The effects of gestational stress and Selective Serotonin reuptake inhibitor antidepressant treatment on structural plasticity in the postpartum brain - A translational model for postpartum depression

Hormones and Behavior

Volumn 77, Issue , 2016, Pages 124-131

  Haim, Achikam ^a   Albin Brooks, Christopher ^b   Sherer, Morgan ^b   Mills, Emily ^b   Leuner, Benedetta ^a,b  

^a THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Amygdala; Dendritic spines; Maternal; Mood; Nucleus accumbens; Prefrontal cortex

Indexed keywords

ANTIDEPRESSANT AGENT; CITALOPRAM; SEROTONIN UPTAKE INHIBITOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BASOLATERAL AMYGDALA; CELL DENSITY; CONTROLLED STUDY; DENDRITIC SPINE; DRUG EFFICACY; FEMALE; FORCED SWIM TEST; MALE; MATERNAL STRESS; MEDIAL PREFRONTAL CORTEX; NERVE CELL PLASTICITY; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PUERPERAL DEPRESSION; RAT; ANIMAL; BRAIN; DISEASE MODEL; DRUG EFFECTS; MENTAL STRESS; PATHOPHYSIOLOGY; PHYSIOLOGY; PUERPERIUM;

ANIMALS; ANTIDEPRESSIVE AGENTS; BRAIN; CITALOPRAM; DEPRESSION, POSTPARTUM; DISEASE MODELS, ANIMAL; FEMALE; NEURONAL PLASTICITY; POSTPARTUM PERIOD; RATS; SEROTONIN UPTAKE INHIBITORS; STRESS, PSYCHOLOGICAL;

EID: 84956580208     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2015.05.005     Document Type: Article

References (74)

