Long-term postpartum anxiety and depression-like behavior in mother rats subjected to maternal separation are ameliorated by palatable high fat diet

Behavioural Brain Research

Volumn 208, Issue 1, 2010, Pages 72-79

  Maniam, Jayanthi ^a   Morris, Margaret J ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Anxiety; Behavior; Corticosterone; Dams; Depression; High fat diet; Maternal separation; Neuropeptides

Indexed keywords

CORTICOSTERONE; GLUCOCORTICOID RECEPTOR; INSULIN; LEPTIN; MESSENGER RNA; NEUROPEPTIDE Y; CORTICOTROPIN RELEASING FACTOR; CORTICOTROPIN RELEASING HORMONE (9 41); CORTICOTROPIN RELEASING HORMONE (9-41); PEPTIDE FRAGMENT; SUCROSE; SWEETENING AGENT;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; BODY WEIGHT; BRAIN TISSUE; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; FEMALE; FORCED SWIMMING TEST; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LIPID DIET; MALE; MATERNAL DEPRIVATION; MAZE TEST; NONHUMAN; PRIORITY JOURNAL; PUERPERAL DEPRESSION; RAT; WHITE ADIPOSE TISSUE; ADIPOSE TISSUE; AGE; ANALYSIS OF VARIANCE; ANIMAL; BLOOD; BRAIN; DIET THERAPY; DISEASE MODEL; DRUG EFFECT; FAT INTAKE; FOOD PREFERENCE; GENETICS; METABOLISM; NEWBORN; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGICAL ASPECT; SPRAGUE DAWLEY RAT; SWIMMING;

ADIPOSE TISSUE; AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; ANXIETY; BODY WEIGHT; BRAIN; CORTICOSTERONE; CORTICOTROPIN-RELEASING HORMONE; DEPRESSION, POSTPARTUM; DIETARY FATS; DISEASE MODELS, ANIMAL; FEMALE; FOOD PREFERENCES; MALE; MATERNAL DEPRIVATION; MAZE LEARNING; NEUROPEPTIDE Y; PEPTIDE FRAGMENTS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SUCROSE; SWEETENING AGENTS; SWIMMING;

EID: 77951913306     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2009.11.005     Document Type: Article

References (72)

