Social stress during lactation, depressed maternal care, and neuropeptidergic gene expression

Behavioural Pharmacology

Volumn 26, Issue , 2015, Pages 642-653

  Murgatroyd, Christopher A ^a   Taliefar, Mohammad ^a   Bradburn, Steven ^a   Carini, Lindsay M ^b   Babb, Jessica A ^b   Nephew, Benjamin C ^b  

^a MANCHESTER METROPOLITAN UNIVERSITY   (United Kingdom)

^b TUFTS UNIVERSITY   (United States)

Author keywords

anxiety; gene expression; lactation; maternal care; postpartum depression; rat; social stress

Indexed keywords

ARGIPRESSIN; CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR; DNA; ESTRADIOL; GLUCOCORTICOID RECEPTOR; MESSENGER RNA; MINERALOCORTICOID RECEPTOR; NEUROPEPTIDE; OREXIN 2 RECEPTOR; OXYTOCIN; OXYTOCIN RECEPTOR; PROLACTIN; SACCHARIN; OREXIN RECEPTOR;

AGGRESSION; ANHEDONIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR CHANGE; BINDING SITE; BRAIN REGION; CALORIC DENSITY; CHRONIC SOCIAL STRESS; CHRONIC STRESS; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; CPG ISLAND; DNA METHYLATION; ESTRADIOL BLOOD LEVEL; FEMALE; FLUID INTAKE; GENE EXPRESSION; GROOMING; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; LACTATION; LOCOMOTION; MATERNAL CARE; MEDIAL AMYGDALA; NONHUMAN; PROMOTER REGION; PUERPERAL DEPRESSION; RAT; SOCIAL STRESS; SUPRAOPTIC NUCLEUS; ANIMAL; ANXIETY DISORDER; BRAIN; CHRONIC DISEASE; DISEASE MODEL; MATERNAL BEHAVIOR; MENTAL STRESS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY; SOCIAL BEHAVIOR; SPRAGUE DAWLEY RAT; TASTE;

AGGRESSION; ANHEDONIA; ANIMALS; ANXIETY DISORDERS; BRAIN; CHRONIC DISEASE; DEPRESSION, POSTPARTUM; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION; LACTATION; MATERNAL BEHAVIOR; OREXIN RECEPTORS; OXYTOCIN; RATS, SPRAGUE-DAWLEY; RECEPTORS, GLUCOCORTICOID; RNA, MESSENGER; SACCHARIN; SOCIAL BEHAVIOR; STRESS, PSYCHOLOGICAL; TASTE PERCEPTION;

EID: 84942123443     PISSN: 09558810     EISSN: 14735849     Source Type: Journal    
DOI: 10.1097/FBP.0000000000000147     Document Type: Article

References (96)