1. Baker S., Chebli M., Rees S., LeMarec N., Godbout R., Bielajew C. Effects of gestational stress: 1. Evaluation of maternal and juvenile offspring behavior. Brain Res. 2008, 12:98-110.
2. Belzung C., Turiault M., Griebel G. Optogenetics to study the circuits of fear-and depression-like behaviors: a critical analysis. Pharmacol. Biochem. Behav. 2014, 122:144-157.
3. Berle J.O., Spigset O. Antidepressant use during breastfeeding. Curr. Womens Health Rev. 2011, 7:28-34.
4. Bessa J.M., Ferreira D., Melo I., Marques F., Cerqueira J.J., Palha J.A., Almeida O.F., Sousa N. The mood-improving actions of antidepressants do not depend on neurogenesis but are associated with neuronal remodeling. Mol. Psychiatry 2009, 14:764-773.
5. Bessa J.M., Morais M., Marques F., Pinto L., Palha J.A., Almeida O.F., Sousa N. Stress-induced anhedonia is associated with hypertrophy of medium spiny neurons of the nucleus accumbens. Transl. Psychiatry 2013, 3:e266.
6. Boyarskikh U.A., Bondar N.P., Filipenko M.L., Kudryavtseva N.N. Dowregulation of serotonergic gene expression in the raphe nuclei of the midbrain under chronic social defeat stress in male mice. Mol. Neurobiol. 2013, 48:13-21.
7. Bratt A.M., Kelley S.P., Knowles J.P., Barrett J., Davis K., Davis M., Mittleman G. Long term modulation of the HPA axis by the hippocampus. Behavioral, biochemical and immunological endpoints in rats exposed to chronic mild stress. Psychoneuroendocrinology 2001, 26:141-145.
8. Brawarsky P., Stotland N.E., Jackson R.A., Fuentes-Afflick E., Escobar G.J., Rubashkin N., Haas J.S. Pre-pregnancy and pregnancy-related factors and the risk of excessive or inadequate gestational weight gain. Int. J. Gynaecol. Obstet. 2005, 91:125-131.
9. Brummelte S., Galea L.A.M. Depression during pregnancy and postpartum: contribution of stress and ovarian hormones. Prog. Neuropsychopharmacol. Biol. Psychiatry 2010, 34:766-776.
10. Celada P., Puig M.V., Artigas F. Serotonin modulation of cortical neurons and networks. Front. Integr. Neurosci. 2013, 7:25.
11. Chen Y.C., Tan Q.R., Dang W., Wang H.N., Zhang R.B., Li Z.Y., Lin H., Liu R. The effects of Citalopram on chronic stress-induced depressive-like behavior in rats through GSK3β/β-catenin activation in the medial prefrontal cortex. Brain Res. Bull. 2012, 88:338-344.
12. Christoffel D.J., Golden S.A., Dumitriu D., Robinson A.J., Janssen W.G., Ahn H.F., Krishnan V., Reyes C.M., Han M.H., Ables J.L., Eisch A.J., Dietz D.M., Ferguson D., Neve R.L., Greengard P., Kim Y., Morrison J.H., Russo S.J. IkB kinase regulates social defeat-induced synaptic and behavioral plasticity. J. Neurosci. 2011, 31:314-321.
13. Davey H.L., Tough S.C., Adair C.E., Benzies K.M. Risk factors for sub-clinical and major postpartum depression among a community cohort of Canadian women. Matern. Child Health J. 2011, 15:866-875.
14. Emiliano A.B.F., Cruz T., Pannoni V., Fudge J.L. The interface of oxytocin-labeled cells and serotonin transporter containing fibers in the primate hypothalamus: a substrate for SSRIs therapeutic effects?. Neuropsychopharmacology 2007, 32:977-988.
15. Garrett J.E., Wellman C.L. Chronic stress effects on dendritic morphology in medial prefrontal cortex: sex differences and estrogen dependence. Neuroscience 2009, 162:195-207.
16. Glynn L.M., Davis E., Sandman C.A. New insights into the role of perinatal HPA-axis dysregulation in postpartum depression. Neuropeptides 2013, 47:363-370.
17. Grace S.L., Evindar A., Steward D.E. The effect of postpartum depression on child cognitive development and behavior: a review and critical analysis of the literature. Arch. Womens Ment. Health 2003, 6:263-274.
18. Gress-Smith J.L., Luecken L.J., Lemery-Chalfant K., Howe R. Postpartum depression prevalence and impact on infant health, weight, and sleep in low-income and ethnic minority women and infants. Matern. Child Health J. 2012, 16:887-893.
19. Grissom N., Bhatnagar S. Habituation to stress: get used to it. Neurobiol. Learn. Mem. 2009, 92:215-224.
20. Haim A., Sherer M.S., Leuner B. Gestational stress induces persistent depressive-like behavior and structural modifications within the postpartum nucleus accumbens. Eur. J. Neurosci. 2014, 40:3766-3773.
21. Hillerer K.M., Reber S.O., Neumann I.D., Slattery D.A. Exposure to chronic pregnancy stress reverses peripartum-associated adaptations: implications for postpartum anxiety and mood disorders. Endocrinology 2011, 152:3930-3940.
22. Holsen L.M., Lancaster K., Klibanski K., Whitfield-Gabrieli S., Cherkerzian S., Buka S., Goldstein J.M. HPA-axis hormone modulation of stress response circuitry activity in women with remitted major depression. Neuroscience 2013, 250:733-742.
23. Isgor C., Kabbaj M., Akil H., Watson S.J. Delayed effects of chronic variable stress during peripubertal-juvenile period on hippocampal morphology and on cognitive and stress axis functions in rats. Hippocampus 2004, 14:636-648.
