Maternal sensitivity predicts anterior hippocampal functional networks in early childhood
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Maternal care influences child hippocampal development. The hippocampus is functionally organized along an anterior–posterior axis. Little is known with regards to the extent maternal care shapes offspring anterior and posterior hippocampal (aHPC, pHPC) functional networks. This study examined maternal behavior, especially maternal sensitivity, at 6 months postpartum in relation to aHPC and pHPC functional networks of children at age 4 and 6 years. Maternal sensitivity was assessed at 6 months via the “Maternal Behavior Q Sort (MBQS) mini for video”. Subsequently, 61 and 76 children underwent resting-state functional magnetic resonance imaging (rs-fMRI), respectively, at 4 and 6 years of age. We found that maternal sensitivity assessed at 6 months postpartum was associated with the right aHPC functional networks in children at both 4 and 6 years of age. At age 4 years, maternal sensitivity was associated positively with the right aHPC’s functional connectivity with the sensorimotor network and negatively with the aHPC’s functional connectivity with the top–down cognitive control network. At 6 years of age, maternal sensitivity was linked positively with the right aHPC’s functional connectivity with the visual-processing network. Our findings suggested that maternal sensitivity in infancy has a long-term impact on the anterior hippocampal functional network in preschool children, implicating a potential role of maternal care in shaping child brain development in early life.
KeywordsResting-state fMRI Maternal sensitivity Anterior hippocampus Posterior hippocampus Functional networks
This research is supported by the Singapore National Research Foundation under its Translational and Clinical Research (TCR) Flagship Programme and administered by the Singapore Ministry of Health’s National Medical Research Council (NMRC), Singapore- NMRC/TCR/004-NUS/2008; NMRC/TCR/012-NUHS/2014. Additional funding is provided by the Singapore Institute for Clinical Sciences, Agency for Science Technology and Research (A*STAR), Singapore Ministry of Education (Academic research fund tier 1; NUHSRO/2017/052/T1-SRP-Partnership/01), and NUS Institute of Data Science, Singapore.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.
Informed consent was obtained from all individual participants included in the study.
- Ainsworth MD, Blehar MC, Waters E, Wall S (1978) Patterns of attachment: assessed in the strange situation and at home. Erlbaum, HillsdaleGoogle Scholar
- Bagot RC, Zhang T-Y, Wen X, Nguyen TTT, Nguyen H-B, Diorio J, Wong TP, Meaney MJ (2012) Variations in postnatal maternal care and the epigenetic regulation of metabotropic glutamate receptor 1 expression and hippocampal function in the rat. Proc Natl Acad Sci USA 109(Supplement 2):17200–17207PubMedGoogle Scholar
- Bernier A, Dégeilh F, Leblanc É, Daneault V, Bailey HN, Beauchamp MH (2019) Mother–infant interaction and child brain morphology: a multidimensional approach to maternal sensitivity. Infancy 24(2):120–138Google Scholar
- Champagne DL, Bagot RC, van Hasselt F, Ramakers G, Meaney MJ, De Kloet ER, Joëls M, Krugers H (2008) Maternal care and hippocampal plasticity: evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress. J Neurosci 28(23):6037–6045PubMedPubMedCentralGoogle Scholar
- Gabard-Durnam LJ, Flannery J, Goff B, Gee DG, Humphreys KL, Telzer E, Hare T, Tottenham N (2014) The development of human amygdala functional connectivity at rest from 4 to 23 years: a cross-sectional study. Neuroimage 95:193–207. https://doi.org/10.1016/j.neuroimage.2014.03.038 PubMedPubMedCentralGoogle Scholar
- Gee DG, Gabard-Durnam LJ, Flannery J, Goff B, Humphreys KL, Telzer EH, Hare TA, Bookheimer SY, Tottenham N (2013) Early developmental emergence of human amygdala-prefrontal connectivity after maternal deprivation. Proc Natl Acad Sci USA 110(39):15638–15643. https://doi.org/10.1073/pnas.1307893110 PubMedGoogle Scholar
- Herman JP, Ostrander MM, Mueller NK, Figueiredo H (2005) Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Progr Neuro-Psychopharmacol Biol Psychiatry 29(8):1201–1213Google Scholar
- Maheu FS, Dozier M, Guyer AE, Mandell D, Peloso E, Poeth K, Jenness J, Lau JY, Ackerman JP, Pine DS (2010) A preliminary study of medial temporal lobe function in youths with a history of caregiver deprivation and emotional neglect. Cogn Affect Behav Neurosci 10(1):34–49PubMedPubMedCentralGoogle Scholar
