Prenatal maternal depression alters amygdala functional connectivity in 6-month-old infants

Translational Psychiatry

Volumn 5, Issue 2, 2015, Pages

  Qiu, A ^a,b   Anh, T T ^a   Li, Y ^a   Chen, H ^c   Rifkin Graboi, A ^b   Broekman, B F P ^b,d   Kwek, K ^c   Saw, S M ^a   Chong, Y S ^d   Gluckman, P D ^b   Fortier, M V ^c   Meaney, M J ^b,e,f  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b AGENCY FOR SCIENCE   (Singapore)

^c KK WOMEN'S AND CHILDREN'S HOSPITAL   (Singapore)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^e DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

^f MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMYGDALA FUNCTIONAL CONNECTIVITY; AMYGDALOID NUCLEUS; ANTERIOR CINGULATE; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CLINICAL ARTICLE; CLINICAL ASSESSMENT; DISEASE ASSOCIATION; EDINBURGH POSTNATAL DEPRESSION SCALE; EMOTIONALITY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GESTATIONAL AGE; HUMAN; INFANT; INSULA; LABOR INDUCTION; MAJOR DEPRESSION; MALE; MEMORY; MOOD DISORDER; NERVE CELL NETWORK; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; ORBITAL CORTEX; PATTERN RECOGNITION; POSTNATAL DEVELOPMENT; PRENATAL CARE; PRENATAL DEVELOPMENT; PRENATAL DIAGNOSIS; PRENATAL DISORDER; PRENATAL MATERNAL DEPRESSION; PROGENY; PSYCHOLOGICAL WELL BEING; PUERPERAL DEPRESSION; SENSORY CORTEX; SYMPTOMATOLOGY; TEMPORAL CORTEX; VENTROMEDIAL PREFRONTAL CORTEX; ADULT; AMYGDALA; BRAIN CORTEX; CINGULATE GYRUS; DEPRESSION; FRONTAL LOBE; FUNCTIONAL NEUROIMAGING; NERVE TRACT; ORGAN SIZE; PATHOLOGY; PATHOPHYSIOLOGY; PREFRONTAL CORTEX; PREGNANCY; PREGNANCY COMPLICATION; PRENATAL EXPOSURE; STATISTICAL MODEL; TEMPORAL LOBE;

ADULT; AMYGDALA; CEREBRAL CORTEX; DEPRESSION; FEMALE; FRONTAL LOBE; FUNCTIONAL NEUROIMAGING; GYRUS CINGULI; HUMANS; INFANT; LINEAR MODELS; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; ORGAN SIZE; PREFRONTAL CORTEX; PREGNANCY; PREGNANCY COMPLICATIONS; PRENATAL EXPOSURE DELAYED EFFECTS; TEMPORAL LOBE;

EID: 84927711187     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2015.3     Document Type: Article

References (68)

