Using animal models to disentangle the role of genetic, epigenetic, and environmental influences on behavioral outcomes associated with maternal anxiety and depression

Frontiers in Psychiatry

Volumn 2, Issue JUL, 2011, Pages

  Tarantino, Lisa M ^a   Sullivan, Patrick F ^a   Meltzer Brody, Samantha ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Anxiety; Bonding; Depression; Epigenetic; Genetic; Mice; Mothering; Perinatal

Indexed keywords

ANXIETY DISORDER; BEHAVIOR CHANGE; CLINICAL FEATURE; DISEASE ASSOCIATION; DISEASE MODEL; DNA METHYLATION; ENVIRONMENTAL FACTOR; EPIGENETICS; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENOTYPE ENVIRONMENT INTERACTION; HUMAN; LIFE STRESS; MATERNAL BEHAVIOR; MATERNAL CARE; MATERNAL STRESS; NONHUMAN; PATHOGENESIS; PUERPERAL DEPRESSION; REVIEW; STRAIN DIFFERENCE;

EID: 81855218559     PISSN: None     EISSN: 16640640     Source Type: Journal    
DOI: 10.3389/fpsyt.2011.00044     Document Type: Review

References (119)

1. Adrian, B. (2007). Perceptions of epige-netics. Nature 447, 396-398.
2. Anisman, H., Lacosta, S., Kent, P., McIn-tyre, D. C., and Merali, Z. (1998a). Stressor-induced corticotropin-releasing hormone, bombesin, ACTH and corticosterone variations in strains of mice differentially responsive to stressors. Stress 2, 209-220.
3. Anisman, H., Zaharia, M. D., Meaney, M. J., and Merali, Z. (1998b). Do early-life events permanently alter behavioral and hormonal responses to stressors? Int. J. Dev. Neurosci. 16, 149-164.
4. Anisman, H., and Matheson, K. (2005). Stress, depression, and anhedonia: caveats concerning animal models. Neurosci. Biobehav. Rev. 29, 525-546.
5. Anisman, H., Prakash, P., Merali, Z., and Poulter, M. O. (2007). Corticotropin releasing hormone receptor alterations elicited by acute and chronic unpredictable stressor challenges in stressor-susceptible and resilient strainsof mice. Behav. Brain Res. 181, 180-190.
6. Bartels, A., and Zeki, S. (2004). The neural correlates of maternal and romantic love. Neuroimage 21, 1155-1166.
7. Bennett, H. A., Einarson, A., Tad-dio, A., Koren, G., and Einarson, T. R. (2004). Prevalence of depression during pregnancy: systematic review. Obstet. Gynecol. 103, 698-709.
8. Beuzen, A., and Belzung, C. (1995). Link between emotional memory and anxiety states: a study by principal component analysis. Physiol. Behav. 58, 111-118.
9. Bhave, S. V., Hornbaker, C., Phang, T. L., Saba, L., Lapadat, R., Kechris, K., Gaydos, J., McGoldrick, D., Dolbey, A., Leach, S., Soriano, B., Ellington, A., Ellington, E., Jones, K., Mangion, J., Belknap, J. K., Williams, R. W., Hunter, L. E., Hoffman, P. L., and Tabakoff, B. (2007). The PhenoGen informatics website: tools for analyses of complex traits. BMC Genet. 8, 59. doi: 10.1186/1471-2156-8-59
10. Bloch, M., Daly, R. C., and Rubinow, D. R. (2003). Endocrine factors in the etiology of postpartum depression. Compr. Psychiatry 44, 234-246.
11. Bloch, M., Rubinow, D. R., Schmidt, P. J., Lotsikas, A., Chrousos, G. P., and Cizza, G. (2005). Corti-sol response to ovine corticotropin-releasing hormone in a model of pregnancy and parturition in euthymic women with and without a history of postpartum depression. J. Clin. Endocrinol. Metab. 90, 695-699.
12. Bloch, M., Schmidt, P. J., Danaceau, M., Murphy, J., Nieman, L., and Rubinow, D. R. (2000). Effects of gonadal steroids in women with a history of postpartum depression. Am. J. Psychiatry 157, 924-930.
