Abstract
Early life maltreatment (ELM) has long-lasting effects on social interaction. When interacting with their own child, women with ELM often report difficulties in parenting and show reduced maternal sensitivity. Sensitive maternal behavior requires the recognition of the child’s emotional state depicted in its facial emotions. Based on previous studies, it can be expected that ELM affects the neural processing of facial emotions by altering activation patterns in parts of the brain’s empathy and mentalizing networks. However, so far studies have focused on the processing of standardized, adult facial emotions. Therefore, the current study investigated the impact of ELM on the processing of one’s own child’s facial emotions using functional magnetic resonance imaging. To achieve this, 27 mothers with and 26 mothers without a history of ELM (all without current mental disorders and psychopharmacological treatment) took part in an emotional face recognition paradigm with happy, sad, and neutral faces of their own and an unknown primary school-aged child of the same age and sex. We found elevated activations in regions of the mentalizing (superior temporal sulcus, precuneus) and mirror neuron (inferior parietal lobule) networks as well as in the visual face processing network (cuneus, middle temporal gyrus) in mothers with ELM compared to the non-maltreated mothers in response to happy faces of their own child. This suggests a more effortful processing and cognitive empathic mentalizing of the own child’s facial happiness in mothers with ELM. Future research should address whether this might indicate a compensatory recruitment of mentalizing capacities to maintain maternal sensitivity.
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References
Butchart A, Mikton C (2014) Global status report on violence prevention, 2014
Stoltenborgh M, Bakermans-Kranenburg MJ, Alink LR, IJzendoorn MH (2015) The prevalence of child maltreatment across the globe: review of a series of meta-analyses. Child Abuse Rev 24(1):37–50
Batten SV, Aslan M, Maciejewski PK, Mazure CM (2004) Childhood maltreatment as a risk factor for adult cardiovascular disease and depression. J Clin Psychiatry 65(2):249–254
Widom CS, DuMont K, Czaja SJ (2007) A prospective investigation of major depressive disorder and comorbidity in abused and neglected children grown up. Arch Gen Psychiatry 64(1):49–56. https://doi.org/10.1001/archpsyc.64.1.49
Cougle JR, Timpano KR, Sachs-Ericsson N, Keough ME, Riccardi CJ (2010) Examining the unique relationships between anxiety disorders and childhood physical and sexual abuse in the National Comorbidity Survey-Replication. Psychiatry Res 177(1):150–155
Ibrahim J, Cosgrave N, Woolgar M (2017) Childhood maltreatment and its link to borderline personality disorder features in children: a systematic review approach. Clin Child Psychol Psychiatry 23:57–76 (1359104517712778)
Varese F, Smeets F, Drukker M, Lieverse R, Lataster T, Viechtbauer W, Read J, van Os J, Bentall RP (2012) Childhood adversities increase the risk of psychosis: a meta-analysis of patient-control, prospective- and cross-sectional cohort studies. Schizophr Bull 38:661–671. https://doi.org/10.1093/schbul/sbs050
DiLillo D, Damashek A (2003) Parenting characteristics of women reporting a history of childhood sexual abuse. Child Maltreat 8(4):319–333. https://doi.org/10.1177/1077559503257104
Moehler E, Biringen Z, Poustka L (2007) Emotional availability in a sample of mothers with a history of abuse. Am J Orthopsychiatry 77(4):624–628. https://doi.org/10.1037/0002-9432.77.4.624
Roberts R, O’Connor T, Dunn J, Golding J (2004) The effects of child sexual abuse in later family life; mental health, parenting and adjustment of offspring. Child Abuse Negl 28(5):525–545. https://doi.org/10.1016/j.chiabu.2003.07.006
Bailey HN, DeOliveira CA, Wolfe VV, Evans EM, Hartwick C (2012) The impact of childhood maltreatment history on parenting: a comparison of maltreatment types and assessment methods. Child Abuse Negl 36(3):236–246. https://doi.org/10.1016/j.chiabu.2011.11.005