1. Pearson RM, Evans J, Kounali D, Lewis G, Heron J, Ramchandani PG et al. Maternal depression during pregnancy and the postnatal period: risks and possible mechanisms for offspring depression at age 18 years. JAMA Psychiatry 2013; 70: 1312-1319.
2. Pawlby S, Hay DF, Sharp D, Waters CS, O'Keane V. Antenatal depression predicts depression in adolescent offspring: prospective longitudinal communitybased study. J Affect Disord 2009; 113: 236-243.
3. Mian AI. Depression in pregnancy and the postpartum period: balancing adverse effects of untreated illness with treatment risks. J Psychiatr Pract 2005; 11: 389-396.
4. Sohr-Preston SL, Scaramella LV. Implications of timing of maternal depressive symptoms for early cognitive and language development. Clin Child Family Psychol Rev 2006; 9: 65-83.
5. Lundy B, Field T, Pickens J. Newborns of mothers with depressive symptoms are less expressive. Infant Behav Dev 1996; 19: 419-424.
6. Davis EP, Glynn LM, Schetter CD, Hobel C, Chicz-Demet A, Sandman CA. Prenatal exposure to maternal depression and cortisol influences infant temperament. J Am Acad Child Adolesc Psychiatry 2007; 46: 737-746.
7. Buss C, Davis EP, Shahbaba B, Pruessner JC, Head K, Sandman CA. Maternal cortisol over the course of pregnancy and subsequent child amygdala and hippocampus volumes and affective problems. Proc Natl Acad Sci USA 2012; 109: E1312-E1319.
8. Lupien SJ, Parent S, Evans AC, Tremblay RE, Zelazo PD, Corbo V et al. Larger amygdala but no change in hippocampal volume in 10-year-old children exposed to maternal depressive symptomatology since birth. Proc Natl Acad Sci USA 2011; 108: 14324-14329.
9. Malykhin NV, Carter R, Hegadoren KM, Seres P, Coupland NJ. Fronto-limbic volumetric changes in major depressive disorder. J Affect Disord 2012; 136: 1104-1113.
10. Holmes AJ, Lee PH, Hollinshead MO, Bakst L, Roffman JL, Smoller JW et al. Individual differences in amygdala-medial prefrontal anatomy link negative affect, impaired social functioning, and polygenic depression risk. J Neurosci 2012; 32: 18087-18100.
11. van Eijndhoven P, van Wingen G, van Oijen K, Rijpkema M, Goraj B, Jan Verkes R et al. Amygdala volume marks the acute state in the early course of depression. Biol Psychiatry 2009; 65: 812-818.
12. Fleming AS, Flett GL, Ruble DN, Shaul DL. Postpartum adjustment in 1st-time mothers-relations between mood, maternal attitudes, and mother infant interactions. Dev Psychol 1988; 24: 71-81.
13. Rifkin-Graboi A, Bai J, Chen H, Hameed WB, Sim LW, Tint MT et al. Prenatal maternal depression associates with microstructure of right amygdala in neonates at birth. Biol Psychiatry 2013; 74: 837-844.
14. Price JL, Drevets WC. Neurocircuitry of mood disorders. Neuropsychopharmacology 2009; 35: 192-216.
15. Hamilton JP, Gotlib IH. Neural substrates of increased memory sensitivity for negative stimuli in major depression. Biol Psychiatry 2008; 63: 1155-1162.
16. Pruessner JC, Dedovic K, Khalili-Mahani N, Engert V, Pruessner M, Buss C et al. Deactivation of the limbic system during acute psychosocial stress: evidence from positron emission tomography and functional magnetic resonance imaging studies. Biol Psychiatry 2008; 63: 234-240.
17. Abercrombie HC, Schaefer SM, Larson CL, Oakes TR, Lindgren KA, Holden JE et al. Metabolic rate in the right amygdala predicts negative affect in depressed patients. Neuroreport 1998; 9: 3301-3307.
18. Perez-Edgar K, Roberson-Nay R, Hardin MG, Poeth K, Guyer AE, Nelson EE et al. Attention alters neural responses to evocative faces in behaviorally inhibited adolescents. Neuroimage 2007; 35: 1538-1546.
19. Gaffrey MS, Barch DM, Singer J, Shenoy R, Luby JL. Disrupted amygdala reactivity in depressed 4-to 6-year-old children. J Am Acad Child Adolesc Psychiatry 2013; 52: 737-746.
20. Caspi A, Moffitt TE, Newman DL, Silva PA. Behavioral observations at age 3 years predict adult psychiatric disorders. Longitudinal evidence from a birth cohort. Arch Gen Psychiatry 1996; 53: 1033-1039.
21. Cote SM, Boivin M, Liu X, Nagin DS, Zoccolillo M, Tremblay RE. Depression and anxiety symptoms: onset, developmental course and risk factors during early childhood. J Child Psychol Psychiatry 2009; 50: 1201-1208.