1. Beck C. Predictors of postpartum depression: an update. Nurs Res 2001, 50:275-285.
2. Bennett H.A., Taddio A., Koren G., Einarson T.R. Prevalence of depression during pregnancy:systematic review. Obstet Gynecol 2004, 103:698-709.
3. Halbreich U. Postpartum disorders: multiple interacting underlying mechanisms and risk factors. J Affect Disord 2005, 88:1-7.
4. Pearlstein T., Howard M., Salisbury A., Zlotnick C. Postpartum depression. Am J Obstet Gynecol 2009, 200:357-364.
5. Boccia M.L., Razzoli M., Prasad Vadlamudi S., Trumbull W., Caleffie C., Pedersen C.A. Repeated long separations from pups produce depression-like behavior in rat mothers. Psychoneuroendocrinology 2007, 32:65-71.
6. Macri S., Chiarotti F., Wurbel H. Maternal separation and maternal care act independently on the development of HPA responses in male rats. Behav Brain Res 2008, 191:227-234.
7. Macri S., Mason G.J., Wurbel H. Dissociation in the effects of neonatal maternal separations on maternal care and the offspring's HPA and fear responses in rats. Eur J Neurosci 2004, 20:1017-1024.
8. 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. Proc Nat Acad Sci USA 1998, 95:5335-5340.
9. Pryce C.R., Feldon J. Long-term neurobehavioural impact of the postnatal environment in rats: manipulations, effects and mediating mechanisms. Neurosci Biobehav Rev 2003, 27:57-71.
10. Marais L., van Rensburg S.J., van Zyl J.M., Stein D.J., Daniels W.M. Maternal separation of rat pups increases the risk of developing depressive-like behavior after subsequent chronic stress by altering corticosterone and neurotrophin levels in the hippocampus. Neurosci Res 2008, 61:106-112.
11. Huot R.L., Thrivikraman K.V., Meaney M.J., Plotsky P.M. Development of adult ethanol preference and anxiety as a consequence of neonatal maternal separation in Long Evans rats and reversal with antidepressant treatment. Psychopharmacology 2001, 158:366-373.
12. Colorado R.A., Shumake J., Conejo N.M., Gonzalez-Pardo H., Gonzalez-Lima F. Effects of maternal separation, early handling, and standard facility rearing on orienting and impulsive behavior of adolescent rats. Behav Process 2006, 71:51-58.
13. Millstein R.A., Holmes A. Effects of repeated maternal separation on anxiety and depression-related phenotypes in different mouse strains. Neurosci Biobehav Rev 2006, 1-15.
14. Ladd C.O., Thrivikraman K.V., Huot R.L., Plotsky P.M. Differential neuroendocrine responses to chronic variable stress in adult Long Evans rats exposed to handling-maternal separation as neonates. Psychoneuroendocrinology 2005, 30:520-533.
15. Ladd C.O., Huot R.L., Thrivikraman K.V., Nemeroff C.B., Plotsky P.M. Long-term adaptations in glucocorticoid receptor and mineralocorticoid receptor mRNA and negative feedback on the hypothalamo-pituitary-adrenal axis following neonatal maternal separation. Biol Psychiatry 2004, 55:367-375.
16. Meaney M.J., Diorio J., Francis D., Widdowson J., LaPlante P., Caldji C., et al. Early environmental regulation of forebrain glucocorticoid receptor gene expression: implications for adrenocortical responses to stress. Dev Neurosci 1996, 18:49-72.
17. Alberts J.R., Gubernick D.J. Reciprocity and resource exchange. A symbiotic model of parent-offspring relations. Symbiosis in parent-offspring interactions 1983, 7-44. Plenum Press, New York. L.A. Rosenblum, H. Moltz (Eds.).
18. Banky Z., Nagy G.M., Halasz B. Effect of various partial separations of the litters from their mother on plasma prolactin levels of lactating rats. Acta Biol Hung 1994, 45:169-178.
19. Cheng H.W., Muir W.M. Chronic social stress differentially regulates neuroendocrine responses in laying hens: II. Genetic basis of adrenal responses under three different social conditions. Psychoneuroendocrinology 2004, 29:961-971.
20. Ulrich-Lai Y.M., Figueiredo H.F., Ostrander M.M., Choi D.C., Engeland W.C., Herman J.P. Chronic stress induces adrenal hyperplasia and hypertrophy in a subregion-specific manner. Am J Physiol Endocrinol Metab 2006, 291:E965-973.
21. Eklund M.B., Johansson L.M., Uvnas-Moberg K., Arborelius L. Differential effects of repeated long and brief maternal separation on behaviour and neuroendocrine parameters in Wistar dams. Behav Brain Res 2009, 203:69-75.
22. Salzberg M., Kumar G., Supit L., Jones N.C., Morris M.J., Rees S., et al. Early postnatal stress confers enduring vulnerability to limbic epileptogenesis. Epilepsia 2007, 48:2079-2085.
