Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-23T09:06:29.205Z Has data issue: false hasContentIssue false

Caregiving adversity during infancy and preschool cognitive function: adaptations to context?

Published online by Cambridge University Press:  13 January 2021

Anne Rifkin-Graboi*
Affiliation:
Centre for Research in Child Development, National Institute of Education, 1 Nanyang Walk, SingaporeS637616, Singapore
Shaun Kok-Yew Goh
Affiliation:
Centre for Research in Child Development, National Institute of Education, 1 Nanyang Walk, SingaporeS637616, Singapore
Hui Jun Chong
Affiliation:
Integrative Neurosciences, Singapore Institute for Clinical Sciences (SICS), Agency for Science and Technology (A*STAR), Brenner Centre for Molecular Medicine, Singapore117609, Singapore
Stella Tsotsi
Affiliation:
Centre for Research in Child Development, National Institute of Education, 1 Nanyang Walk, SingaporeS637616, Singapore
Lit Wee Sim
Affiliation:
Integrative Neurosciences, Singapore Institute for Clinical Sciences (SICS), Agency for Science and Technology (A*STAR), Brenner Centre for Molecular Medicine, Singapore117609, Singapore
Kok Hian Tan
Affiliation:
Division of Obstetrics and Gynaecology, KK Women and Children’s Hospital, Singapore229899, Singapore
Yap Seng Chong
Affiliation:
Integrative Neurosciences, Singapore Institute for Clinical Sciences (SICS), Agency for Science and Technology (A*STAR), Brenner Centre for Molecular Medicine, Singapore117609, Singapore Department of Gynaecology and Obstetrics, National University Hospital Singapore, Singapore119228, Singapore
Michael J. Meaney
Affiliation:
Integrative Neurosciences, Singapore Institute for Clinical Sciences (SICS), Agency for Science and Technology (A*STAR), Brenner Centre for Molecular Medicine, Singapore117609, Singapore Department of Psychiatry, Douglas Mental Health University Institute, McGill University, Montreal, Quebec, Canada Sackler Program for Epigenetics and Psychobiology, McGill University, Montreal, Quebec, Canada
*
Address for correspondence: Anne Rifkin-Graboi, Centre for Research in Child Development, National Institute of Education, 1 Nanyang Walk, SingaporeS637616, Singapore. Email: [email protected]

Abstract

From a conditional adaptation vantage point, early life caregiving adversity likely enhances aspects of cognition needed to manage interpersonal threats. Yet, research examining early life care and offspring cognition predominantly relies upon experiments including affectively neutral stimuli, with findings generally interpreted as “early-life caregiving adversity is, de facto, ‘bad’ for cognitive performance.” Here, in a Southeast Asian sample, we examined observed maternal sensitivity in infancy and cognitive performance 3 years later as preschoolers took part in three tasks, each involving both a socioemotional (SE) and non-socioemotional (NSE) version: relational memory (n = 236), cognitive flexibility (n = 203), and inhibitory control (n = 255). Results indicate the relation between early life caregiving adversity and memory performance significantly differs (Wald test = 7.67, (1), P = 0.006) depending on the SE versus NSE context, with maternal sensitivity in infancy highly predictive of worse memory for SE stimuli, and amongst girls, also predictive of better memory when NSE stimuli are used. Results concerning inhibitory control, as well as cognitive flexibility in girls, also tentatively suggest the importance of considering the SE nature of stimuli when assessing relations between the caregiving environment and cognitive performance. As not all approaches to missing data yielded similar results, implications for statistical approaches are elaborated. We conclude by considering how an adaptation-to-context framework approach may aid in designing pedagogical strategies and well-being interventions that harness pre-existing cognitive strengths.