1. Adewuya AO, Ola BO, Aloba OO, Mapayi BM, Okeniyi JA (2008). Impact of postnatal depression on infants' growth in Nigeria. J Affect Disord 108:191-193.
2. Arendt DH, Ronan PJ, Oliver KD, Callahan LB, Summers TR, Summers CH(2013). Depressive behavior and activation of the orexin/hypocretin system. Behav Neurosci 127:86-94.
3. Babb JA, Carini LM, Spears SL, Nephew BC (2014). Transgenerational effects of social stress on social behavior, corticosterone, oxytocin, and prolactin in rats. Horm Behav 65:386-393.
4. Beebe B, Jaffe J, Buck K, Chen H, Cohen P, Feldstein S, Andrews H (2008). Sixweek postpartum maternal depressive symptoms and 4-month mother-infant self- and interactive contingency. Infant Ment Health J 29:442-471.
5. Bernstein IH, Rush AJ, Yonkers K, Carmody TJ, Woo A, McConnell K, Trivedi MH (2008). Symptom features of postpartum depression: are they distinct?Depress Anxiety 25:20-26.
6. Bettscheider M, Murgatroyd C, Spengler D (2011). Simultaneous DNA and RNA isolation from brain punches for epigenetics. BMC research notes 4:314.
7. Bloch M, Schmidt PJ, Danaceau M, Murphy J, Nieman L, Rubinow DR (2000). Effects of gonadal steroids in women with a history of postpartum depression. Am J Psychiatry 157:924-930.
8. Bloch M, Daly RC, Rubinow DR (2003). Endocrine factors in the etiology of postpartum depression. Compr Psychiatry 44:234-246.
9. Bosch OJ, Neumann ID (2012). Both oxytocin and vasopressin are mediators of maternal care and aggression in rodents: from central release to sites of action. Horm Behav 61:293-303.
10. Brummelte S, Galea LA (2010). Chronic corticosterone during pregnancy and postpartum affects maternal care, cell proliferation and depressive-like behavior in the dam. Horm Behav 58:769-779.
11. Brummelte S, Pawluski JL, Galea LA (2006). High post-partum levels of corticosterone given to dams influence postnatal hippocampal cell proliferation and behavior of offspring: A model of post-partum stress and possible depression. Horm Behav 50:370-382.
12. Byrnes EM, Rigero BA, Bridges RS (2000). Opioid receptor antagonism during early lactation results in the increased duration of nursing bouts. Physiol Behav 70:211-216.
13. Callahan LB, Tschetter KE, Ronan PJ (2013). Inhibition of corticotropin releasing factor expression in the central nucleus of the amygdala attenuates stress-induced behavioral and endocrine responses. Front Neurosci 7:195.
14. Campbell A (2008). Attachment, aggression and affiliation: the role of oxytocin in female social behavior. Biol Psychol 77:1-10.
15. Carini LM, Nephew BC (2013). Effects of early life social stress on endocrinology, maternal behavior, and lactation in rats. Horm Behav 64:634-641.
16. Carini LM, Murgatroyd CA, Nephew BC (2013). Using chronic social stress to model postpartum depression in lactating rodents. J Vis Exp e50324.
17. Champagne FA, Francis DD, Mar A, Meaney MJ (2003). Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol Behav 79:359-371.
18. Cox ET, Hodge CW, Sheikh MJ, Abramowitz AC, Jones GF, Jamieson-Drake AW, et al. (2012). Delayed developmental changes in neonatal vocalizations correlates with variations in ventral medial hypothalamus and central amygdala development in the rodent infant: effects of prenatal cocaine. Behav Brain Res 235:166-175.
19. Cyranowski JM, Hofkens TL, Frank E, Seltman H, Cai HM, Amico JA (2008). Evidence of dysregulated peripheral oxytocin release among depressed women. Psychosom Med 70:967-975.
20. D'Anna KL, Gammie SC (2006). Hypocretin-1 dose-dependently modulates maternal behaviour in mice. J Neuroendocrinol 18:553-566.
21. D'Anna KL, Gammie SC (2009). Activation of corticotropin-releasing factor receptor 2 in lateral septum negatively regulates maternal defense. Behav Neurosci 123:356-368.
22. Dennis CL, McQueen K (2009). The relationship between infant-feeding outcomes and postpartum depression: a qualitative systematic review. Pediatrics 123:e736-e751.
23. Di Sebastiano AR, Coolen LM (2012). Orexin and natural reward: feeding, maternal, and male sexual behavior. Prog Brain Res 198:65-77.
24. Donaldson ZR, Young LJ (2008). Oxytocin, vasopressin, and the neurogenetics of sociality. Science 322:900-904.
25. Essex MJ, Shirtcliff EA, Burk LR, Ruttle PL, Klein MH, Slattery MJ, et al. (2011). Influence of early life stress on later hypothalamic-pituitary-adrenal axis functioning and its covariation with mental health symptoms: a study of the allostatic process from childhood into adolescence. Dev Psychopathol 23:1039-1058.