13. Bridges, R., Zarrow, M. X., Gandelman, R., and Denenberg, V. H. (1972). Differences in maternal responsiveness between lactating and sensitized rats. Dev. Psychobiol. 5,123-127.
14. Brumariu, L. E., and Kerns, K. A. (2010a). Mother-child attachment patterns and different types of anxiety symptoms: is there specificityof relations? Child Psychiatry Hum. Dev. 41, 663-674.
15. Brumariu, L. E., and Kerns, K. A. (2010b). Parent-child attachment and internalizing symptoms in childhood and adolescence: a review of empirical findings and future directions. Dev. Psychopathol. 22, 177-203.
16. Brunton, P. J., and Russell, J. A. (2008). The expectant brain: adapting for motherhood. Nat. Rev. Neurosci. 9, 11-25.
17. Brunton, P. J., and Russell, J. A. (2010). Endocrine induced changes in brain function during pregnancy. Brain Res. 1364,198-215.
18. Butcher, L. M., and Beck, S. (2010). AutoMeDIP-seq: a high-throughput, whole genome, DNA methylation assay. Methods 52, 223-231.
19. Campbell, S. B., Brownell, C. A., Hungerford, A., Spieker, S. I., Mohan, R., and Blessing, J. S. (2004). The course of maternal depressive symptoms and maternal sensitivity as predictors of attachment security at 36 months. Dev. Psychopathol. 16, 231-252.
20. Carlier, M., Roubertoux, P., and Cohen-Salmon, C. (1982). Differences in patterns of pup care in Mus musculus domesticus l-Comparisons between eleven inbred strains. Behav. Neural Biol. 35,205-210.
21. Carola, V., D'Olimpio, F., Brunamonti, E., Mangia, F., and Renzi, P. (2002). Evaluation of the elevated plus-maze and open-field tests for the assessment of anxiety-related behaviour in inbred mice. Behav. Brain Res. 134, 49-57.
22. Champagne, F. A., Francis, D. D., Mar, A., and Meaney, M. J. (2003). Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Phys-iol Behav. 79, 359-371.
23. Champagne, F. A., and Meaney, M. J. (2007). Transgenerational effects of social environment on variations in maternal care and behavioral response to novelty. Behav. Neurosci. 121, 1353-1363.
24. Champagne, E A., Weaver, I. C., Dio-rio, J., Dymov, S., Szyf, M., and Meaney, M. J. (2006). Maternal care associated with methylation of the estrogen receptor-alpha1b promoter and estrogen receptor-alpha expression in the medial preoptic area of female offspring. Endocrinology 147, 2909-2915.
25. Chapillon, P., Manneche, C., Belzung, C., and Caston, J. (1999). Rearing environmental enrichment in two inbred strains of mice: 1. Effects on emotional reactivity. Behav. Genet. 29,41-46.
26. Charney, D. S., and Manji, H. K. (2004). Life stress, genes, and depression: multiple pathways lead to increased risk and new opportunities for intervention. Sci. STKE 2004, re5.