22. van Marle HJ, Hermans EJ, Qin S, Fernandez G. From specificity to sensitivity: how acute stress affects amygdala processing of biologically salient stimuli. Biol Psychiatry 2009; 66: 649-655.
23. Connolly CG, Wu J, Ho TC, Hoeft F, Wolkowitz O, Eisendrath S et al. Resting-state functional connectivity of subgenual anterior cingulate cortex in depressed adolescents. Biol Psychiatry 2013; 74: 898-907.
24. Kong L, Chen K, Tang Y, Wu F, Driesen N, Womer F et al. Functional connectivity between the amygdala and prefrontal cortex in medication-naive individuals with major depressive disorder. J Psychiatr Neurosci 2013; 38: 417.
25. Ramasubbu R, Konduru N, Cortese F, Bray S, Gaxiola-Valdez I, Goodyear B. Reduced intrinsic connectivity of amygdala in adults with major depressive disorder. Front Psychiatry 2014; 5: 17.
26. Fransson P, Skiöld B, Horsch S, Nordell A, Blennow M, Lagercrantz H et al. Restingstate networks in the infant brain. Proc Natl Acad Sci USA 2007; 104: 15531-15536.
27. Eberhard-Gran M, Eskild A, Tambs K, Opjordsmoen S, Samuelsen SO. Review of validation studies of the Edinburgh Postnatal Depression Scale. Acta Psychiatr Scand 2001; 104: 243-249.
28. Bergink V, Kooistra L, Lambregtse-van den Berg MP, Wijnen H, Bunevicius R, van Baar A et al. Validation of the Edinburgh Depression Scale during pregnancy. J Psychosom Res 2011; 70: 385-389.
29. Murray D, Cox JL. Screening for depression during pregnancy with the Edinburgh Depression Scale (EPDS). J Reprod Infant Psychol 1990; 8: 99-107.
30. Smith SM. Fast robust automated brain extraction. Hum Brain Mapp 2002; 17: 143-155.
31. Griffiths P Morris J Larroche J-C. Atlas of Fetal and Postnatal Brain MR. Elsevier Health Sciences, USA, 2009.
32. Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 2012; 59: 2142-2154.
33. Miller MI, Qiu A. The emerging discipline of computational functional anatomy. Neuroimage 2009; 45: 16-39.
34. Amaral DG, Price JL. Amygdalo-cortical projections in the monkey (Macaca fascicularis). J Comp Neurol 1984; 230: 465-496.
35. Qin S, Young CB, Duan X, Chen T, Supekar K, Menon V. Amygdala subregional structure and intrinsic functional connectivity predicts individual differences in anxiety during early childhood. Biol Psychiatry 2013; 75: 892-900.
36. Roy AK, Shehzad Z, Margulies DS, Kelly A, Uddin LQ, Gotimer K et al. Functional connectivity of the human amygdala using resting state fMRI. Neuroimage 2009; 45: 614-626.
37. Stein JL, Wiedholz LM, Bassett DS, Weinberger DR, Zink CF, Mattay VS et al. A validated network of effective amygdala connectivity. Neuroimage 2007; 36: 736-745.
38. Hariri AR, Mattay VS, Tessitore A, Fera F, Weinberger DR. Neocortical modulation of the amygdala response to fearful stimuli. Biol Psychiatry 2003; 53: 494-501.
39. Ochsner KN, Ray RD, Cooper JC, Robertson ER, Chopra S, Gabrieli JD et al. For better or for worse: neural systems supporting the cognitive down-and up-regulation of negative emotion. Neuroimage 2004; 23: 483-499.
40. Critchley HD, Mathias CJ, Dolan RJ. Neural activity in the human brain relating to uncertainty and arousal during anticipation. Neuron 2001; 29: 537-545.
41. Zald DH, Pardo JV. Emotion, olfaction, and the human amygdala: amygdala activation during aversive olfactory stimulation. Proc Natl Acad Sci USA 1997; 94: 4119-4124.
42. Dubois S, Rossion B, Schiltz C, Bodart JM, Michel C, Bruyer R et al. Effect of familiarity on the processing of human faces. Neuroimage 1999; 9: 278-289.
43. Phillips ML, Young AW, Scott SK, Calder AJ, Andrew C, Giampietro V et al. Neural responses to facial and vocal expressions of fear and disgust. Proc Biol Sci 1998; 265: 1809-1817.
44. Dolcos F, LaBar KS, Cabeza R. Interaction between the amygdala and the medial temporal lobe memory system predicts better memory for emotional events. Neuron 2004; 42: 855-863.
45. Fairhall SL, Ishai A. Effective connectivity within the distributed cortical network for face perception. Cerebr Cortex 2007; 17: 2400-2406.
46. Cauda F, D'Agata F, Sacco K, Duca S, Geminiani G, Vercelli A. Functional connectivity of the insula in the resting brain. Neuroimage 2011; 55: 8-23.