26. Feldman R, Granat A, Pariente C, Kanety H, Kuint J, 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.
27. Feng P, Vurbic D, Wu Z, Strohl KP(2007). Brain orexins and wake regulation in rats exposed to maternal deprivation. Brain Res 18:163-172.
28. Ferris C (2014). Using awake animal imaging to understand neural circuits of emotion: studies ranging from maternal care to aggression. In: Decety J, Christen Y, editors. New Frontiers in Social Neuroscience.New York, NY: Springer International Publishing. pp. 111-126.
29. Ferris CF, Kulkarni P, Sullivan JM Jr, Harder JA, Messenger TL, Febo M (2005). Pup suckling is more rewarding than cocaine: evidence from functional magnetic resonance imaging and three-dimensional computational analysis. J Neurosci 25:149-156.
30. Figueiredo B, Canário C, Field T (2014). Breastfeeding is negatively affected by prenatal depression and reduces postpartum depression. Psychol Med 44:927-936.
31. Forman DR, O'Hara MW, Stuart S, Gorman LL, Larsen KE, Coy KC (2007). Effective treatment for postpartum depression is not sufficient to improve the developing mother-child relationship. Dev Psychopathol 19:585-602.
32. Gammie SC, Negron A, Newman SM, Rhodes JS (2004). Corticotropin-releasing factor inhibits maternal aggression in mice. Behav Neurosci 118:805-814.
33. Gammie SC, Seasholtz AF, Stevenson SA (2008). Deletion of corticotropin-releasing factor binding protein selectively impairs maternal, but not intermale aggression. Neuroscience 157:502-512.
34. Giovenardi M, Padoin MJ, Cadore LP, Lucion AB (1997). Hypothalamic paraventricular nucleus, oxytocin, and maternal aggression in rats. Ann N Y Acad Sci 807:606-609.
35. Giovenardi M, Padoin MJ, Cadore LP, Lucion AB (1998). Hypothalamic paraventricular nucleus modulates maternal aggression in rats: effects of ibotenic acid lesion and oxytocin antisense. Physiol Behav 63:351-359.
36. Goodman SH, Rouse MH, Connell AM, Broth MR, Hall CM, Heyward D (2011). Maternal depression and child psychopathology: a meta-analytic review. Clin Child Fam Psychol Rev 14:1-27.
37. Grace SL, Evindar A, Stewart DE (2003). The effect of postpartum depression on child cognitive development and behavior: a review and critical analysis of the literature. Arch Womens Ment Health 6:263-274.
38. Gress-Smith JL, Luecken LJ, Lemery-Chalfant K, Howe R (2012). Postpartum depression prevalence and impact on infant health, weight, and sleep in low-income and ethnic minority women and infants. Matern Child Health J 16:887-893.
39. Haga SM, Ulleberg P, Slinning K, Kraft P, Steen TB, Staff A (2012). A longitudinal study of postpartum depressive symptoms: multilevel growth curve analyses of emotion regulation strategies, breastfeeding self-efficacy, and social support. Arch Womens Ment Health 15:175-184.
40. Henning SJ, Romano TJ (1982). Investigation of body temperature as a possible feeding control in the suckling rat. Physiol Behav 28:693-696.
41. Herman JP, Cullinan WE (1997). Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci 20:78-84.
42. Insel TR, Young LJ (2001). The neurobiology of attachment. Nat Rev Neurosci 2:129-136.
43. Johnson NL, Carini L, Schenk ME, Stewart M, Byrnes EM (2011). Adolescent opiate exposure in the female rat induces subtle alterations in maternal care and transgenerational effects on play behavior. Front Psychiatry 2:29.
44. Jolley SN, Betrus P (2007). Comparing postpartum depression and major depressive disorder: issues in assessment. Issues Ment Health Nurs 28:765-780.
45. Kalueff AV, Tuohimaa P (2005). The grooming analysis algorithm discriminates between different levels of anxiety in rats: potential utility for neurobehavioural stress research.J Neurosci Methods 143:169-177.
46. Kosten TA, Nielsen DA (2014). Litter and sex effects on maternal behavior and DNA methylation of the Nr3c1 exon 17 promoter gene in hippocampus and cerebellum. Int J Dev Neurosci 36:5-12.
47. Lau C (1992). Effects of various stressors on milk release in the rat. Physiol Behav 51:1157-1163.
48. Lau C (2001). Effects of stress on lactation. Pediatr Clin North Am 48:221-234.
49. Lau C, Simpson C (2004). Animal models for the study of the effect of prolonged stress on lactation in rats. Physiol Behav 82:193-197.