24. Kalivas P.W., Duffy P. Selective activation of dopamine transmission in the shell of the nucleus accumbens by stress. Brain Res. 1995, 675:325-328.
25. Lancaster C.A., Gold K.J., Flynn H.A., Yoo H., Marcus S.M., Davis M.M. Risk factors for depressive symptoms during pregnancy: a systematic review. Am. J. Obstet. Gynecol. 2010, 202:5-14.
26. Laurent H.K., Ablow J.C. A cry in the dark: depressed mothers show reduced neural activation to their own infant's cry. Soc. Cogn. Affect. Neurosci. 2012, 7:125-134.
27. Letourneau N.L., Dennis C.L., Benzies K., Duffett-Leger L., Stewart M., Tryphonopoulous P.D., Este D., Watson W. Postpartum depression is a family affair: addressing the impact on mothers, fathers, and children. Issues Ment. Health Nurs. 2012, 3:445-457.
28. Leuner B., Fredericks P.J., Nealer C., Albin-Brooks C. Chronic gestational stress leads to depressive-like behavior and compromises medial prefrontal cortex structure and function during the postpartum period. PLoS One 2014, 9:e89912.
29. Licznerski P., Duman R.S. Remodeling of axo-spinous synapses in the pathophysiology and treatment of depression. Neuroscience 2013, 251:33-50.
30. Logsdon M.C., Wisner K., Sit D., Luther J.F., Wisniewski S.R. Depression treatment and maternal functioning. Depress. Anxiety 2011, 28:1020-1026.
31. Malenka R.C., Nestler E.J., Hyman S.E. Molecular Neuropharmacology: A Foundation for Clinical Neuroscience 2009, McGraw-Hill Medical, NY.
32. McEwen A.M., Burgess D.T., Hanstcok C.C., Seres P., Khalili P., Newman S.C., Baker G.B., Mitchell N.D., Khudabux-Der J., Allen P.S., LeMelledo J.M. Increased glutamate levels in the medial prefrontal cortex in patients with postpartum depression. Neuropsychopharmacology 2012, 37:2428-2435.
33. Misri S., Abizadeh J., Albert G., Carter D., Ryan D. Restoration of functionality in postpartum depressed mothers: an open label study with escitalopram. J. Clin. Psychopharmacol. 2012, 32:729-732.
34. Mitra R., Jadhav S., McEwen B.S., Vyas S., Chattarji A. Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala. Proc. Natl. Acad. Sci. U. S. A. 2005, 26:9371-9376.
35. Mizoguchi K., Shoji H., Ikeda R., Tanaka Y., Tabira T. Persistent depressive state after chronic stress in rats is accompanied by HPA axis dysregulation and reduced prefrontal dopaminergic neurotransmission. Pharmacol. Biochem. Behav. 2008, 91:170-175.
36. Morales-Medina J.C., Sanchez F., Flores G., Dumont Y., Quirion R. Morphological reorganization after repeated corticosterone administration in the hippocampus, nucleus accumbens and amygdala in the rat. J. Chem. Neuroanat. 2009, 38:266-272.
37. Moses-Kolko E.L., Perlman S.B., Wisner K.L., James J., Saul A.T., Phillips M.L. Abnormally reduced dorsomedial prefrontal cortical activity and effective connectivity with amygdala in response to negative emotional faces in postpartum depression. Am. J. Psychiatry 2010, 167:1373-1380.
38. Moses-Kolko E.L., Fraser D., Wisner K.L., James J.A., Saul A.T., Fiez J.A., Phillips M.L. Rapid habituation of ventral striatal response to reward receipt in postpartum depression. Biol. Psychiatry 2011, 70:395-399.
39. Nemeroff C.B., Owens M.J. Pharmacologic differences among the SSRIs: focus on monoamine transporters and the HPA axis. CNS Spectr. 2004, 9:23-31.
40. Numan M., Insel T. The Neurobiology of Parental Behavior 2003, Springer, New York.
41. O'Hara M.W., Wisner K.L. Perinatal mental illness: definition, description and aetiology. Best Pract. Res. Clin. Obstet. Gynaecol. 2014, 28:3-12.
42. O'Mahony S.M., Myint A.M., van den Hove D., Desbonnet L., Steinbusch H., Leonard B.E. Gestational stress leads to depressive-like behavioural and immunological changes in the rat. Neuroimmunomodulation 2006, 13:82-88.
43. O'Hara M.W. Postpartum depression: what we know. J. Clin. Psychol. 2009, 65:1258-1269.
44. Padival M.A., Blume S.R., Rosenkranz J.A. Repeated restraint stress exerts different impact on structure of neurons in the lateral and basal nuclei of the amygdala. Neuroscience 2013, 246:230-242.
45. Pariante C.M., Lightman S.L. The HPA axis in major depression: classical theories and new developments. Trends Neurosci. 2008, 31:464-468.
46. Pawluski J.L., Charlier T.D., Fillet M., Houbart V., Crispin H.T., Steinbusch H.W., van den Hove D.L. Chronic fluoxetine treatment and maternal adversity differentially alter neurobehavioral outcomes in the rat dam. Behav. Brain Res. 2012, 228:159-168.
47. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 1998, Academic Press, San Diego.
48. Picone T.A., Allen J.H., Schramm M.M., Olsen P.N. Pregnancy outcome in North American women. I. Effects of diet, cigarette smoking, and psychological stress on maternal weight gain. Am. J. Clin. Nutr. 1982, 36:1214-1224.
49. Pillai A.G., Anilkumar S., Chattarji S. The same antidepressant elicits contrasting patterns of synaptic changes in the amygdala vs hippocampus. Neuropsychopharmacology 2012, 37:2702-2711.
50. Price J.L., Drevets W.C. Neural circuits underlying the pathophysiology of mood disorders. Trends Cogn. Sci. 2012, 16:61-71.
