et al. CAMP response element-mediated gene transcription is upregulated by chronic antidepressant treatment. Journal of Neuroscience 2000, 20:4030-4036.
62. Koponen E., Lakso M., Castrén E. Overexpression of the full-length neurotrophin receptor trkB regulates the expression of plasticity-related genes in mouse brain. Brain Research. Molecular Brain Research 2004, 130(1-2):81-94.
63. Silhol M., Arancibia S., Maurice T., Tapia-Arancibia L. Spatial memory training modifies the expression of brain-derive neurotrophic factor tyrosine kinase receptors in young and aged rats. Neuroscience 2007, 146(3):962-973.
64. Bracken B.K., Turrigiano G.G. Experience-dependent regulation of TrkB isoforms in rodent visual cortex. Development Neurobiology 2009, 69:267-278.
65. Weaver I.C., Cervoni N., Champagne F.A., D'Alessio A.C., Sharma S., Seckl J.R., et al. Epigenetic programming by maternal behavior. Nature Neuroscience 2004, 7:847-854.
66. Eisch A.J., Bolanos C.A., de Wit J., Simonak R.D., Pudiak C.M., Barrot M., et al. Brain-derived neurotrophic factor in the ventral midbrain-nucleus accumbens pathway: a role in depression. Biological Psychiatry 2003, 54:994-1005.
67. Berton O., McClung C.A., Dileone R.J., Krishnan V., Renthal W., Russo S.J., et al. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 2006, 311:864-868.
68. Marmigère F., Rage F., Tapia-Arancibia L. Regulation of brain-derived neurotrophic factor transcripts by neuronal activation in rat hypothalamic neurons. Journal of Neuroscience Research 2001, 66(3):377-389.
69. Silhol M., Bonnichon V., Rage F., Tapia-Arancibia L. Age-related changes in brain-derived neurotrophic factor and tyrosine kinase receptor isoforms in the hippocampus and hypothalamus in male rats. Neuroscience 2005, 132:613-624.
70. Zeeni N., Chaumontet C., Moyse E., Fromentin G., Tardivel C., Tome D., et al. A positive change in energy balance modulates TrkB expression in the hypothalamus and nodose ganglia of rats. Brain Research 2009, 1289:49-55.
71. Huber K., Kuehnel F., Wyatt S., Davies A.M. TrkB expression and early sensory neuron survival are independent of endogenous BDNF. Journal of Neuroscience Research 2000, 59(3):372-378.
72. + channel (ENaC), BDNF, and TrkB mRNA expression in the rat tongue. BMC Neuroscience 2009, 10:19.
73. Dutton A.C., Barnes N.M. 5-Hydroxytryptamine in the Central Nervous System. Handbook of Neurochemistry and Molecular Neurobiology: Neurotransmitter Systems 2008, 171-212. Springer Science and Business Media, LLC. Abel Lajtha (Ed.).
74. Tang A.C., Akers K.G., Reeb B.C., Romeo R.D., McEwen B.S. Programming social, cognitive, and neuroendocrine development by early exposure to novelty. Proceedings of the National Academy of Sciences of the United States of America 2006, 103(42):15716-15721.