- Migo E, Mitterschiffthaler M, O’Daly O, Dawson G, Dourish C, Craig K, Simmons A, Wilcock G, McCulloch E, Jackson S (2015) Alterations in working memory networks in amnestic mild cognitive impairment. Aging Neuropsychol Cogn 22(1):106–127Google Scholar
- Mori S, Oishi K, Jiang H, Jiang L, Li X, Akhter K, Hua K, Faria AV, Mahmood A, Woods R, Toga AW, Pike GB, Neto PR, Evans A, Zhang J, Huang H, Miller MI, van Zijl P, Mazziotta J (2008) Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. Neuroimage 40(2):570–582. https://doi.org/10.1016/j.neuroimage.2007.12.035 PubMedPubMedCentralGoogle Scholar
- Paavola L, Kemppinen K, Kumpulainen K, Moilanen I, Ebeling H (2006) Maternal sensitivity, infant co-operation and early linguistic development: Some predictive relations. Eur J Dev Psychol 3(1):13–30Google Scholar
- Palmer FB, Graff JC, Jones TL, Murphy LE, Keisling BL, Whitaker TM, Wang L, Tylavsky FA (2018) Socio-demographic, maternal, and child indicators of socioemotional problems in 2-year-old children: a cohort study. Medicine (Baltimore) 97(28):e11468. https://doi.org/10.1097/md.0000000000011468 Google Scholar
- Power JD, Mitra A, Laumann TO, Snyder AZ, Schlaggar BL, Petersen SE (2014) Methods to detect, characterize, and remove motion artifact in resting state fMRI. NeuroImage 84:320–341Google Scholar
- Rifkin-Graboi A, Meaney MJ, Chen H, Bai J, Hameed WBR, Tint MT, Broekman BF, Chong Y-S, Gluckman PD, Fortier MV (2015b) Antenatal maternal anxiety predicts variations in neural structures implicated in anxiety disorders in newborns. J Am Acad Child Adolesc Psychiatry 54(4):313–321PubMedGoogle Scholar
- Satpute AB, Mumford JA, Naliboff BD, Poldrack RA (2012) Human anterior and posterior hippocampus respond distinctly to state and trait anxiety. Emotion 12(1):58–68Google Scholar
- Soe NN, Wen DJ, Poh JS, Li Y, Broekman BF, Chen H, Chong YS, Kwek K, Saw SM, Gluckman PD, Meaney MJ, Rifkin-Graboi A, Qiu A (2016) Pre- and Post-Natal Maternal Depressive Symptoms in Relation with Infant Frontal Function, Connectivity, and Behaviors. PLoS One 11(4):e0152991. https://doi.org/10.1371/journal.pone.0152991 PubMedPubMedCentralGoogle Scholar
- Tarabulsy GM, Provost MA, Bordeleau S, Trudel-Fitzgerald C, Moran G, Pederson DR, Trabelsi M, Lemelin JP, Pierce T (2009) Validation of a short version of the maternal behavior Q-set applied to a brief video record of mother-infant interaction. Infant Behav Dev 32(1):132–136. https://doi.org/10.1016/j.infbeh.2008.09.006 PubMedGoogle Scholar
- Treyvaud K, Doyle LW, Lee KJ, Ure A, Inder TE, Hunt RW, Anderson PJ (2016) Parenting behavior at 2 years predicts school-age performance at 7 years in very preterm children. J Child Psychol Psyc 57(7):814–821Google Scholar
- van der Werff SJ, Pannekoek JN, Veer IM, van Tol M-J, Aleman A, Veltman DJ, Zitman FG, Rombouts SA, Elzinga BM, van der Wee NJ (2013) Resilience to childhood maltreatment is associated with increased resting-state functional connectivity of the salience network with the lingual gyrus. Child Abuse Neglect 37(11):1021–1029PubMedGoogle Scholar
- Veer IM, Beckmann C, Van Tol M-J, Ferrarini L, Milles J, Veltman D, Aleman A, Van Buchem MA, Van Der Wee NJ, Rombouts SA (2010) Whole brain resting-state analysis reveals decreased functional connectivity in major depression. Front Syst Neurosci 4:1–10Google Scholar
- Wen DJ, Poh JS, Ni SN, Chong YS, Chen H, Kwek K, Shek LP, Gluckman PD, Fortier MV, Meaney MJ, Qiu A (2017a) Influences of prenatal and postnatal maternal depression on amygdala volume and microstructure in young children. Transl Psychiatry 7(4):e1103. https://doi.org/10.1038/tp.2017.74 PubMedPubMedCentralGoogle Scholar
- Wen DJ, Soe NN, Sim LW, Sanmugam S, Kwek K, Chong YS, Gluckman PD, Meaney MJ, Rifkin-Graboi A, Qiu A (2017b) Infant frontal EEG asymmetry in relation with postnatal maternal depression and parenting behavior. Transl Psychiatry 7(3):e1057. https://doi.org/10.1038/tp.2017.28 PubMedPubMedCentralGoogle Scholar
- Zhang Y, Zhang J, Hsu J, Oishi K, Faria AV, Albert M, Miller MI, Mori S (2014) Evaluation of group-specific, whole-brain atlas generation using Volume-based Template Estimation (VTE): application to normal and Alzheimer’s populations. Neuroimage 84:406–419. https://doi.org/10.1016/j.neuroimage.2013.09.011 PubMedGoogle Scholar