Emotion reactivity is increased 4-6 weeks postpartum in healthy women: A longitudinal fMRI study

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Gingnell, Malin ^a   Bannbers, Elin ^a   Moes, Harmen ^a   Engman, Jonas ^a   Sylvén, Sara ^a   Skalkidou, Alkistis ^a   Kask, Kristiina ^a   Wikström, Johan ^a   Sundström Poromaa, Inger ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; PROGESTERONE;

ADAPTATION; ADULT; ANXIETY DISORDER; ARTICLE; CESAREAN SECTION; CLINICAL ARTICLE; CONTROLLED STUDY; DEPRESSION; DISEASE ASSOCIATION; EDINBURGH POSTNATAL DEPRESSION SCALE; ELECTROENCEPHALOGRAM; EMOTIONALITY; ESTRADIOL BLOOD LEVEL; FEMALE; FOLLICULAR PHASE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HORMONE DETERMINATION; HUMAN; INFERIOR FRONTAL GYRUS; INSULA; LONGITUDINAL STUDY; LUTEAL PHASE; MIDDLE FRONTAL GYRUS; MONTGOMERY ASBERG DEPRESSION RATING SCALE; PROGESTERONE BLOOD LEVEL; PUERPERIUM; SELF CONCEPT; STATE TRAIT ANXIETY INVENTORY; TASK PERFORMANCE; VAGINAL DELIVERY; ANXIETY; BRAIN CORTEX; BRAIN MAPPING; DEPRESSION, POSTPARTUM; MATERNAL WELFARE; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PROCEDURES; PSYCHOLOGY; YOUNG ADULT;

ADULT; ANXIETY; BRAIN MAPPING; CEREBRAL CORTEX; DEPRESSION, POSTPARTUM; FEMALE; HUMANS; LONGITUDINAL STUDIES; MAGNETIC RESONANCE IMAGING; MATERNAL HEALTH; POSTPARTUM PERIOD; YOUNG ADULT;

EID: 84936797748     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0128964     Document Type: Article

References (64)

1. Grattan D. A mother's brain knows. J Neuroendocrinol. 2011; 23: 1188-1189. doi: 10.1111/j.1365-2826.2011.02175.x PMID: 22004569
2. Meinlschmidt G, Martin C, Neumann ID, Heinrich M. Maternal cortisol in late pregnancy and hypothalamic-pituitary-adrenal reactivity to psychosocial stress postpartum in women. Stress. 2010; 13: 163-171. doi: 10.3109/10253890903128632 PMID: 20214437
3. Bailara KM, Henry C, Lestage J, Launay JM, Parrot F, Swendsen J, et al. Decreased brain tryptophan availability as a partial determinant of post-partum blues. Psychoneuroendocrinology. 2006; 31: 407-413. PMID: 16303256
4. Doornbos B, Fekkes D, Tanke MA, de Jonge P, Korf J. Sequential serotonin and noradrenalin associated processes involved in postpartum blues. Prog Neuropsychopharmacol Biol Psychiatry. 2008; 32: 1320-1325. doi: 10.1016/j.pnpbp.2008.04.010 PMID: 18502014
5. Sacher J, Wilson AA, Houle S, Rusjan P, Hassan S, Bloomfield PM, et al. Elevated brain monoamine oxidase A binding in the early postpartum period. Arch Gen Psychiatry. 2010; 67: 468-474. doi: 10.1001/archgenpsychiatry.2010.32 PMID: 20439828
6. Epperson CN, Gueorguieva R, Czarkowski KA, Stiklus S, Sellers E, et al. Preliminary evidence of reduced occipital GABA concentrations in puerperal women: a 1H-MRS study. Psychopharmacology (Berl). 2006; 186: 425-433. PMID: 16724188
7. Kendall-Tackett K. A new paradigm for depression in new mothers: the central role of inflammation and how breastfeeding and anti-inflammatory treatments protect maternal mental health. Int Breastfeed J. 2007; 2: 6. PMID: 17397549
8. Hellgren C, Bannbers E, Akerud H, Risbrough V, Poromaa IS. Decreased startle modulation during anticipation in the postpartum period in comparison to late pregnancy. Arch Womens Ment Health. 2012; 15: 87-94. doi: 10.1007/s00737-012-0261-7 PMID: 22315106
9. O'Hara MW, McCabe JE. Postpartum depression: current status and future directions. Annu Rev Clin Psychol. 2013; 9: 379-407. doi: 10.1146/annurev-clinpsy-050212-185612 PMID: 23394227
10. Bloch M., Schmidt PJ,Danaceau M, Murphy J, Nieman L, Rubinow D. Effects of gonadal steroids in women with a history of postpartum depression. Am J Psychiatry. 2000; 157: 924-930. PMID: 10831472
11. Bartels A, Zeki S. The neural correlates of maternal and romantic love. Neuroimage. 2004; 21: 1155-66. PMID: 15006682
12. Leckman JF, Feldman R, Swain JE, Eicher V, Thompson N, Mayes LC. Primary Parental Preoccupation: Circuits, Genes, and the Crucial Role of the Environment. Journal of Neural Transmission 2004; 111: 753-771. PMID: 15205997
13. Kim P., Mayes LC, Feldman R, Leckman JF, Swain JE. Early Postpartum Parental Preoccupation and Positive Parenting Thoughts: Relationship with Parent-Infant Interaction. Journal of Infant Mental Health 2013; 34: 104-116.