27. Churchill, G. A., Airey D. C., Allayee, H., Angel, J. M., Attie, A. D., Beatty, J., Beavis, W. D., Belknap, J. K., Bennett, B., Berrettini, W., Bleich, A., Bogue, M., Broman, K. W., Buck, K. J., Buckler, E., Burmeister, M., Chesler, E. J., Cheverud, J. M., Clapcote, S., Cook, M. N., Cox, R. D., Crabbe, J. C., Crusio, W. E., Darvasi, A., Deschep-per, C. F., Doerge, R. W., Farber, C. R., Forejt, J., Gaile, D., Garlow, S. J., Geiger, H., Gershenfeld, H., Gordon, T., Gu, J., Gu, W., de Haan, G., Hayes, N. L., Heller, C., Himmelbauer, H., Hitzemann, R., Hunter, K., Hsu, H. C., Iraqi, E A., Ivandic, B., Jacob, H. J., Jansen, R. C., Jepsen, K. J., Johnson, D. K., Johnson, T. E., Kem-permann, G., Kendziorski, C., Kotb, M., Kooy, R. F., Llamas, B., Lammert, E, Lassalle, J. M., Lowenstein, P. R., Lu, L., Lusis, A., Manly, K. F., Mar-cucio, R., Matthews, D., Medrano, J. F., Miller, D. R., Mittleman, G.,Mock, B. A., Mogil, J. S., Mon-tagutelli, X., Morahan, G., Morris, D. G., Mott, R., Nadeau, J. H., Nagase, H., Nowakowski, R. S., O'Hara, B. F., Osadchuk, A. V., Page, G. P., Paigen, B., Paigen, K., Palmer, A. A., Pan, H. J., Peltonen-Palotie. L, Peirce. J., Pomp, D., Pravenec, M., Prows, D. R., Qi, Z., Reeves, R. H., Roder, J., Rosen, G. D., Schadt, E. E., Schalk-wyk, L. C., Seltzer, Z., Shimomura, K., Shou, S., Sillanpää, M. J., Sira-cusa, L. D., Snoeck, H. W., Spearow, J. L., Svenson, K., Tarantino, L. M., Threadgill, D., Toth, L. A., Valdar, W., deVillena,F.P.,Warden,C.,Whatley, S., Williams, R. W., Wiltshire, T., Yi, N.,Zhang, D., Zhang, M, Zou, F.,. (2004).and Complex Trait Consortium, The collaborative cross, a community resource for the genetic analysis of complex traits. Nat. Genet. 36, 1133-1137.
28. Clancy, B., Darlington, R. B., and Fin-lay, B. L. (2001). Translating developmental time across mammalian species. Neuroscience 105, 7-17.
29. Crabbe, J. C., Wahlsten, D., and Dudek, B. C. (1999). Genetics of mouse behavior: interactions with laboratory environment. Science 284, 1670-1672.
30. Crawley, J. N., and Davis, L. G. (1982). Baseline exploratory activity predicts anxiolytic responsiveness to diazepam in five mouse strains. Brain Res. Bull. 8, 609-612.
31. Cryan, J. F., Mombereau, C., and Vas-sout, A. (2005). The tail suspension test as a model for assessing anti-depressant activity: review of pharmacological and genetic studies in mice. Neurosci. Biobehav. Rev. 29, 571-625.
32. Curley, J. P., Davidson, S., Bateson, P., and Champagne, E A. (2009). Social enrichment during postnatal development induces trans-generational effects on emotional and reproductive behavior in mice. Front. Behav. Neurosci. 3, 25. doi: 10.3389/neuro.08.025.2009
33. Curley, J. P., Jensen, C. L., Mashoodh, R., and Champagne, E A. (2011). Social influences on neurobiology and behavior: epigenetic effects during development. Psychoneuroen-docrinology 36, 352-371.
34. Cuthbert, B., and Insel, T. (2011). The data of diagnosis: new approaches to psychiatric classification. Psychiatry 73,311-314.
35. Davis, E. P., Snidman, N., Wadhwa, P. D., Glynn, L. M., Schetter, C. D., and Sandman, C. A. (2004). Prenatal maternal anxiety and depression predict negative behavioral reactivity in infancy. Infancy 6, 319-331.
36. Depino, A. M., and Gross, C. (2007). Simultaneous assessment of auto-nomic function and anxiety-related behavior in BALB/c and C57BL/6 mice. Behav. Brain Res. 177, 254-260.
37. Feldman, R., Granat, A., Pariente, C., Kanety, H., Kuint, J., and Gilboa-Schechtman, E. (2009). Maternal depression and anxiety across the postpartum year and infant social engagement, fear regulation, and stress reactivity. J. Am. Acad. Child Adolesc. Psychiatry 48, 919-927.
38. Field, T. (2010). Postpartum depression effects on early interactions, parenting, and safety practices: a review. Infant Behav. Dev. 33,1-6.
39. Fleming, A. S., and Corter, C. (1988). Factors influencing maternal responsiveness in humans: usefulness of an animal model. Psychoneuroendocrinology 13,189-212.