Type
Original Article
Copyright
© The Author(s), 2021. Published by Cambridge University Press in association with International Society for Developmental Origins of Health and Disease

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Belsky, J, Steinberg, L, Draper, P. Childhood experience, interpersonal development, and reproductive strategy: an evolutionary theory of socialization. Child Dev. 1991; 62(4), 647670.CrossRefGoogle ScholarPubMed
Cahill, L, Alkire, MT. Epinephrine enhancement of human memory consolidation: interaction with arousal at encoding. Neurobiol Learn Mem. 2003; 79(2), 194198.CrossRefGoogle ScholarPubMed
Bernier, A, Carlson, SM, Whipple, N. From external regulation to self-regulation: early parenting precursors of young children’s executive functioning. Child Dev. 2010; 81(1), 326339.CrossRefGoogle ScholarPubMed
Matte-Gagne, C, Bernier, A, Sirois, MS, Lalonde, G, Hertz, S. Attachment Security and Developmental Patterns of Growth in Executive Functioning During Early Elementary School. Child Dev. 2018; 89(3), e167e182.CrossRefGoogle ScholarPubMed
Main, M. Avoidance in the service of attachment. In Behavioral Development (eds. Immelman, K. Barlow, G, Petrinovitch, L, Main, M), 1981; pp. 651693. Cambridge University Press, Cambridge, UK.Google Scholar
Gluckman, PD, Hanson, MA, Spencer, HG. Predictive adaptive responses and human evolution. Trends Ecol Evol. 2005; 20(10), 527533.CrossRefGoogle ScholarPubMed
Boyce, WT, Ellis, BJ. Biological sensitivity to context: I. An evolutionary-developmental theory of the origins and functions of stress reactivity. Dev Psychopathol. 2005; 17(2), 271–230.CrossRefGoogle ScholarPubMed
Ellis, BJ, Boyce, WT, Belsky, J, Bakermans-Kranenburg, MJ, van IJzendoorn, MH. Differential susceptibility to the environment: an evolutionary – neurodevelopmental theory. Dev Psychopathol. 2011; 23(1), 728.CrossRefGoogle Scholar
Cameron, NM, Champagne, FA, Parent, C, Fish, EW, Ozaki-Kuroda, K, Meaney, MJ. The programming of individual differences in defensive responses and reproductive strategies in the rat through variations in maternal care. Neurosci Biobehav Rev. 2005; 29(4–5), 843865.CrossRefGoogle ScholarPubMed
Mesman, J, van IJzendoorn, MH, Bakermans-Kranenburg, MJ. Unequal in opportunity, equal in process: parental sensitivity promotes positive child development in ethnic minority families. Child Dev Perspect. 2012; 6(3), 239250.CrossRefGoogle Scholar
Sapolsky, RM. Social status and health in humans and other animals. Annu Rev Anthropol. 2004; 33, 393418.CrossRefGoogle Scholar
Suomi, SJ. Attachment in rhesus monkeys. In Handbook of Attachment: Theory, Research, and Clinical Applications, 3rd Edition. (ed. Shaver, JCPR), 2016; pp. 133154. New York: The Guilford Press.Google Scholar
Perry, RE, Finegood, ED, Braren, SH, et al. Developing a neurobehavioral animal model of poverty: drawing cross-species connections between environments of scarcity-adversity, parenting quality, and infant outcome. Dev Psychopathol. 2018; 31(2): 399418.CrossRefGoogle ScholarPubMed
De Wolff, MS, van IJzendoorn, MH. Sensitivity and attachment: a meta-analysis on parental antecedents of infant attachment. Child Dev. 1997; 68(4), 571591.CrossRefGoogle ScholarPubMed
Madigan, S, Bakermans-Kranenburg, MJ, van IJzendoorn, MH, Moran, G, Pederson, DR, Benoit, D. Unresolved states of mind, anomalous parental behavior, and disorganized attachment: a review and meta-analysis of a transmission gap. Attach Hum Dev. 2006; 8(2), 89111.CrossRefGoogle ScholarPubMed