50. Li J, Hu Z, de Lecea L (2014). The hypocretins/orexins: integrators of multiple physiological functions. Br J Pharmacol 171:332-350.
51. Lupien SJ, McEwen BS, Gunnar MR, Heim C (2009). Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10:434-445.
52. Makino S, Gold PW, Schulkin J (1994). Corticosterone effects on corticotropin-releasing hormone mRNA in the central nucleus of the amygdala and the parvocellular region of the paraventricular nucleus of the hypothalamus. Brain Res 640:105-112.
53. Mattson BJ, Williams S, Rosenblatt JS, Morrell JI (2001). Comparison of two positive reinforcing stimuli: pups and cocaine throughout the postpartum period. Behav Neurosci 115:683-694.
54. Mattson BJ, Williams SE, Rosenblatt JS, Morrell JI (2003). Preferences for cocaine- or pup-associated chambers differentiates otherwise behaviorally identical postpartum maternal rats. Psychopharmacology (Berl) 167:1-8.
55. McGowan PO, Sasaki A, D'Alessio AC, Dymov S, Labonté B, Szyf M, et al. (2009). Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci 12:342-348.
56. Meaney MJ, Viau V, Aitken DH, Bhatnagar S (1989). Glucocorticoid receptors in brain and pituitary of the lactating rat. Physiol Behav 45:209-212.
57. Meltzer-Brody S, Stuebe A, Dole N, Savitz D, Rubinow D, Thorp J (2011). Elevated corticotropin releasing hormone (CRH) during pregnancy and risk of postpartum depression (PPD). J Clin Endocrinol Metab 96:E40-E47.
58. Meyer-Lindenberg A, Domes G, Kirsch P, Heinrichs M (2011). Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine. Nat Rev Neurosci 12:524-538.
59. Mueller BR, Bale TL (2008). Sex-specific programming of offspring emotionality after stress early in pregnancy. J Neurosci 28:9055-9065.
60. Murgatroyd CA, Nephew BC (2013). Effects of early life social stress on maternal behavior and neuroendocrinology. Psychoneuroendocrinology 38:219-228.
61. Nephew BC. Behavioral roles of oxytocin and vasopressin. In: Sumiyoshi T, editor. Neuroendocrinology and behavior.Rijeka, Croatia: InTech; 2012.
62. Nephew BC, Bridges RS (2011). Effects of chronic social stress during lactation on maternal behavior and growth in rats. Stress 14:677-684.
63. Nephew BC, Bridges RS, Lovelock DF, Byrnes EM (2009). Enhanced maternal aggression and associated changes in neuropeptide gene expression in multiparous rats. Behav Neurosci 123:949-957.
64. Nocjar C, Zhang J, Feng P, Panksepp J (2012). The social defeat animal model of depression shows diminished levels of orexin in mesocortical regions of the dopamine system, and of dynorphin and orexin in the hypothalamus. Neuroscience 218:138-153.
65. Nollet M, Leman S (2013). Role of orexin in the pathophysiology of depression: potential for pharmacological intervention. CNS Drugs 27:411-422.
66. O'Hara MW, McCabe JE (2013). Postpartum depression: current status and future directions. Annu Rev Clin Psychol 9:379-407.
67. O'Hara MW, Wisner KL (2014). Perinatal mental illness: definition, description and aetiology. Best Pract Res Clin Obstet Gynaecol 28:3-12.
68. Oberlander TF, Weinberg J, Papsdorf M, Grunau R, Misri S, Devlin AM (2008). Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics 3:97-106.
69. Okabe S, Nagasawa M, Kihara T, Kato M, Harada T, Koshida N, et al. (2013). Pup odor and ultrasonic vocalizations synergistically stimulate maternal attention in mice. Behav Neurosci 127:432-438.
70. Ozsoy S, Esel E, Kula M (2009). Serum oxytocin levels in patients with depression and the effects of gender and antidepressant treatment. Psychiatry Res 169:249-252.
71. Parker KJ, Kenna HA, Zeitzer JM, Keller J, Blasey CM, Amico JA, Schatzberg AF (2010). Preliminary evidence that plasma oxytocin levels are elevated in major depression. Psychiatry Res 178:359-362.
72. Pearson RM, Evans J, Kounali D, Lewis G, Heron J, Ramchandani PG, et al. (2013). Maternal depression during pregnancy and the postnatal period: risks and possible mechanisms for offspring depression at age 18 years. JAMA Psychiatry 70:1312-1319.
73. Perani CV, Slattery DA (2014). Using animal models to study postpartum psychiatric disorders. Br J Pharmacol 16:12640.
74. Reck C, Struben K, Backenstrass M, Stefenelli U, Reinig K, Fuchs T, et al. (2008). Prevalence, onset and comorbidity of postpartum anxiety and depressive disorders. Acta Psychiatr Scand 118:459-468.