14. Swain JE, Kim P, Spicer J, Ho SS, Dayton CJ, Elmadih A, et al. Approaching the Biology of Human Parental Attachment: Brain Imaging, Oxytocin and Coordinated Assessments of Mothers and Fathers. Brain Research. 2014; 1580: 78-101. doi: 10.1016/j.brainres.2014.03.007 PMID: 24637261
15. Moses-Kolko EL, Wisner KL, Price JC, Berga SL, Drevets WC, Hanusa BH, et al. Serotonin 1A receptor reductions in postpartum depression: a positron emission tomography study. Fertil Steril. 2008; 89: 685-692. PMID: 17543959
16. Moses-Kolko EL, Perlman SB, Wisner KL, James J, Saul AT, Philips ML. 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. doi: 10.1176/appi.ajp.2010.09081235 PMID: 20843875
17. Moses-Kolko EL, Fraser D, Wisner KL, James JA, Saul AT, Fiez JA, et al. Rapid habituation of ventral striatal response to reward receipt in postpartum depression. Biol Psychiatry. 2011; 70: 395-399. doi: 10.1016/j.biopsych.2011.02.021 PMID: 21507385
18. Silverman ME, Loudon H, Liu X, Mauro C, Leiter G, Goldstein MA. The neural processing of negative emotion postpartum: a preliminary study of amygdala function in postpartum depression. Arch Womens Ment Health. 2011; 14: 355-359. doi: 10.1007/s00737-011-0226-2 PMID: 21713456
19. Seifritz E, Esposito F, Neuhoff JG, Lüthi A, Mustovic H, Dammann G, et al. Differential sex-independent amygdala response to infant crying and laughing in parents versus nonparents. Biological Psychiatry. 2003; 54: 1367-1375. PMID: 14675800
20. Leibenluft E, Gobbini MI, Harrison T, Haxby JV. Mothers' neural activation in response to pictures of their children and other children. Biol Psychiatry. 2004; 56: 225-232. PMID: 15312809
21. Noriuchi M, Kikuchi YSenoo A. The functional neuroanatomy of maternal love: mother's response to infant's attachment behaviors. Biol Psychiatry. 2008; 63: 415-423. PMID: 17686467
22. Swain JE, Tasgin E, Mayes LC, Feldman R, constable RT, Leckman JF. Maternal brain response to own baby-cry is affected by cesarean section delivery. J Child Psychol Psychiatry. 2008: 49: 1042-1052. doi: 10.1111/j.1469-7610.2008.01963.x PMID: 18771508
23. Lenzi D, Trentini C, Pantano P, Macaluso E, Iacoboni M, Lenzi GL, et al. Neural basis of maternal communication and emotional expression processing during infant preverbal stage. Cereb Cortex. 2009; 19: 1124-1133. doi: 10.1093/cercor/bhn153 PMID: 18787229
24. Kim P, Feldman R, Leckman JF, Mayes LC, Swain JE. Breastfeeding, Brain Activation to Own Infant Cry, and Maternal Sensitivity. Journal of Child Psychology and Psychiatry 2011; 52: 907-915. doi: 10.1111/j.1469-7610.2011.02406.x PMID: 21501165
25. Kim P, Leckman JF, Mayes LC, Feldman R, Wang X, Swain JE. The plasticity of human maternal brain: longitudinal changes in brain anatomy during the early postpartum period. Behav Neurosci. 2010; 124: 695-700. doi: 10.1037/a0020884 PMID: 20939669
26. Kim P, Rigo P, Mayes LC, Feldman R, Leckman JF, Swain JE. Neural plasticity in fathers of human infants. Social Neuroscience 2014; 9: 522-535. doi: 10.1080/17470919.2014.933713 PMID: 24958358
27. Bannbers E, Gingnell M, Engman J, Morell A, Sylvén S, Skalkidou A, et al. Prefrontal activity during response inhibition decreases over time in the postpartum period. Behav Brain Res. 2013; 241: 132-138. doi: 10.1016/j.bbr.2012.12.003 PMID: 23238040
28. Rupp HA, James TW, Ketterson ED, Sengelaub DR, Ditzen B, Heiman JR. Amygdala response to negative images in postpartum vs nulliparous women and intranasal oxytocin. Soc Cogn Affect Neurosci. 2014; 9: 48-54. doi: 10.1093/scan/nss100 PMID: 22956670
29. Shin LM, Liberzon I. The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology. 2010; 35: 169-191. doi: 10.1038/npp.2009.83 PMID: 19625997
30. Davidsson R, Putnam K, Larson C. Dysfunction in the neural circuitry of emotion regulation - a possible prelude to violence. Science. 2000; 258: 591-594.