47. Anand A, Li Y, Wang Y, Lowe MJ, Dzemidzic M. Resting state corticolimbic connectivity abnormalities in unmedicated bipolar disorder and unipolar depression. Psychiatry Res 2009; 171: 189-198.
48. Alexopoulos GS, Hoptman MJ, Yuen G, Kanellopoulos D, Seirup JK, Lim KO et al. Functional connectivity in apathy of late-life depression: a preliminary study. J Affect Disord 2013; 149: 398-405.
49. Surguladze S, Brammer MJ, Keedwell P, Giampietro V, Young AW, Travis MJ et al. A differential pattern of neural response toward sad versus happy facial expressions in major depressive disorder. Biol Psychiatry 2005; 57: 201-209.
50. Chan SW, Norbury R, Goodwin GM, Harmer CJ. Risk for depression and neural responses to fearful facial expressions of emotion. Br J Psychiatry 2009; 194: 139-145.
51. Tahmasian M, Knight DC, Manoliu A, Schwerthoffer D, Scherr M, Meng C et al. Aberrant intrinsic connectivity of hippocampus and amygdala overlap in the fronto-insular and dorsomedial-prefrontal cortex in major depressive disorder. Front Hum Neurosci 2013; 7: 639.
52. Zeng LL, Shen H, Liu L, Wang L, Li B, Fang P et al. Identifying major depression using whole-brain functional connectivity: a multivariate pattern analysis. Brain 2012; 135(Pt 5): 1498-1507.
53. Burghy CA, Stodola DE, Ruttle PL, Molloy EK, Armstrong JM, Oler JA et al. Developmental pathways to amygdala-prefrontal function and internalizing symptoms in adolescence. Nat Neurosci 2012; 15: 1736-1741.
54. Perlman G, Simmons AN, Wu J, Hahn KS, Tapert SF, Max JE et al. Amygdala response and functional connectivity during emotion regulation: a study of 14 depressed adolescents. J Affect Disord 2012; 139: 75-84.
55. Erk S, Mikschl A, Stier S, Ciaramidaro A, Gapp V, Weber B et al. Acute and sustained effects of cognitive emotion regulation in major depression. J Neurosci 2010; 30: 15726-15734.
56. Drevets WC, Price JL, Furey ML. Brain structural and functional abnormalities in mood disorders: implications for neurocircuitry models of depression. Brain Struct Funct 2008; 213: 93-118.
57. Gilmore JH, Lin W, Prastawa MW, Looney CB, Vetsa YSK, Knickmeyer RC et al. Regional gray matter growth, sexual dimorphism, and cerebral asymmetry in the neonatal brain. J Neurosci 2007; 27: 1255-1260.
58. Salm AK, Pavelko M, Krouse EM, Webster W, Kraszpulski M, Birkle DL. Lateral amygdaloid nucleus expansion in adult rats is associated with exposure to prenatal stress. Brain Res Dev Brain Res 2004; 148: 159-167.
59. Murmu MS, Salomon S, Biala Y, Weinstock M, Braun K, Bock J. Changes of spine density and dendritic complexity in the prefrontal cortex in offspring of mothers exposed to stress during pregnancy. Eur J Neurosci 2006; 24: 1477-1487.
60. Wyrwoll CS, Holmes MC. Prenatal excess glucocorticoid exposure and adult affective disorders: a role for serotonergic and catecholamine pathways. Neuroendocrinology 2011; 95: 47-55.
61. Byravan S, Campagnoni AT. Serum factors and hydrocortisone influence the synthesis of myelin basic proteins in mouse brain primary cultures. Int J Dev Neurosci 1994; 12: 343-351.
62. Herman JP, Ostrander MM, Mueller NK, Figueiredo H. Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Prog Neuropsychopharmacol Biol Psychiatry 2005; 29: 1201-1213.
63. Field T, Diego M, Hernandez-Reif M. Prenatal depression effects and interventions: a review. Infant Behav Dev 2010; 33: 409-418.
64. Huizink AC, de Medina PGR, Mulder EJH, Visser GHA, Buitelaar JK. Psychological measures of prenatal stress as predictors of infant temperament. J Am Acad Child Adolesc Psychiatry 2002; 41: 1078-1085.
65. Seckl JR, Holmes MC. Mechanisms of disease: glucocorticoids, their placental metabolism and fetal 'programming' of adult pathophysiology. Nat Clin Pract Endocrinol Metab 2007; 3: 479-488.
66. Diorio J, Meaney MJ. Maternal programming of defensive responses through sustained effects on gene expression. J Psychiatry Neurosci 2007; 32: 275-284.
67. Wichers M, Geschwind N, Jacobs N, Kenis G, Peeters F, Derom C et al. Transition from stress sensitivity to a depressive state: longitudinal twin study. Br J Psychiatry 2009; 195: 498-503.
68. Widom CS, DuMont K, Czaja SJ. A prospective investigation of major depressive disorder and comorbidity in abused and neglected children grown up. Arch Gen Psychiatry 2007; 64: 49-56.