23. Fleming A.S., Rosenblatt J.S. Maternal behavior in the virgin and lactating rat. J Comp Physiol Psychol 1974, 86:957-972.
24. Leon M., Croskerry P.G., Smith G.K. Thermal control of mother-young contact in rats. Physiol Behav 1978, 21:790-811.
25. Kalinichev M., Easterling K.W., Holtzman S.G. Periodic postpartum separation from the offspring results in long-lasting changes in anxiety-related behaviors and sensitivity to morphine in Long-Evans mother rats. Psychopharmacology 2000, 152:431-439.
26. Kalinichev M., Easterling K.W. Holtzman SG.Repeated neonatal maternal separation alters morphine-induced antinociception in male rats. Brain Res Bull 2001, 54:649-654.
27. Kallen V.L., Tulen J.H., Utens E.M., Treffers P.D., De Jong F.H., Ferdinand R.F. Associations between HPA axis functioning and level of anxiety in children and adolescents with an anxiety disorder. Depress Anxiety 2008, 25:131-141.
28. Kara S., Yazici K.M., Gulec C., Unsal I. Mixed anxiety-depressive disorder and major depressive disorder: comparison of the severity of illness and biological variables. Psychiatry Res 2000, 94:59-66.
29. Tafet G.E., Bernardini R. Psychoneuroendocrinological links between chronic stress and depression. Prog Neuropsychopharmacol Biol Psychiatry 2003, 27:893-903.
30. van Gaalen M.M., Reul J.H., Gesing A., Stenzel-Poore M.P., Holsboer F., Steckler T. Mice overexpressing CRH show reduced responsiveness in plasma corticosterone after a5-HT1A receptor challenge. Genes Brain Behav 2002, 1:174-177.
31. Chrousos G.P. The role of stress and the hypothalamic-pituitary-adrenal axis in the pathogenesis of the metabolic syndrome: neuro-endocrine and target tissue-related causes. Int J Obes Relat Metab Disord 2000, 24:S50-55.
32. Wilcoxon J.S., Redei E.E. Maternal glucocorticoid deficit affects hypothalamic-pituitary-adrenal function and behavior of rat offspring. Horm Behav 2007, 51:321-327.
33. Rosmond R., Chagnon Y.C., Holm G., Chagnon M., Perusse L., Lindell K., et al. A glucocorticoid receptor gene marker is associated with abdominal obesity, leptin, and dysregulation of the hypothalamic-pituitary-adrenal axis. Obes Res 2000, 8:211-218.
34. la Fleur S.E., Houshyar H., Roy M., Dallman M.F. Choice of lard, but not total lard calories, damps adrenocorticotropin responses to restraint. Endocrinology 2005, 146:2193-2199.
35. Dallman M.F., Pecoraro N.C., la Fleur S.E. Chronic stress and comfort foods: self-medication and abdominal obesity. Brain Behav Immun 2005, 19:275-280.
36. Adam T.C., Epel E.S. Stress, eating, and the reward system. Physiol Behav 2007, 91:449-458.
37. Oliver G., Wardle J., Gibson E.L. Stress and food choice: a laboratory study. Psychosom Med 2000, 62:853-865.
38. Parker G., Crawford J. Chocolate craving when depressed: a personality marker. Bri J Psychiatry 2007, 191:351-352.
39. Parker G., Parker I., Brotchie H. Mood state effects of chocolate. J Affect Disord 2006, 92:149-159.
40. American Psychiatric Association Diagnostic and statistical manual of mental disorders 2000, American Psychiatric Association, Washington, DC.
41. Jones N.C., Cardamone L., Williams J.P., Salzberg M.R., Myers D., O'Brien T.J. Experimental traumatic brain injury induces a pervasive hyperanxious phenotype in rats. J Neurotrauma 2008, 25:1367-1374.
42. Porsolt R.D., Le Pichon M., Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nature 1977, 266:730-732.
43. Michelle J.H., Valentina J., Margaret J.M. Adaptive responses in hypothalamic neuropeptide Y in the face of prolonged high-fat feeding in the rat. J Neurochem 2004, 88:909-916.
44. Velkoska E., Cole T.J., Morris M.J. Early dietary intervention: long-term effects on blood pressure, brain neuropeptide Y, and adiposity markers. Am J Physiol Endocrinol Metab 2005, 288:E1236-1243.
45. Morris M.J., Velkoska E., Cole T.J. Central and peripheral contributions to obesity-associated hypertension: impact of early overnourishment. Exp Physiol 2005, 90:697-702.
46. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 2001, 25:402-408.
47. Lovic V., Gonzalez A., Fleming A.S. Maternally separated rats show deficits in maternal care in adulthood. Dev Psychobiol 2001, 39:19-33.
48. Boccia M.L., Pedersen C.A. Brief vs. long maternal separations in infancy: contrasting relationships with adult maternal behavior and lactation levels of aggression and anxiety. Psychoneuroendocrinology 2001, 26:657-672.