Fuchs A, Mohler E, Resch F, Kaess M (2015) Impact of a maternal history of childhood abuse on the development of mother–infant interaction during the first year of life. Child Abuse Negl 48:179–189. https://doi.org/10.1016/j.chiabu.2015.05.023
Kluczniok D, Boedeker K, Fuchs A, Hindi Attar C, Fydrich T, Fuehrer D, Dittrich K, Reck C, Winter S, Heinz A, Herpertz SC, Brunner R, Bermpohl F (2016) emotional availability in mother–child interaction: the effects of maternal depression in remission and additional history of childhood abuse. Depress Anxiety 33(7):648–657. https://doi.org/10.1002/da.22462
Mielke EL, Neukel C, Bertsch K, Reck C, Mohler E, Herpertz SC (2016) Maternal sensitivity and the empathic brain: Influences of early life maltreatment. J Psychiatr Res 77:59–66. https://doi.org/10.1016/j.jpsychires.2016.02.013
Leerkes EM, Blankson AN, O’Brien M (2009) Differential effects of maternal sensitivity to infant distress and nondistress on social-emotional functioning. Child Dev 80(3):762–775
Raby KL, Roisman GI, Fraley RC, Simpson JA (2015) The enduring predictive significance of early maternal sensitivity: Social and academic competence through age 32 years. Child Dev 86(3):695–708
Haxby JV, Hoffman EA, Gobbini MI (2000) The distributed human neural system for face perception. Trends Cogn Sci 4(6):223–233
Hein TC, Monk CS (2017) Research Review: neural response to threat in children, adolescents, and adults after child maltreatment—a quantitative meta-analysis. J Child Psychol Psychiatry Allied Discip 58(3):222–230. https://doi.org/10.1111/jcpp.12651
Luo L, Ma X, Zheng X, Zhao W, Xu L, Becker B, Kendrick KM (2015) Neural systems and hormones mediating attraction to infant and child faces. Front Psychol 6:970. https://doi.org/10.3389/fpsyg.2015.00970
Leibenluft E, Gobbini MI, Harrison T, Haxby JV (2004) Mothers’ neural activation in response to pictures of their children and other children. Biol Psychiatry 56(4):225–232. https://doi.org/10.1016/j.biopsych.2004.05.017
Nitschke JB, Nelson EE, Rusch BD, Fox AS, Oakes TR, Davidson RJ (2004) Orbitofrontal cortex tracks positive mood in mothers viewing pictures of their newborn infants. NeuroImage 21(2):583–592. https://doi.org/10.1016/j.neuroimage.2003.10.005
Strathearn L, Li J, Fonagy P, Montague PR (2008) What’s in a smile? Maternal brain responses to infant facial cues. Pediatrics 122(1):40–51. https://doi.org/10.1542/peds.2007-1566
Barrett J, Wonch KE, Gonzalez A, Ali N, Steiner M, Hall GB, Fleming AS (2012) Maternal affect and quality of parenting experiences are related to amygdala response to infant faces. Soc Neurosci 7(3):252–268. https://doi.org/10.1080/17470919.2011.609907
Kluczniok D, Hindi Attar C, Stein J, Poppinga S, Fydrich T, Jaite C, Kappel V, Brunner R, Herpertz SC, Boedeker K, Bermpohl F (2017) Dissociating maternal responses to sad and happy facial expressions of their own child: an fMRI study. PloS One 12(8):e0182476. https://doi.org/10.1371/journal.pone.0182476
Neukel C, Bertsch K, Fuchs Ph DA, Zietlow AL, Reck C, Moehler E, Brunner R, Bermpohl F, Herpertz SC (2018) The maternal brain in women with a history of early-life maltreatment: an imagination-based fMRI study of conflictual versus pleasant interactions with children. J Psychiatry Neurosci 43(4):170026. https://doi.org/10.1503/jpn.170026
Bifulco A, Brown GW, Harris TO (1994) Childhood experience of care and abuse (CECA): a retrospective interview measure. J Child Psychol Psychiatry 35(8):1419–1435
Thabrew H, de Sylva S, Romans S (2012) Evaluating childhood adversity. In: Fava GA, Sonino N, Wise TN (eds) The psychosomatic assessment, vol 32. Karger Publishers, Basel, pp 35–57
Sheehan DV, Lecrubier Y, Sheehan KH, Amorim P, Janavs J, Weiller E, Hergueta T, Baker R, Dunbar GC (1998) 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 59(Suppl 20):22–33 (quiz 34–57)
Loranger AW, Sartorius N, Andreoli A, Berger P, Buchheim P, Channabasavanna S, Coid B, Dahl A, Diekstra RF, Ferguson B (1994) The international personality disorder examination: the World Health Organization/Alcohol, Drug Abuse, and Mental Health Administration international pilot study of personality disorders. Arch Gen Psychiatry 51(3):215–224
