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Insensitive parenting may accelerate the development of the amygdala–medial prefrontal cortex circuit

Published online by Cambridge University Press:  12 April 2017

Sandra Thijssen
Leiden University Erasmus University Medical Center, Rotterdam
Ryan L. Muetzel
Erasmus University Medical Center, Rotterdam Erasmus University Medical Center Sophia Children's Hospital, Rotterdam
Marian J. Bakermans-Kranenburg
Leiden University
Vincent W. V. Jaddoe
Erasmus University Medical Center, Rotterdam
Henning Tiemeier
Erasmus University Medical Center, Rotterdam Erasmus University Medical Center Sophia Children's Hospital, Rotterdam
Frank C. Verhulst
Erasmus University Medical Center, Rotterdam Erasmus University Medical Center Sophia Children's Hospital, Rotterdam
Tonya White
Erasmus University Medical Center, Rotterdam Erasmus University Medical Center Sophia Children's Hospital, Rotterdam
Marinus H. Van Ijzendoorn
Leiden University Erasmus University, Rotterdam
E-mail address:


This study examined whether the association between age and amygdala–medial prefrontal cortex (mPFC) connectivity in typically developing 6- to 10-year-old children is correlated with parental care. Resting-state functional magnetic resonance imaging scans were acquired from 124 children of the Generation R Study who at 4 years old had been observed interacting with their parents to assess maternal and paternal sensitivity. Amygdala functional connectivity was assessed using a general linear model with the amygdalae time series as explanatory variables. Higher level analyses assessing Sensitivity × Age as well as exploratory Sensitivity × Age × Gender interaction effects were performed restricted to voxels in the mPFC. We found significant Sensitivity × Age interaction effects on amygdala–mPFC connectivity. Age was related to stronger amygdala–mPFC connectivity in children with a lower combined parental sensitivity score (b = 0.11, p = .004, b = 0.06, p = .06, right and left amygdala, respectively), but not in children with a higher parental sensitivity score, (b = –0.07, p = .12, b = –0.06, p = .12, right and left amygdala, respectively). A similar effect was found for maternal sensitivity, with stronger amygdala–mPFC connectivity in children with less sensitive mothers. Exploratory (parental, maternal, paternal) Sensitivity × Age × Gender interaction analyses suggested that this effect was especially pronounced in girls. Amygdala-mPFC resting-state functional connectivity has been shown to increase from age 10.5 years onward, implying that the positive association between age and amygdala–mPFC connectivity in 6- to 10-year-old children of less sensitive parents represents accelerated development of the amygdala–mPFC circuit.

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The Generation R Study is conducted by the Erasmus Medical Center in close collaboration with the Erasmus University Rotterdam, School of Law and Faculty of Social Sciences; the Municipal Health Service Rotterdam area, Rotterdam; the Rotterdam Homecare Foundation, Rotterdam; and the Stichting Trombosedienst & Artsenlaboratorium Rijnmond (STAR), Rotterdam. The first phase of the Generation R Study is made possible by financial support from Erasmus Medical Centre, Rotterdam; Erasmus University, Rotterdam; the Netherlands Organization for Health Research and Development (ZonMw); the Netherlands Organisation for Scientific Research; the Ministry of Health, Welfare and Sport; and the Ministry of Youth and Families. In addition, this study is financially supported through ZonMw TOP project number 91211021 (to T.W.). Henning Tiemer, Marian J. Bakermans-Kranenburg, and Marinus H. van IJzendoorn were supported by research awards from the Netherlands Organization for Scientific Research (H.T., VIDI grant; M.H.v.I., SPINOZA prize; M.J.B.K., VICI grant), and by the Gravitation program of the Dutch Ministry of Education, Culture, and Science and the Netherlands Organization for Scientific Research (Grant 024.001.003). Bakermans-Kranenburg was also supported by the European Research Council (ERC AdG).


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Insensitive parenting may accelerate the development of the amygdala–medial prefrontal cortex circuit
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