Klein Velderman, M, Bakermans-Kranenburg, MJ, Juffer, F, Van, IMH, Mangelsdorf, SC, Zevalkink, J. Preventing preschool externalizing behavior problems through video-feedback intervention in infancy. Infant Ment Health J. 2006; 27(5), 466493.CrossRefGoogle ScholarPubMed
Lewis-Morrarty, E, Dozier, M, Bernard, K, Terracciano, SM, Moore, SV. Cognitive flexibility and theory of mind outcomes among foster children: Preschool follow-up results of a randomized clinical trial. J Adolesc Health. 2012; 51(2, Suppl), S17S22.CrossRefGoogle ScholarPubMed
Bernard, K, Lee, AH, Dozier, M. Effects of the ABC intervention on foster children’s receptive vocabulary: follow-up results from a randomized clinical trial. Child Maltreatment. 2017; 22(2), 174179.CrossRefGoogle ScholarPubMed
Lind, T, Lee Raby, K, Caron, EB, Roben, CK, Dozier, M. Enhancing executive functioning among toddlers in foster care with an attachment-based intervention. Dev Psychopathol. 2017; 29(2), 575586.CrossRefGoogle ScholarPubMed
Raby, KL, Freedman, E, Yarger, HA, Lind, T, Dozier, M. Enhancing the language development of toddlers in foster care by promoting foster parents’ sensitivity: results from a randomized controlled trial. Dev Sci. 2018; 22, e12753.Google ScholarPubMed
Bakermans-Kranenburg, MJ, van IJzendoorn, MH, Pijlman, FTA, Mesman, J, Juffer, F. Experimental evidence for differential susceptibility: dopamine D4 receptor polymorphism (DRD4 VNTR) moderates intervention effects on toddlers’ externalizing behavior in a randomized controlled trial. Dev Psychol. 2008; 44(1), 293300.CrossRefGoogle Scholar
Bagot, RC, van Hasselt, FN, Champagne, DL, Meaney, MJ, Krugers, HJ, Joels, M. Maternal care determines rapid effects of stress mediators on synaptic plasticity in adult rat hippocampal dentate gyrus. Neurobiol Learn Mem. 2009; 92(3), 292300.CrossRefGoogle ScholarPubMed
Callaghan, BL, Richardson, R. The effect of adverse rearing environments on persistent memories in young rats: removing the brakes on infant fear memories. Transl Psychiatry. 2012; 2(7), e138.CrossRefGoogle ScholarPubMed
Tsotsi, S, Borelli, J, Binte Abdulla, N, et al. Maternal sensitivity during infancy and the regulation of startle in preschoolers. 2018. 1–18 p.Google Scholar
Rifkin-Graboi, A, Quan, J, Richmond, J, et al. Greater caregiving risk, better infant memory performance? Hippocampus. 2018; 28(7), 497511.CrossRefGoogle ScholarPubMed
Farrington, DP, Gallagher, B, Morley, L, St Ledger, RJ, West, DJ. Are there any successful men from criminogenic backgrounds? Psychiatry. 1988; 51(2), 116130.CrossRefGoogle ScholarPubMed
Kerr, M, Tremblay, RE, Pagani, L, Vitaro, F. Boys’ behavioral inhibition and the risk of later delinquency. Arch Gen Psychiatry. 1997; 54(9), 809816.CrossRefGoogle ScholarPubMed
Ellis, BJ, Abrams, LS, Masten, AS, Sternberg, RJ, Tottenham, N, Frankenhuis, WE. Hidden talents in harsh environments. Dev Psychopathol. 2020, 119.CrossRefGoogle ScholarPubMed
Pollak, SD, Klorman, R, Thatcher, JE, Cicchetti, D. P3b reflects maltreated children’s reactions to facial displays of emotion. Psychophysiology. 2001; 38(2), 267274.CrossRefGoogle ScholarPubMed
Shackman, JE, Shackman, AJ, Pollak, SD. Physical abuse amplifies attention to threat and increases anxiety in children. Emotion. 2007; 7(4), 838852.CrossRefGoogle ScholarPubMed
Pollak, SD, Cicchetti, D, Klorman, R, Brumaghim, JT. Cognitive brain event-related potentials and emotion processing in maltreated children. Child Dev. 1997; 68(5), 773787.CrossRefGoogle ScholarPubMed