51. Rampono J., Hackett L.P., Kristensen J.H., Kohan R., Page-Sharp M., Ilett K.F. Transfer of escitalopram and its metabolite demethylescitalopram into breastmilk. Br. J. Clin. Pharmacol. 2006, 62:316-322.
52. Rodrigues S.M., LeDoux J.E., Sapolsky R.M. The influence of stress hormones on fear circuitry. Ann. Rev. Neurosci. 2009, 32:289-313.
53. Rosenblatt J.S. Hormonal and nonhormonal regulation of maternal behavior: a theoretical survey. Reprod. Nutr. Dev. 1980, 20:791-800.
54. Rosenblatt J.S. The physiological and evolutionary background of maternal responsiveness. New Dir. Child Dev. 1989, 43:15-30.
55. Rosenblatt J.S., Mayer A.D., Giordano A.L. Hormonal basis during pregnancy for the onset of maternal behavior in the rat. Psychoneuroendocrinology 1988, 13:29-46.
56. Russo S.J., Nestler E.J. The brain reward circuitry in mood disorders. Nat. Rev. Neurosci. 2013, 14:609-625.
57. Sacher J., Rekkas P.V., Wilson A.A., Houle S., Romano L., Hamidi J., Rusjan P., Stewart D.E., Meyer J.H. Relationship of monoamine oxidase-A distribution volume to postpartum depression and postpartum crying. Neuropsychopharmacology 2015, 40:429-435.
58. Selvaraj S., Mouchlianitis E., Faulkner P., Turkheimer F., Cowen P.J., Roiser J.P., Howes O. Presynaptic serotonergic regulation of emotional processing: a mutlimodal brain imaging study. Biol. Psychiatry 2014, (in press). 10.1016/j.biopsych.2014.04.011.
59. Shansky R.M., Morrison J.H. Stress-induced dendritic remodeling in the medial prefrontal cortex: effects of circuit, hormones and rest. Brain Res. 2009, 1293:108-113.
60. Silverman M.E., Loudon H., Liu X., Mauro C., Leiter G., Goldstein M.A. The neural processing of negative emotion postpartum: a preliminary study of amygdala function in postpartum depression. Arch. Womens Ment. Health 2011, 14:355-359.
61. Smith J.W., Seckl J.R., Evans A.T., Costall B., Smythe J.W. Gestational stress induces post-partum depression-like behavior and alters maternal care in rats. Psychoneuroendocrinology 2004, 29:227-244.
62. Stevenson C.W., Gratton A. Basolateral amygdala modulation of the nucleus accumbens dopamine response to stress: role of the medial prefrontal cortex. Eur. J. Neurosci. 2003, 17:1287-1295.
63. Sun Z.Y., Schacher S. Binding of serotonin to receptors at multiple sites is required for structural plasticity accompanying long-term facilitation of Aplysia sensorimotor synapses. J. Neurosci. 1998, 18:3991-4000.
64. Swaab D.F., Bao A.M., Lucassen P.J. The stress system in the human brain in depression and neurodegeneration. Ageing Res. Rev. 2005, 4:141-194.
65. Van Bockstaele E.J., Pickel V.M. Ultrastructure of serotonin-immunoreactive terminals in the core and shell of the rat nucleus accumbens: cellular substrates for interactions with catecholamine afferents. J. Comp. Neurol. 1993, 334:603-617.
66. Varghese F.P., Brown E.S. The hypothalamic-pituitary-adrenal axis in major depressive disorder: a brief primer for primary care physicians. Prim. Care Companion J. Clin. Psychiatry 2001, 3:151-155.
67. Verbeek T., Bockting C.L., van Pampus M.G., Ormel J., Meijer J.L., Hartman C.A., Burger H. Postpartum depression predicts offspring mental health problems in adolescence independently of parental lifetime psychopathology. J. Affect. Disord. 2012, 136:948-954.
68. Vetencourt J.F.M., Tiraboschi E., Spolidoro M., Castren E., Maffei L. Serotonin triggers a transient epigenetic mechanism that reinstates adult visual cortex plasticity in rats. Eur. J. Neurosci. 2011, 33:49-57.
69. Vialou V., Bagot R.C., Cahill M.E., Ferguson D., Robinson A.J., Dietz D.M., Fallon B., Mazei-Robinson M., Ku S.M., Harrigan E., Winstanley C.A., Joshi T., Feng J., Berton O., Nestler E.J. Prefrontal cortical circuit for depression and anxiety related behaviors mediated by cholecystokinin: role of deltaFosB. J. Neurosci. 2014, 34:3878-3887.
70. Vyas A., Pillai A.G., Chattarji S. Recovery after chronic stress fails to reverse amygdaloid neuronal hypertrophy and enhanced anxiety-like behavior. Neuroscience 2004, 128:667-673.
71. Wang Y.C., Ho U.C., Ko M.C., Liao C.C., Lee L.J. Differential neuronal changes in medial prefrontal cortex, basolateral amygdala and nucleus accumbens after postweaning social isolation. Brain Struct. Funct. 2012, 217:337-351.
72. Zahm D.S. Functional-anatomical implications of the nucleus accumbens core and shell subterritories. Ann. N. Y. Acad. Sci. 1999, 29:113-128.
73. Zelkowitz P., Gold I., Feeley N., Hayton B., Carter C.S., Tulandi T., Abenhaim H.A., Levin P. Psychosocial stress moderates the relationships between oxytocin, perinatal depression, and maternal behavior. Horm. Behav. 2014, 66:351-360.
74. Zhang J., Fan Y., Li Y., Zhu H., Wang L., Zhu M.Y. Chronic social defeat up-regulates expression of the serotonin transporter in rat dorsal raphe nucleus and projection regions in a glucocorticoid-dependent manner. J. Neurochem. 2012, 123:1054-1068.