40. Flynn, H. A., Davis, M., Marcus, S. M., Cunningham, R., and Blow, E C. (2004). Rates of maternal depression in pediatric emergency department and relationship to child service utilization. Gen. Hosp. Psychiatry 26, 316-322.
41. Francis, D., Diorio, J., Liu, D., and Meaney, M. J. (1999a). Non-genomic transmission across generations of maternal behavior and stress responses in the rat. Science 286,1155-1158.
42. Francis, D. D., Champagne, F. A., Liu, D., and Meaney, M. J. (1999b). Maternal care, gene expression, and the development of individual differences in stress reactivity. Ann. N. Y. Acad. Sci. 896, 66-84.
43. Francis, D. D., Diorio, J., Plotsky, P. M., and Meaney, M. J. (2002). Environmental enrichment reverses the effects of maternal separation on stress reactivity. J. Neurosci. 22, 7840-7843.
44. Francis, D. D., and Meaney, M. J. (1999). Maternal care and the development of stress responses. Curr. Opin. Neu-robiol. 9,128-134.
45. Francis, D. D., Szegda, K., Campbell, G., Martin, W.D., and Insel, T.R. (2003). Epigenetic sources of behavioral differences in mice. Nat. Neurosci. 6, 445-446.
46. Franklin, T. B., Russig, H., Weiss, I. C., Gräff, J., Linder, N., Michalon, A., Vizi, S., and Mansuy, I. M. (2010). Epigenetic transmission of the impact of early stress across generations. Biol. Psychiatry 68, 408-415.
47. Galbally M., Lewis, A. J.,Ijzendoorn,M., and Permezel, M. (2011). The role of oxytocin in mother-infant relations: a systematic review of humanstudies. Harv. Rev. Psychiatry 19, 1-14.
48. Gavin, N. I., Gaynes, B. N., Lohr, K. N., Meltzer-Brody, S., Gartlehner, G., and Swinson, T. (2005). Perinatal depression: a systematic review of prevalence and incidence. Obstet. Gynecol. 106(5 Pt 1), 1071-1083.
49. Gaynes, B. N., Gavin, N., Meltzer-Brody, S., Lohr, K. N., Swinson, T., Gartlehner, G., Brody, S., and Miller, W. C. (2005). Perinatal depression: prevalence, screening accuracy, and screening outcomes. Evid. Rep. Technol. Assess. (Summ.) 119, 1-8.
50. Gluckman, P. D., Hanson, M. A., Cooper, C., and Thornburg, K. L. (2008). Effect of in utero and early-life conditions on adult health and disease. N. Engl. J. Med. 359, 61-73.
51. Griebel, G., Belzung, C., Perrault, G., and Sanger, D. J. (2000). Differences in anxiety-related behaviours and in sensitivity to diazepam in inbred and outbred strains of mice. Psychophar-macology (Berl.) 148, 164-170.
52. Insel, T., Cuthbert, B., Garvey, M., Heinssen, R., Pine, D. S., Quinn, K., Sanislow, C., and Wang, P. (2010). Research domain criteria (RDoC): toward a new classification framework for research on mental disorders. Am. J. Psychiatry 167, 748-751.
53. Jeddeloh, J. A., Greally, J. M., and Rando, O.J. (2008). Reduced-representation methylation mapping. Genome Biol. 9,231.
54. Jones, P. A., and Taylor, S. M. (1980). Cellular differentiation, cyti-dine analogs and DNA methylation. Cell 20, 85-93.
55. Kagan, J., Reznick, J. S., and Snidman, N. (1987). The physiology and psychology of behavioral inhibition in children. Child Dev. 58, 1459-1473.
56. Kammerer, M., Taylor, A., and Glover, V (2006). The HPA axis and perinatal depression: a hypothesis. Arch. Womens Ment. Health 9, 187-196.
57. Kendler, K. S., Karkowski, L. M., and Prescott, C. A. (1999). Causal relationship between stressful life events and the onset of major depression. Am. J. Psychiatry 156, 837-841.
58. Kriaucionis, S., and Heintz, N. (2009). The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 324, 929-930.
59. Krishnan, V., and Nestler, E. J. (2011). Animal models of depression: molecular perspectives. Curr. Top. Behav. Neurosci. 7, 121-147.