Peltola, MJ, Forssman, L, Puura, K, van IJzendoorn, MH, Leppänen, JM. Attention to faces expressing negative emotion at 7 months predicts attachment security at 14 months. Child Dev. 2015; 86(5), 13211332.CrossRefGoogle ScholarPubMed
Zeijlmans van Emmichoven, IA, van IJzendoorn, MH, de Ruiter, C, Brosschot, JF. Selective processing of threatening information: effects of attachment representation and anxiety disorder on attention and memory. Dev Psychopathol. 2003; 15(1), 219237.CrossRefGoogle ScholarPubMed
Bernier, A, Carlson, SM, Deschenes, M, Matte-Gagne, C. Social factors in the development of early executive functioning: a closer look at the caregiving environment. Dev Sci. 2012; 15(1), 1224.CrossRefGoogle Scholar
Merz, EC, Landry, SH, Montroy, JJ, Williams, JM. Bidirectional associations between parental responsiveness and executive function during early childhood. Soc Dev (Oxford, England). 2017; 26(3), 591609.Google ScholarPubMed
Mittal, C, Griskevicius, V, Simpson, JA, Sung, S, Young, ES. Cognitive adaptations to stressful environments: when childhood adversity enhances adult executive function. J Pers Soc Psychol. 2015; 109(4), 604621.CrossRefGoogle ScholarPubMed
Phelps, EA, LeDoux, JE. Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron. 2005; 48(2), 175187.CrossRefGoogle ScholarPubMed
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 U S A. 2012; 109(20), E1312E1319.CrossRefGoogle ScholarPubMed
Gee, DG, Gabard-Durnam, LJ, Flannery, J, et al. Early developmental emergence of human amygdala-prefrontal connectivity after maternal deprivation. Proc Natl Acad Sci U S A. 2013; 110(39), 1563815643.CrossRefGoogle ScholarPubMed
Hanson, JL, Nacewicz, BM, Sutterer, MJ, et al. Behavioral problems after early life stress: contributions of the hippocampus and amygdala. Biol Psychiatry. 2015; 77(4), 314323.CrossRefGoogle ScholarPubMed
Rifkin-Graboi, A, Bai, J, Chen, H, et al. Prenatal maternal depression associates with microstructure of right amygdala in neonates at birth. Biol Psychiatry. 2013; 74(11), 837844.CrossRefGoogle ScholarPubMed
Thijssen, S, Muetzel, RL, Bakermans-Kranenburg, MJ, et al. Insensitive parenting may accelerate the development of the amygdala–medial prefrontal cortex circuit. Dev Psychopathol. 2017; 29(2), 505518.CrossRefGoogle ScholarPubMed
Lee, A, Poh, JS, Wen, DJ, et al. Maternal care in infancy and the course of limbic development. Dev Cogn Neurosci. 2019; 40, 100714.CrossRefGoogle ScholarPubMed
Bernier, A, Dégeilh, F, Leblanc, É, Daneault, V, Bailey, HN, Beauchamp, MH. Mother–infant interaction and child brain morphology: a multidimensional approach to maternal sensitivity. Infancy. 2019; 24(2), 120138.CrossRefGoogle ScholarPubMed
Rao, H, Betancourt, L, Giannetta, JM, et al. Early parental care is important for hippocampal maturation: evidence from brain morphology in humans. NeuroImage. 2010; 49(1), 11441150.CrossRefGoogle ScholarPubMed
Luby, JL, Belden, A, Harms, MP, Tillman, R, Barch, DM. Preschool is a sensitive period for the influence of maternal support on the trajectory of hippocampal development. Proc Natl Acad Sci U S A. 2016; 113(20), 57425747.CrossRefGoogle ScholarPubMed
Moutsiana, C, Fearon, P, Murray, L, et al. Making an effort to feel positive: insecure attachment in infancy predicts the neural underpinnings of emotion regulation in adulthood. J Child Psychol Psychiatry. 2014; 55(9), 9991008.CrossRefGoogle ScholarPubMed