49. Jaworski J.N., Francis D.D., Brommer C.L., Morgan E.T., Kuhar M.J. Effects of early maternal separation on ethanol intake, GABA receptors and metabolizing enzymes in adult rats. Psychopharmacology 2005, 181:8-15.
50. Michaels C.C., Holtzman S.G. Enhanced sensitivity to naltrexone-induced drinking suppression of fluid intake and sucrose consumption in maternally separated rats. Pharmacol Biochem Behav 2007, 86:784-796.
51. Michaels C.C., Holtzman S.G. Neonatal stress and litter composition alter sucrose intake in both rat dam and offspring. Physiol Behav 2006, 89:735-741.
52. Dal-Zotto S., Martí O., Armario A. Influence of single or repeated experience of rats with forced swimming on behavioural and physiological responses to the stressor. Behav Brain Res 2000, 114:175-181.
53. Giakoumaki O., Vasilaki K., Lili L., Skouroliakou M., Liosis G. The role of maternal anxiety in the early postpartum period: screening for anxiety and depressive symptomatology in Greece. J Psychos Obstet Gynecol 2009, 30:21-28.
54. Figueiredo B., Costa R. Mother's stress, mood and emotional involvement with the infant: 3 months before and 3 months after childbirth. Arch Womens Ment Health 2009, 12:143-153.
55. Greaves-Lord K., Ferdinand R.F., Oldehinkel A.J., Sondeijker F.E., Ormel J., Verhulst F.C. Higher cortisol awakening response in young adolescents with persistent anxiety problems. Acta Psychiatr Scand 2007, 116:137-144.
56. Pecoraro N., Reyes F., Gomez F., Bhargava A., Dallman M.F. Chronic stress promotes palatable feeding, which reduces signs of stress: feedforward and feedback effects of chronic stress. Endocrinology 2004, 145:3754-3762.
57. Buwalda B., Blom W.A., Koolhaas J.M., van Dijk G. Behavioral and physiological responses to stress are affected by high-fat feeding in male rats. Physiol Behav 2001, 73:371-377.
58. Prasad A., Prasad C. Short-term consumption of a diet rich in fat decreases anxiety response in adult male rats. Physiol Behav 1996, 60:1039-1042.
59. Levin B.E., Richard D., Michel C., Servatius R. Differential stress responsivity in diet-induced obese and resistant rats. Am J Physiol Regul Integr Comp Physiol 2000, 279:R1357-R1364.
60. Legendre A., Papakonstantinou E., Roy M.-C., Richard D., Harris R.B.S. Differences in response to corticotropin-releasing factor after short- and long-term consumption of a high-fat diet. Am J Physiol Regul Integr Comp Physiol 2007, 293:R1076-1085.
61. Shiraev T., Chen H., Morris M.J. Differential effects of restricted versus unlimited high-fat feeding in rats on fat mass, plasma hormones and brain appetite regulators. J Neuroendocrinol 2009, 21:602-609.
62. Ladd C.O., Thrivikraman K.V., Rebecca L.H., Plotsky P.M. Differential neuroendocrine responses to chronic variable stress in adult Long Evans rats exposed to handling-maternal separation as neonates. Psychoneuroendocrinology 2005, 30:520-533.
63. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 2001, 24:1161-1192.
64. Weaver C.I., Cervoni N., Champagne F.A., D'Alessio A.C., Sharma S., Seckl J.R., et al. Epigenetic programming by maternal behaviour. Nat Neurosci 2004, 7:847-853.
65. Michel C., Levin B.E., Dunn-Meynell A.A. Stress facilitates body weight gain in genetically predisposed rats on medium-fat diet. Am J Physiol Regul Integr Comp Physiol 2003, 285:R791-799.
66. Gehlert D.R. Role of hypothalamic neuropeptide Y in feeding and obesity. Neuropeptides 1999, 33:329-338.
67. Miller C.C., Holmes P.V., Edwards G.L. Area postrema lesions elevate NPY levels and decrease anxiety-related behavior in rats. Physiol Behav 2002, 77:135-140.
68. Heilig M. The NPY system in stress, anxiety and depression. Neuropeptides 2004, 38:213-224.
69. Thorsell A.K. Central neuropeptide Y in anxiety- and stress-related behavior and in ethanol intake. Ann NY Acad Sci 2008, 1148:136-140.
70. Karl T., Duffy L., Herzog H. Behavioural profile of a new mouse model for NPY deficiency. Eu J Neurosci 2008, 28:173-180.
71. Erickson J.C., Clegg K.E., Palmiter R.D. Sensitivity to leptin and susceptibility to seizures of mice lacking neuropeptide Y. Nature 1996, 381:415-421.
72. Heilig M., McLeod S., Brot M., Heinrichs S.C., Menzaghi F., Koob G.F., et al. Anxiolytic-like action of neuropeptide Y: mediation by Y1 receptors in amygdala, and dissociation from food intake effects. Neuropsychopharmacology 1993, 8:357-363.