60. Li, N., Ye, M., Li, Y., Yan, Z., Butcher, L. M., Sun, J., Han, X., Chen, Q., Zhang, X., and Wang, J. (2010). Whole genome DNA methylation analysis based on high throughput sequencing technology. Methods 52, 203-212.
61. Lindahl, V., Pearson, J. L., and Colpe, L. (2005). Prevalence of suicidality during pregnancy and the postpar-tum. Arch. Womens Ment. Health 8, 77-87.
62. Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S., Pearson, D., Plotsky, P. M., and Meaney, M. J. (1997). Maternal care, hippocampal glucocorti-coid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277, 1659-1662.
63. Lucas, B. K., Ormandy, C. J., Binart, N., Bridges, R. S., and Kelly, P. A. (1998). Null mutation of the prolactin receptor gene produces a defect in maternal behavior. Endocrinology 139,4102-4107.
64. Magiakou, M. A., Mastorakos, G., Rabin, D., Dubbert, B., Gold, P. W., and Chrousos, G. P. (1996). Hypothalamic corticotropin-releasing hormone suppression during the postpartum period: implications for the increase in psychiatric manifestations at this time. J. Clin. Endocrinol. Metab. 81, 1912-1917.
65. Maguire, J., and Mody, I. (2008). GABA(A)R plasticity during pregnancy: relevance to postpartum depression. Neuron 59,207-213.
66. Mann, P. E., and Gervais, K. J. (2011). Environmental enrichment delays pup-induced maternal behavior in rats. Dev. Psychobiol. 53, 371-382.
67. Marmorstein, N. R., Malone, S. M., and Lacono, W G. (2004). Psychiatric disorders among offspring of depressed mothers: associations with paternal psy-chopathology. Am. J. Psychiatry 161, 1588-1594.
68. Mastorakos, G., and Ilias, I. (2003). Maternal and fetal hypothalamic-pituitary-adrenal axes during pregnancy and postpartum. Ann. N. Y. Acad. Sci. 997,136-149.
69. Meaney, M. J., and Szyf, M. (2005). Environmental programming of stress responses through DNA methylation: life at the interface between a dynamic environment and a fixed genome. Dialogues Clin. Neurosci. 7, 103-123.
70. Meltzer-Brody, S., Stuebe, A. M., Dole, N., Savitz, D., Rubinow, D., and Thorp, J. (2011). Elevated corticotropin releasing hormone (CRH) during pregnancy and risk of postpartum depression (PPD). J. Clin. Endocrinol. Metab. 96, E40-E47.
71. Merikangas, K. R., and Low, N. C. (2004). The epidemiology of mood disorders. Curr Psychiatry Rep 6, 411-421.
72. Metivier, R., Gallais, R., Tiffoche, C., Le Péron, C., Jurkowska, R. Z., Carmouche, R. P., Ibberson, D., Barath, P., Demay, F., Reid, G., Benes, V., Jeltsch, A., Gannon, F., and Salbert, G. (2008). Cyclical DNA methylation of a transcrip-tionally active promoter. Nature 452, 45-50.
73. Millstein, R. A., and Holmes, A. (2007). Effects of repeated maternal separation on anxiety- and depression-related phenotypes in different mouse strains. Neurosci. Biobehav. Rev. 31,3-17.
74. Mitchell,B. F.,andTaggart,M. J. (2009). Are animal models relevant to key aspects of human parturition? Am. J. Physiol. Regul. Integr. Comp. Physiol. 297, R525-R545.