Narita, K, Takei, Y, Suda, M, et al. Relationship of parental bonding styles with gray matter volume of dorsolateral prefrontal cortex in young adults. Prog Neuropsychopharmacol Biol Psychiatry. 2010; 34(4), 624631.CrossRefGoogle ScholarPubMed
Merz, EC, Landry, SH, Zucker, TA, et al. Parenting predictors of delay inhibition in socioeconomically disadvantaged preschoolers. Infant Child Dev. 2016; 25(5), 371390.CrossRefGoogle ScholarPubMed
McClure, EB. A meta-analytic review of sex differences in facial expression processing and their development in infants, children, and adolescents. Psychol Bull. 2000; 126(3), 424453.CrossRefGoogle ScholarPubMed
Kim, MJ, Loucks, RA, Palmer, AL, et al. The structural and functional connectivity of the amygdala: from normal emotion to pathological anxiety. Behav Brain Res. 2011; 223(2), 403410.CrossRefGoogle ScholarPubMed
Soh, SE, Tint, MT, Gluckman, PD, et al. Cohort profile: Growing Up in Singapore Towards healthy Outcomes (GUSTO) birth cohort study. Int J Epidemiol. 2014; 43(5), 14011409.CrossRefGoogle ScholarPubMed
Madigan, S, Moran, G, Pederson, DR. Unresolved states of mind, disorganized attachment relationships, and disrupted interactions of adolescent mothers and their infants. Dev Psychol. 2006; 42(2), 293304.CrossRefGoogle ScholarPubMed
Moran, G. Mini-MBQS-V Revised Mini-MBQS 25 Item for Video Coding. 2009. Retrieved from http://works.bepress.com/gregmoran/49 CrossRefGoogle Scholar
Moran, G, Pederson, DR, Bento, S. Maternal Behavior Q-Sort (MBQS) – Overview, Available Materials and Support. 2009. Retrieved from http://works.bepress.com/gregmoran/48 Google Scholar
Heng, J, Quan, J, Sim, LW, et al. The role of ethnicity and socioeconomic status in Southeast Asian mothers’ parenting sensitivity. Attach Hum Dev. 2018; 20(1), 2442.CrossRefGoogle ScholarPubMed
Egger, HL, Pine, DS, Nelson, E, et al. The NIMH Child Emotional Faces Picture Set (NIMH-ChEFS): a new set of children’s facial emotion stimuli. Int J Methods Psychiatry Res. 2011; 20(3), 145156.CrossRefGoogle ScholarPubMed
Zelazo, PD. The Dimensional Change Card Sort (DCCS): a method of assessing executive function in children. Nat Protoc. 2006; 1(1), 297301.CrossRefGoogle ScholarPubMed
Goh, SKY, Yang, H, Tsotsi, S, et al. Mitigation of a prospective association between early language delay at toddlerhood and ADHD among bilingual preschoolers: evidence from the GUSTO cohort. J Abnorm Child Psychol. 2020; 48(4), 511523. doi: 10.1007/s10802-019-00607-5 CrossRefGoogle ScholarPubMed
Tsotsi, S, Broekman, BFP, Sim, LW, et al. Maternal anxiety, parenting stress, and preschoolers’ behavior problems: the role of child self-regulation. J Dev Behav Pediatr. 2019; 40(9), 696705.CrossRefGoogle ScholarPubMed
Kochanska, G, Murray, KT, Harlan, ET. Effortful control in early childhood: Continuity and change, antecedents, and implications for social development. Dev Psychol. 2000; 36(2), 220232.CrossRefGoogle ScholarPubMed
Wen, DJ, Soe, NN, Sim, LW, et al. Infant frontal EEG asymmetry in relation with postnatal maternal depression and parenting behavior. Transl Psychiatry. 2017; 7(3), e1057.CrossRefGoogle ScholarPubMed
Muthén, LK, Muthén, BO. Mplus: Statistical Analysis with Latent Variables: User’s Guide. 8th Edition, 2017. Los Angeles, CA: Muthén & Muthén.Google Scholar
Field, AP. Discovering Statistics Using IBM SPSS Statistics, 2013. SAGE Publications, Thousand Oaks, CA.Google Scholar
Bernier, A, Beauchamp, MH, Carlson, SM, Lalonde, G. A secure base from which to regulate: Attachment security in toddlerhood as a predictor of executive functioning at school entry. Dev Psychol. 2015; 51(9), 11771189.CrossRefGoogle ScholarPubMed