31. Bush G, Luu P, Posner MI. Cognitive and emotional influences in anterior cingulate cortex. Trends in Cognition & Science. 2000; 4: 215-222.
32. Fusar-Poli P, Placentino A, Carletti F, Landi P, Allen P, Surguladze S, et al. Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. Journal of Psychiatry & Neuroscience. 2009; 34: 418-443. doi: 10.3233/JAD-131544 PMID: 25914902
33. Pessoa L, Adolphs R. Emotion processing and the amygdala: from a 'low road' to 'many roads' of evaluating biological significance. Nat Rev Neuroscience. 2010; 11: 773-783.
34. Hariri AR, Mattay VS, Tessitore A, Kolachana B, Fera F, Goldman D, et al. Serotonin transporter genetic variation and the response of the human amygdala. Science. 2002; 297: 400-403. PMID: 12130784
35. Gingnell M, Morell A, Bannbers E, Wikström J, Sundström Poromaa I. Menstrual cycle effects on amygdala reactivity to emotional stimulation in premenstrual dysphoric disorder. Horm Behav. 2012; 62: 400-406. doi: 10.1016/j.yhbeh.2012.07.005 PMID: 22814368
36. van Wingen GA, van Broekhoven F, Verkes RJ, Petersson KM, Backstrom T, Buitelaar TK, et al. Progesterone selectively increases amygdala reactivity in women. Molecular Psychiatry. 2008; 13: 325-333. PMID: 17579609
37. Gingnell M, Engman J, Frick A, Moby L, Wikström J, Fredrikson M, et al. Oral contraceptive use changes brain activity and mood in women with previous negative affect on the pill-A double-blinded, placebo-controlled randomized trial of a levonorgestrel-containing combined oral contraceptive. Psychoneuroendocrinology. 2013; 38: 1133-1144. doi: 10.1016/j.psyneuen.2012.11.006 PMID: 23219471
38. Andreano JM, Cahill L. Menstrual cycle modulation of medial temporal activity evoked by negative emotion. Neuroimage. 2010; 53: 1286-1293. doi: 10.1016/j.neuroimage.2010.07.011 PMID: 20637290
39. Bayer J, Schultz H, Gamer M, Sommer T. Menstrual-cycle dependent fluctuations in ovarian hormones affect emotional memory. Neurobiol Learn Mem. 2014; 110: 55-63. doi: 10.1016/j.nlm.2014.01.017 PMID: 24492058
40. Protopopescu X, Pan H, Altemus M, Tuescher O, Polanecsky M, McEwen B, et al. Orbitofrontal cortex activity related to emotional processing changes across the menstrual cycle. Proc Natl Acad Sci U S A. 2005; 102:16060-16065. PMID: 16247013
41. Love T, Smith YR, Persad CC, Tkaczyk A, Zubieta JK. Short-term hormone treatment modulates emotion response circuitry in postmenopausal women. Fertil Steril. 2010; 93: 1929-1937. doi: 10.1016/j.fertnstert.2008.12.056 PMID: 19243753
42. Shafir T, Love T, Berent-Spillson A, Persad CC, Wang H, Reame NK, et al. Postmenopausal hormone use impact on emotion processing circuitry. Behav Brain Res. 2012; 226: 147-153. doi: 10.1016/j.bbr.2011.09.012 PMID: 21930160
43. Dreher JC, Schmidt PJ, Kohn P, Furman D, Rubinow D, Berman KF. Menstrual cycle phase modulates reward-related neural function in women. Proceedings of the National Academy of Sciences U S A. 2007; 104: 2465-2470. PMID: 17267613
44. van Wingen GA, Ossewaarde L, Backstrom T, Hermans EJ, Fernandez G. Gonadal hormone regulation of the emotion circuitry in humans. Neuroscience. 2011; 191: 38-45. doi: 10.1016/j.neuroscience.2011.04.042 PMID: 21540080
45. Sheehan DV, Lecrubier Y, Sheehan KH, Amorim P, Janavs J, Weiller E, et al. The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry. 1998; 59 Suppl 20:22-33;quiz 34-57. PMID: 9881538
46. Sundström Poromaa I, Gingnell M. Menstrual cycle influence on cognitive function and emotion processing-from a reproductive perspective.Front Neurosci. 2014; 8: 380. doi: 10.3389/fnins.2014.00380 PMID: 25505380
47. Montgomery S, Åsberg M. A new depression scale designed to be sensitive to change. Br J Psychiatry. 1979; 134: 382-389. PMID: 444788
48. Spielberger CD, Gorusch RL, Lushene R. Manual for the State-Trait Anxiety (STAI Form Y), Consulting Psychologist Press, Palo Alto, CA, 1983. PMID: 12922120
49. Cox JL, Holden JM, Sagovsky R. Detection of postnatal depression: Development of the 10-item Edinburgh Postnatal Depression Scale. British Journal of Psychiatry. 1987; 150: 782-786. PMID: 3651732
50. Lancaster J, Summerlin J, Rainey L, Freitas C, Fox P. The Talairach Daemon, A Database Server for Talairach Atlas Labels. Neuroimage 1997; 5(4, Part 2 of 4 Parts): S633 Academic Press.
51. Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage. 2003; 19: 1233-1239. PMID: 12880848
52. Mitterschiffthaler MT, Kumari V, Malhi GS, Brown RG, Giampietro VP, Brammer MJ, et al. Neural response to pleasant stimuli in anhedonia: an fMRI study. Neuroreport. 2003; 14: 177-182. PMID: 12598724
53. Simmons A, Strigo I, Matthews SC, Paulus MP, Stein MB. Anticipation of aversive visual stimuli is associated with increased insula activation in anxiety-prone subjects. Biol Psychiatry. 2006; 60: 402-409. PMID: 16919527
54. Stein MB, Simmons AN, Feinstein JS, Paulus MP. Increased amygdala and insula activation during emotion processing in anxiety-prone subjects. Am J Psychiatry. 2007; 164: 318-327. PMID: 17267796
55. Strigo IA, Simmons AN, Matthews SC, Craig AD, Paulus MP. Association of major depressive disorder with altered functional brain response during anticipation and processing of heat pain. Arch Gen Psychiatry. 2008; 65: 1275-1284. doi: 10.1001/archpsyc.65.11.1275 PMID: 18981339
56. Silverman ME, Loudon H, Safier M, Protopopescu X, Leiter G, Liu X, et al. Neural dysfunction in postpartum depression: an fMRI pilot study. CNS Spectr. 2007; 12: 853-862. PMID: 17984858
57. Reck C, Stehle E, Reinig K, Mundt C. Maternity blues as a predictor of DSM-IV depression and anxiety disorders in the first three months postpartum. J Affect Disord. 2009; 113: 77-87. doi: 10.1016/j.jad.2008.05.003 PMID: 18573539
58. Newman LK, Harris MAllen J. Neurobiological basis of parenting disturbance. Aust N Z J Psychiatry. 2011; 45: 109-122. doi: 10.3109/00048674.2010.527821 PMID: 20977304
59. Altemus M, Deuster PA, Galliven E, Carter CS, Gold PW. Suppression of hypothalmic-pituitary-adrenal axis responses to stress in lactating women. J Clin Endocrinol Metab. 1995; 80: 2954-2959. PMID: 7559880
60. Smith R, Owens PC, Brinsmead MW, Singh B, Hall C. The nonsuppressibility of plasma cortisol persists after pregnancy. Horm Metab Res. 1997; 19: 41-42.
61. Maes M, Claes M, Schotte C, Delbeke L, Jacquemyn Y, Verkerk R, et al. Disturbances in dexamethasone suppression test and lower availability of L-tryptophan and tyrosine in early puerperium and in women under contraceptive therapy. J Psychosom Res. 1992; 36: 191-197. PMID: 1560430
62. Nissen E, Lilja G, Widstrom AM, Ulvnas-Moberg K. Elevation of oxytocin levels early post partum in women. Acta Obstet Gynecol Scand. 1995; 74: 530-533. PMID: 7618451
63. Dawood MY, Khan-Dawood FS, Wahi RS, Fuchs F. Oxytocin release and plasma anterior pituitary and gonadal hormones in women during lactation. J Clin Endocrinol Metab. 1981; 52: 678-683. PMID: 6782115
64. Altemus M, Fong J, Yang R, Damast S, Luine V, Ferguson D. Changes in cerebrospinal fluid neurochemistry during pregnancy. Biol Psychiatry. 2004; 56: 386-392. PMID: 15364035