75. Mouse Genome Sequencing Consortium, Waterston, R. H., Lindblad-Toh, K., Birney, E., Rogers, J., Abril, J. F., Agarwal, P., Agarwala, R., Ain-scough, R., Alexandersson, M., An, P., Antonarakis, S. E., Attwood, J., Baertsch, R., Bailey, J., Barlow, K., Beck, S., Berry, E., Birren, B., Bloom, T., Bork, P., Botcherby, M., Bray, N., Brent, M. R., Brown, D. G., Brown, S. D., Bult, C., Burton, J., Butler, J., Campbell, R. D., Carninci, P., Cawley, S., Chiaromonte, F., Chin-walla, A. T., Church, D. M., Clamp, M., Clee, C., Collins, E S., Cook, L. L., Copley, R. R., Coulson, A., Couronne, O., Cuff, J., Curwen, V., Cutts, T., Daly, M., David, R., Davies, J., Delehaunty, K. D., Deri, J., Der-mitzakis, E. T., Dewey, C., Dickens, N. J., Diekhans, M., Dodge, S., Dubchak, I., Dunn, D. M., Eddy, S. R., Elnitski, L., Emes, R. D., Eswara, P., Eyras, E., Felsenfeld, A., Fewell, G. A., Flicek, P., Foley, K., Frankel, W.N., Fulton, L. A., Fulton, R. S., Furey, T. S., Gage, D., Gibbs, R. A., Glusman, G., Gnerre, S., Goldman, N., Good-stadt, L., Grafham, D., Graves, T. A., Green, E. D., Gregory, S., Guigó, R., Guyer, M., Hardison, R. C., Haus-sler, D., Hayashizaki, Y., Hillier, L. W., Hinrichs, A., Hlavina, W., Holzer, T., Hsu, F., Hua, A., Hubbard, T., Hunt, A., Jackson, I., Jaffe, D. B., Johnson, L. S., Jones, M., Jones, T. A., Joy, A., Kamal, M., Karlsson, E. K., and et al. (2002). Initial sequencing and comparative analysis of the mouse genome. Nature 420,520-562.
76. NECCR, N. (1999). Chronicity of maternal depressive symptoms, maternal sensitivity, and child functioning at 36 months. NICHD Early Child Care Research Network. Dev. Psychol. 35, 1297-1310.
77. Nestler, E. J., and Hyman, S. E. (2010). Animal models of neuropsychi-atric disorders. Nat. Neurosci. 13, 1161-1169.
78. Neumann, I. D. (2002). Involvement of the brain oxytocin system in stress coping: interactions with the hypothalamo-pituitary-adrenal axis. Prog. Brain Res. 139,147-162.
79. Neumann, I. D. (2008). Brain oxytocin: a key regulator of emotional and social behaviours in both females and males. J. Neuroendocrinol. 20, 858-865.
80. Nolten, W E., Lindheimer, M. D., Rueckert, P. A., Oparil, S., and Ehrlich, E. N. (1980). Diurnal patterns and regulation of cor-tisol secretion in pregnancy. J. Clin. Endocrinol. Metab. 51, 466-472.
81. OConnor, T. G., Heron, J., Glover, V., and Alspac Study Team. (2002a). Antenatal anxiety predicts child behavioral/emotional problems independently of postnatal depression. J. Am. Acad. Child Adolesc. Psychiatry 41, 1470-1477.
82. Oconnor, T. G., Heron, J., Golding, J., Beveridge, M., and Glover, V. (2002b). Maternal antenatal anxiety and childrens behavioural/emotional problems at 4 years. Report from the Avon longitudinal study of parents and children. Br. J. Psychiatry 180, 502-508.
83. Ohara, M. W., and Swain, A. M. (1996). Rates and risk of postpartum depression-Ameta-analysis. Int. Rev. Psychiatry 8, 37-54.
84. Omahony, C. M., Bravo, J. A., Dinan, T. G., and Cryan, J. E. (2010a). Comparison of hippocampal metabotropic glutamate receptor 7 (mGlu7) mRNA levels in two animal models of depression. Neurosci. Lett. 482, 137-141.
85. Omahony, C. M., Sweeney, F. F., Daly, E., Dinan, T. G., and Cryan, J. E. (2010b). Restraint stress-induced brain activation patterns in two strains of mice differing in their anxiety behaviour. Behav. Brain Res. 213, 148-154.
86. OMahony, C. M., Clarke, G., Gibney, S., Dinan, T. G., and Cryan, J. E. (2011). Strain differences in the neurochem-ical response to chronic restraint stress in the rat: relevance to depression. Pharmacol. Biochem. Behav. 97, 690-699.