75. Sakamoto F, Yamada S, Ueta Y (2004). Centrally administered orexin-A activates corticotropin-releasing factor-containing neurons in the hypothalamic paraventricular nucleus and central amygdaloid nucleus of rats: possible involvement of central orexins on stress-activated central CRF neurons. Regul Pept 118:183-191.
76. Sharp H, Pickles A, Meaney M, Marshall K, Tibu F, Hill J (2012). Frequency of infant stroking reported by mothers moderates the effect of prenatal depression on infant behavioural and physiological outcomes. PLoS One 7:e45446.
77. Shepard JD, Barron KW, Myers DA (2000). Corticosterone delivery to the amygdala increases corticotropin-releasing factor mRNA in the central amygdaloid nucleus and anxiety-like behavior. Brain Res 861:288-295.
78. Skrundz M, Bolten M, Nast I, Hellhammer DH, Meinlschmidt G (2011). Plasma oxytocin concentration during pregnancy is associated with development of postpartum depression. Neuropsychopharmacology 36:1886-1893.
79. Smith JW, Seckl JR, Evans AT, Costall B, Smythe JW (2004). Gestational stress induces post-partum depression-like behaviour and alters maternal care in rats. Psychoneuroendocrinology 29:227-244.
80. Smotherman WP, Bell RW, Starzec J, Elias J, Zachman TA (1974). Maternal responses to infant vocalizations and olfactory cues in rats and mice. Behav Biol 12:55-66.
81. Sohr-Preston SL, Scaramella LV (2006). Implications of timing of maternal depressive symptoms for early cognitive and language development. Clin Child Fam Psychol Rev 9:65-83.
82. Stein A, Lehtonen A, Harvey AG, Nicol-Harper R, Craske M (2009). The influence of postnatal psychiatric disorder on child development. Is maternal preoccupation one of the key underlying processes? Psychopathology 42:11-21.
83. Stuart S, Couser G, Schilder K, O'Hara MW, Gorman L (1998). Postpartum anxiety and depression: onset and comorbidity in a community sample. J Nerv Ment Dis 186:420-424.
84. Stuebe AM, Grewen KM, Pedersen CA, Propper C, Meltzer-Brody S (2011). Failed lactation and perinatal depression: common problems with shared neuroendocrine mechanism. J Womens Health (Larchmt) 21:264-272.
85. Stuebe AM, Horton BJ, Chetwynd E, Watkins S, Grewen K, Meltzer-Brody S (2014). Prevalence and risk factors for early, undesired weaning attributed to lactation dysfunction. J Womens Health (Larchmt) 23:404-412.
86. Sutter-Dallay AL, Giaconne-Marcesche V, Glatigny-Dallay E, Verdoux H (2004). Women with anxiety disorders during pregnancy are at increased risk of intense postnatal depressive symptoms: a prospective survey of the MATQUID cohort. Eur Psychiatry 19:459-463.
87. Swiergiel AH, Takahashi LK, Kalin NH (1993). Attenuation of stress-induced behavior by antagonism of corticotropin-releasing factor receptors in the central amygdala in the rat. Brain Res 623:229-234.
88. Veenema AH, Bredewold R, Neumann ID (2007). Opposite effects of maternal separation on intermale and maternal aggression in C57BL/6 mice: link to hypothalamic vasopressin and oxytocin immunoreactivity. Psychoneuroendocrinology 32:437-450.
89. Villegas L, McKay K, Dennis CL, Ross LE (2011). Postpartum depression among rural women from developed and developing countries: a systematic review. J Rural Health 27:278-288.
90. Watkins S, Meltzer-Brody S, Zolnoun D, Stuebe A (2011). Early breastfeeding experiences and postpartum depression. Obstet Gynecol 118 (2 Pt 1):214-221.
91. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR (2004). Epigenetic programming by maternal behavior. Nat Neurosci 7:847-854.
92. Weaver IC, Champagne FA, Brown SE, Dymov S, Sharma S, Meaney MJ, Szyf M (2005). Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life. J Neurosci 25:11045-11054.
93. Wisner KL, Sit DK, McShea MC, Rizzo DM, Zoretich RA, Hughes CL, et al. (2013). Onset timing, thoughts of self-harm, and diagnoses in postpartum women with screen-positive depression findings. JAMA Psychiatry 70:490-498.
94. Workman JL, Barha CK, Galea LA (2012). Endocrine substrates of cognitive and affective changes during pregnancy and postpartum. Behav Neurosci 126:54-72.
95. Young LJ (1999). Frank A. Beach Award. Oxytocin and vasopressin receptors and species-typical social behaviors. Horm Behav 36:212-221.
96. Zhang TY, Labonté B, Wen XL, Turecki G, Meaney MJ (2013). Epigenetic mechanisms for the early environmental regulation of hippocampal glucocorticoid receptor gene expression in rodents and humans. Neuropsychopharmacology 38:111-123.