Hamilton M (1960) A rating scale for depression. J Neurol Neurosurg Psychiatry 23(1):56
Eklund A, Nichols TE, Knutsson H (2016) Cluster failure: why fMRI inferences for spatial extent have inflated false-positive rates. Proc Natl Acad Sci 28:201602413
Volman I, von Borries AKL, Bulten BH, Verkes RJ, Toni I, Roelofs K (2016) Testosterone modulates altered prefrontal control of emotional actions in psychopathic offenders. ENeuro 3(1):ENEURO0107 (0107-0115.2016)
Bertsch K, Roelofs K, Roch PJ, Ma B, Hensel S, Herpertz SC, Volman I (2018) Neural correlates of emotional action control in anger-prone women with borderline personality disorder. J Psychiatry Neurosci 43(3):161–170
Frith CD, Frith U (2006) The neural basis of mentalizing. Neuron 50(4):531–534. https://doi.org/10.1016/j.neuron.2006.05.001
Kanske P, Bockler A, Trautwein FM, Singer T (2015) Dissecting the social brain: Introducing the EmpaToM to reveal distinct neural networks and brain-behavior relations for empathy and Theory of Mind. NeuroImage 122:6–19. https://doi.org/10.1016/j.neuroimage.2015.07.082
Schurz M, Radua J, Aichhorn M, Richlan F, Perner J (2014) Fractionating theory of mind: a meta-analysis of functional brain imaging studies. Neurosci Biobehav Rev 42:9–34. https://doi.org/10.1016/j.neubiorev.2014.01.009
Cattaneo L, Rizzolatti G (2009) The mirror neuron system. Arch Neurol 66(5):557–560. https://doi.org/10.1001/archneurol.2009.41
Molenberghs P, Cunnington R, Mattingley JB (2012) Brain regions with mirror properties: a meta-analysis of 125 human fMRI studies. Neurosci Biobehav Rev 36(1):341–349. https://doi.org/10.1016/j.neubiorev.2011.07.004
Schulte-Rüther M, Markowitsch HJ, Fink GR, Piefke M (2007) Mirror neuron and theory of mind mechanisms involved in face-to-face interactions: a functional magnetic resonance imaging approach to empathy. J Cognit Neurosci 19(8):1354–1372
Morgan JK, Guo C, Moses-Kolko EL, Phillips ML, Stepp SD, Hipwell AE (2017) Postpartum depressive symptoms moderate the link between mothers’ neural response to positive faces in reward and social regions and observed caregiving. Soc Cognit Affect Neurosci 12(10):1605–1613. https://doi.org/10.1093/scan/nsx087
Parlar M, Frewen P, Nazarov A, Oremus C, MacQueen G, Lanius R, McKinnon MC (2014) Alterations in empathic responding among women with posttraumatic stress disorder associated with childhood trauma. Brain Behav 4(3):381–389. https://doi.org/10.1002/brb3.215
Aminoff EM, Kveraga K, Bar M (2013) The role of the parahippocampal cortex in cognition. Trends Cognit Sci 17(8):379–390
Kim P, Leckman JF, Mayes LC, Feldman R, Wang X, Swain JE (2010) The plasticity of human maternal brain: longitudinal changes in brain anatomy during the early postpartum period. Behav Neurosci 124(5):695–700. https://doi.org/10.1037/a0020884
Laurent HK, Ablow JC (2013) A face a mother could love: depression-related maternal neural responses to infant emotion faces. Soc Neurosci 8(3):228–239. https://doi.org/10.1080/17470919.2012.762039
Schechter DS, Moser DA, Wang Z, Marsh R, Hao X, Duan Y, Yu S, Gunter B, Murphy D, McCaw J, Kangarlu A, Willheim E, Myers MM, Hofer MA, Peterson BS (2012) An fMRI study of the brain responses of traumatized mothers to viewing their toddlers during separation and play. Soc Cognit Affect Neurosci 7(8):969–979. https://doi.org/10.1093/scan/nsr069
Acknowledgements
We thank J. Rausch and E. Mielke for their help with data collection, and I. Rek and K. Hillmann for participant recruitment and organization. The study was supported by a grant from the German Federal Ministry of Education and Research to SC.H. (BMBF; 01KR1207A; coordinator: R.B.) The German Federal Ministry of Education and Research had no influence on study design or manuscript.
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Neukel, C., Herpertz, S.C., Hinid-Attar, C. et al. Neural processing of the own child’s facial emotions in mothers with a history of early life maltreatment. Eur Arch Psychiatry Clin Neurosci 269, 171–181 (2019). https://doi.org/10.1007/s00406-018-0929-8
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DOI: https://doi.org/10.1007/s00406-018-0929-8