McEwen, BS, Nasca, C, Gray, JD. Stress effects on neuronal structure: hippocampus, amygdala, and prefrontal cortex. Neuropsychopharmacology. 2016; 41(1), 323.CrossRefGoogle ScholarPubMed
Frankenhuis, WE, de Weerth, C. Does early-life exposure to stress shape or impair cognition? Curr Dir Psychol Sci. 2013; 22(5), 407412.CrossRefGoogle Scholar
Frankenhuis, WE, Panchanathan, K, Nettle, D. Cognition in harsh and unpredictable environments. Curr Opin Psychol. 2016; 7, 7680.CrossRefGoogle Scholar
Noble, KG, McCandliss, BD, Farah, MJ. Socioeconomic gradients predict individual differences in neurocognitive abilities. Dev Sci. 2007; 10(4), 464480.CrossRefGoogle ScholarPubMed
Dunn, EC, Busso, DS, Raffeld, MR, et al. Does developmental timing of exposure to child maltreatment predict memory performance in adulthood? Results from a large, population-based sample. Child Abuse Negl. 2016; 51, 181191.CrossRefGoogle ScholarPubMed
Qiu, A, Rifkin-Graboi, A, Chen, H, et al. Maternal anxiety and infants’ hippocampal development: timing matters. Transl Psychiatry. 2013; 3, e306.CrossRefGoogle ScholarPubMed
Krogsrud, SK, Tamnes, CK, Fjell, AM, et al. Development of hippocampal subfield volumes from 4 to 22 years. Hum Brain Mapp. 2014; 35(11), 56465657.CrossRefGoogle ScholarPubMed
Lin, M, Fwu, PT, Buss, C, et al. Developmental changes in hippocampal shape among preadolescent children. Int J Dev Neurosci. 2013; 31(7), 473481.CrossRefGoogle ScholarPubMed
Uematsu, A, Matsui, M, Tanaka, C, et al. Developmental trajectories of amygdala and hippocampus from infancy to early adulthood in healthy individuals. PLoS One. 2012; 7(10), e46970.CrossRefGoogle ScholarPubMed
Tamnes, CK, Bos, MGN, van de Kamp, FC, Peters, S, Crone, EA. Longitudinal development of hippocampal subregions from childhood to adulthood. Dev Cogn Neurosci. 2018; 30, 212222.CrossRefGoogle ScholarPubMed
Rifkin-Graboi, A, Kong, L, Sim, LW, et al. Maternal sensitivity, infant limbic structure volume and functional connectivity: a preliminary study. Transl Psychiatry. 2015; 5, e668.CrossRefGoogle ScholarPubMed
Pauli-Pott, U, Schloß, S, Becker, K. Maternal responsiveness as a predictor of self-regulation development and attention-deficit/hyperactivity symptoms across preschool ages. Child Psychiatry Hum Dev. 2018; 49(1), 4252.CrossRefGoogle ScholarPubMed
Leerkes, EM, Weaver, JM, O’Brien, M. Differentiating maternal sensitivity to infant distress and non-distress. Parent Sci Pract. 2012; 12(2–3), 175184.CrossRefGoogle ScholarPubMed
Main, M, Kaplan, N, Cassidy, J. Security in infancy, childhood and adulthood: a move to the level of representation. Monographs of the Society for Research in Child Dev. 1985; 50(1–), 66104. doi: 10.2307/3333827.CrossRefGoogle Scholar
Kirsh, SJ, Cassidy, J. Preschoolers’ attention to and memory for attachment-relevant information. Child Dev. 1997; 68(6), 11431153.CrossRefGoogle ScholarPubMed
Frankenhuis, WE, Nettle, D. The strengths of people in poverty. Curr Dir Psychol Sci. 2019; 29(1), 1621.CrossRefGoogle Scholar
Williford, C, Carter, LM, Pianta, RC. Attachment & School Readiness. In Handbook of Attachment, 3rd ed (eds. Cassidy, J, Shave, P), 2016; pp. 966982. Guilford Press, New York, NY.Google Scholar
Supplementary material: File

Rifkin-Graboi et al. supplementary material

Rifkin-Graboi et al. supplementary material

Download Rifkin-Graboi et al. supplementary material(File)
File 378.5 KB