87. Parfitt, D. B., Levin, J. K., Saltstein, K. P., Klayman, A. S., Greer, L. M., and Helmreich, D. L. (2004). Differential early rearing environments can accentuate or attenuate the responses to stress in male C57BL/6 mice. Brain Res. 1016, 111-118.
88. Paulson, J. F., Dauber, S., and Leiferman, J. A. (2006). Individual and combined effects of postpartum depression in mothers and fathers on parenting behavior. Pediatrics 118, 659-668.
89. Pereira, M., Uriarte, N., Agrati, D., Zuluaga, M. J., and Ferreira, A. (2005). Motivational aspects of maternal anxiolysis in lactating rats. Psychopharmacology (Berl.) 180, 241-248.
90. Pokholok, D. K., Harbison, C. T., Levine, S., Cole, M., Hannett, N. M., Lee, T. I., Bell, G. W., Walker, K., Rolfe, P. A., Herbolsheimer, E., Zeitlinger, J., Lewitter, F., Gifford, D. K., and Young, R. A. (2005). Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122,517-527.
91. Post, A. M., Weyers, P., Holzer, P., Painsipp, E., Pauli, P., Wultsch, T., Reif, A., and Lesch, K. P. (2011). Gene-environment interaction influences anxiety-like behavior in ethologically based mouse models. Behav. Brain Res. 218, 99-105.
92. Poulter, M. O., Du, L., Zhurov, V., Merali, Z.,andAnisman,H. (2010). Plasticity of the GABA(A) receptor sub-unit cassette in response to stres-sors in reactive versus resilient mice. Neuroscience 165, 1039-1051.
93. Prakash, P., Merali, Z., Kolajova, M., Tannenbaum, B. M., and Anisman, H. (2006). Maternal factors and monoamine changes in stress-resilient and susceptible mice: cross-fostering effects. Brain Res. 1111, 122-133.
94. Priebe, K., Romeo, R. D., Francis, D. D., Sisti, H. M., Mueller, A., McEwen, B. S., and Brake, W. G. (2005). Maternal influences on adult stress and anxiety-like behavior in C57BL/6J and BALB/cJ mice: a cross-fostering study. Dev. Psychobiol. 47, 398-407.
95. Rahman, A., Iqbal,Z., Bunn,J., Lovel, H., and Harrington, R. (2004). Impact of maternal depression on infant nutritional status and illness: a cohort study. Arch. Gen. Psychiatry 61,946-952.
96. Razin, A. (1998). CpG methylation chromatin structure and gene silencing-a three-way connection. EMBOJ. 17,4905-4908.
97. Rich-Edwards, J. W., Mohllajee, A. P., Kleinman, K., Hacker, M. R., Maj-zoub, J., Wright, R. J., and Gillman, M. W. (2008). Elevated midpreg-nancy corticotropin-releasing hormone is associated with prenatal, but not postpartum, maternal depression. J. Clin. Endocrinol. Metab. 93, 1946-1951.
98. Ring, R. H., Malberg, J. E., Potes-tio, L., Ping, J., Boikess, S., Luo, B., Schechter, L. E., Rizzo, S., Rahman, Z., and Rosenzweig-Lipson, S. (2006). Anxiolytic-like activity of oxytocin in male mice: behavioral and autonomic evidence, therapeutic implications. Psychopharmacol-ogy(Berl.) 185,218-225.
99. Rogers, D. C., Jones, D. N., Nelson, P. R., Jones, C. M., Quilter, C. A., Robinson, T. L., and Hagan, J. J. (1999). Use of SHIRPA and discriminant analysis to characterise marked differences in the behavioural pheno-type of six inbred mouse strains. Behav. Brain Res. 105,207-217.
100. Romeo, R. D., Mueller, A., Sisti, H. M., Ogawa, S., McEwen, B. S., and Brake, W G. (2003). Anxiety and fear behaviors in adult male and female C57BL/6 mice are modulated by maternal separation. Horm. Behav. 43, 561-567.
101. Ross, L. E., and Dennis, C. L. (2009). The prevalence of postpartum depression amongst women with substance use, an abuse history, or chronic illness: a systematic review. J. Womens Health 18, 475-486.
102. Shanks, N., and Anisman, H. (1988). Stressor-provoked behavioral changes in six strains of mice. Behav. Neurosci. 102, 894-905.
103. Shanks, N., Griffiths, J., and Anisman, H. (1994). Central catecholamine alterations induced by stressor exposure: analyses in recombinant inbred strains of mice. Behav. Brain Res. 63, 25-33.
104. Silverman, M. E., Loudon, H., Safier, M., Protopopescu, X., Leiter, G., Liu, X., and Goldstein, M. (2007). Neural dysfunction in postpartum depression: an fMRI pilot study. CNS Spectr. 12, 853-862.
105. Skinner, M. K., Manikkam, M., and Guerrero-Bosagna, C. (2010). Epi-genetic transgenerational actions of environmental factors in disease etiology. Trends Endocrinol. Metab. 21, 214-222.
106. Smith, M. V., Shao, L., Howell, H., Lin, H., and Yonkers, K. A. (2011). Perinatal depression and birth outcomes in a Healthy Start project. Matern Child HealthJ. 15,401-409.
107. Swain, J. E. (2008). Baby stimuli and the parent brain: functional neu-roimaging of the neural substrates of parent-infant attachment. Psychiatry (Edgmont) 5, 28-36.
108. Swain, J. E., Lorberbaum, J. P., Kose, S., and Strathearn, L. (2007). Brain basis of early parent-infant interactions: psychology, physiology, and in vivo functional neuroimaging studies. J. Child. Psychol. Psychiatry 48, 262-287.
109. Talge, N. M., Neal, C., Glover, V., and Early Stress, Translational Research and Prevention Science Network: Fetal and Neonatal Experience on Child and Adolescent Mental Health. (2007). Antenatal maternal stress and long-term effects on child neurodevelopment: how and why? J Child Psychol. Psychiatry 48, 245-261.
110. Tang, X., Orchard, S. M., and Sanford, L. D. (2002). Home cage activity and behavioral performance in inbred and hybrid mice. Behav. Brain Res. 136, 555-569.
111. Tarantino, L. M., and Bucan, M. (2000). Dissection of behavior and psychiatric disorders using the mouse as a model. Hum. Mol. Genet. 9,953-965.
112. Trullas, R., and Skolnick, P. (1993). Differences in fear motivated behaviors among inbred mouse strains. Psychopharmacology (Berl.) 111, 323-331.
113. Van den Bergh, B. R., and Marcoen, A. (2004). High antenatal maternal anxiety is related to ADHD symptoms, externalizing problems, and anxiety in 8- and 9-year-olds. Child Dev. 75, 1085-1097.
114. Van den Bergh, B. R., Mennes, M., Oost-erlaan, J., Stevens, V., Stiers, P., Marcoen, A., and Lagae, L. (2005). High antenatal maternal anxiety is related to impulsivity during performance on cognitive tasks in 14- and 15-year-olds. Neurosci. Biobehav. Rev. 29,259-269.
115. Wan, M. W., and Green, J. (2009). The impact of maternal psychopathol-ogy on child-mother attachment. Arch. Womens Ment. Health 12, 123-134.
116. Weaver, I. C., Cervoni, N., Champagne, F. A., DAlessio, A. C., Sharma, S., Seckl, J. R., Dymov, S., Szyf, M., and Meaney, M. J. (2004). Epigenetic programming by maternal behavior. Nat. Neurosci. 7, 847-854.
117. Weinberg, M. K., and Tronick, E. Z. (1998). The impact of maternal psychiatric illness on infant development. J. Clin. Psychiatry 59(Suppl. 2), 53-61.
118. Yan, H. C., Cao, X., Das, M., Zhu, X. H., and Gao, T. M. (2010). Behavioral animal models of depression. Neurosci. Bull. 26, 327-337.
119. Zacharko, R. M., and Anisman, H. (1989). "Pharmacological, biochemical and behavioral analyses of depression: animal models," in Animal Models of Depression, eds G. F. Koob, C. L. Ehlers, and D. J. Kupfer (Boston: Birkhauser), 204-238.