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Cited by 279Child and Adolescent Psychosocial and Emotional DevelopmentNeural and Behavioral Psychology StudiesFunctional Brain Connectivity Studies

Positive parenting predicts the development of adolescent brain structure: a longitudinal study

Open access
Whittle, Sarah, Simmons, Julian G., Dennison, Meg, Vijayakumar, Nandita, Schwartz, Orli, Yap, Marie B.H., Sheeber, Lisa, Allen, Nicholas B.·2014·Developmental Cognitive Neuroscience
DOI 10.1016/j.dcn.2013.10.006PMC PMC6990097
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Abstract

Little work has been conducted that examines the effects of positive environmental experiences on brain development to date. The aim of this study was to prospectively investigate the effects of positive (warm and supportive) maternal behavior on structural brain development during adolescence, using longitudinal structural MRI. Participants were 188 (92 female) adolescents, who were part of a longitudinal adolescent development study that involved mother-adolescent interactions and MRI scans at approximately 12 years old, and follow-up MRI scans approximately 4 years later. FreeSurfer software was used to estimate the volume of limbic-striatal regions (amygdala, hippocampus, caudate, putamen, pallidum, and nucleus accumbens) and the thickness of prefrontal regions (anterior cingulate and orbitofrontal cortices) across both time points. Higher frequency of positive maternal behavior during the interactions predicted attenuated volumetric growth in the right amygdala, and accelerated cortical thinning in the right anterior cingulate (males only) and left and right orbitofrontal cortices, between baseline and follow up. These results have implications for understanding the biological mediators of risk and protective factors for mental disorders that have onset during adolescence.

AI snapshot

Written from the paper’s full text.

TL;DR

In a longitudinal community sample of adolescents, observed positive maternal behavior during a conflictual interaction predicted structural brain development from early to mid-adolescence, including reduced right amygdala growth and greater left/right OFC thinning. Effects were partly sex-specific for right ACC thinning in males and were not explained by aggressive maternal behavior.

Key findings

  • Higher positive maternal behavior predicted reduced growth of the right amygdala (β = −0.284, p = 0.014) and greater thinning of the left and right OFC (β = −0.262, p = 0.024; β = −0.258, p = 0.022).
  • Positive maternal behavior × sex predicted right ACC change (β = −0.311, p = 0.045); follow-up analyses showed greater right ACC thinning in males (β = −0.525, p = 0.007) but no association in females (β = 0.042, p = 0.789).
  • Aggressive maternal behavior predicted increased growth of the right putamen (β = 0.306, p = 0.012); positive maternal behavior effects were not better explained by aggressive maternal behavior.
  • Positive parenting was not associated with the structure of the majority of regions at baseline or follow-up (reported as Supplementary data).

Methods

  • Participants were a community sample of 188 adolescents (92 females) from metropolitan Melbourne, Australia; 163 completed baseline mother–adolescent interaction tasks, and 102 had acceptable baseline and follow-up MRI data (mean follow-up = 3.78 years, SD = 0.20; baseline MRI age = 12.62, SD = 0.44; follow-up MRI age = 16.42, SD = 0.50).
  • Mother–adolescent dyads completed videotaped event-planning and problem-solving interactions coded with the LIFE system; positive maternal behavior was taken from the problem-solving interaction and aggressive maternal behavior from the event-planning interaction. MRI was processed with FreeSurfer longitudinal stream for subcortical volumes (amygdala, hippocampus, caudate, nucleus accumbens, putamen, pallidum) and cortical thickness (ACC, OFC).
  • Hierarchical linear regressions predicted residualized ROI change scores, with covariates age, SES, IQ, depressive and anxiety symptoms, and aggressive maternal behavior; positive maternal behavior and sex were entered next, followed by their interaction. Missing data were handled with FIML in Mplus.

Limitations

  • Stated: only two imaging time points limited modeling to linear patterns of brain development, so non-linear effects and effects extending into late adolescence or adulthood could not be assessed.
  • Stated: only one observed measure of positive parenting was used; fathers were not included; temperament-based sampling may restrict generalizability; no correction for multiple comparisons was applied; some FreeSurfer structures (particularly amygdala and nucleus accumbens) have relatively low reliability; multisite scanner/sequence bias was possible though post-acquisition procedures and an inter-scanner reliability assessment were used.
  • Evident from the text: the observational longitudinal design cannot establish causal effects, and the MRI sample was 102 with complete-case analyses also run in 77 participants, which may limit power and generalizability alongside the temperament oversampling.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1016/j.dcn.2013.10.006

Cites

84 of 84 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 38 cited sources checked · 0 supported · 0 flagged

  • Findingcitation

    The caudate, thalamus, and putamen declined in volume over time from early to mid-adolescence in this sample.

    “Briefly, we found the caudate, thalamus and putamen to decline in volume over time.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Dennison et al., 2013 source

      Not checked in the free run.

  • Findingown data

    A higher rate of positive maternal behavior was associated with reduced growth of the right amygdala from early to mid-adolescence.

    “Higher rate of positive maternal behavior was associated with reduced growth of the right amygdala from early- to mid-adolescence”
    Quote in the paperSubstantial claim
  • Findingown data

    A higher rate of positive maternal behavior was associated with greater thinning of the left OFC.

    “left and right OFC (β = −0.262, p = 0.024; β = −0.258, p = 0.022, respectively)”
    Quote in the paperSubstantial claim
  • Findingown data

    Aggressive maternal behavior predicted increased growth of the right putamen over time.

    “Aggressive maternal behavior was associated with change in only one ROI, the right putamen; specifically, it predicted increased growth of this structure over time (β = 0.306, p = 0.012).”
    Quote in the paperNot a substantial claim
  • Findingcitation

    We found no evidence for significant development of the amygdala from early- to mid-adolescence in this sample.

    “Although we found no evidence for significant development of the amygdala from early- to mid-adolescence in this sample (Dennison et al., 2013)”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Dennison et al., 2013 source

      Not checked in the free run.

  • Classified as probably not a substantial claim. 26
  • The quote only partly states this claim. 1
  • May combine two claims. 10

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingown data

    Whole-brain-corrected thickness was greater in the left compared to the right ACC.

    “Whole brain corrected thickness was greater in the left compared to the right ACC.”
    Quote in the paperNot a substantial claim

  • The quote only partly states this claim.

    Findingown data

    Higher frequency of positive maternal behavior was associated with accelerated thinning of the left and right OFC from early to midadolescence.

    “We found that higher frequency of positive maternal behavior was associated with reduced growth of the right amygdala, and accelerated thinning of the left and right OFC and right ACC (males only) from early to midadolescence.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Positive parenting was associated with development in a number of brain regions, but was not associated with the structure of the majority of these regions at baseline or follow-up.

    “While we found that positive parenting was associated with development in a number of regions, it was not associated with the structure of the majority of these regions at baseline or follow-up (see Supplementary data).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Amygdala volume did not change over time, but the left amygdala was larger than the right.

    “While amygdala volume did not change over time, there was a main effect of hemisphere such that the left amygdala was larger than the right.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Dennison et al., 2013 source

      Not checked in the free run.

  • May combine two claims.

    Findingown data

    The OFC showed significant thinning over time, with greater thinning in the left compared to the right hemisphere.

    “There was significant thinning in the OFC over time, with greater thinning in the left compared to the right hemisphere.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    The ACC showed significant thinning over time, with greater thinning in the right compared to the left hemisphere.

    “There was significant thinning in the ACC over time, with greater in the right compared to the left hemisphere.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingcitation

    The left nucleus accumbens increased in size while the right nucleus accumbens decreased in size over the follow-up period.

    “While the left nucleus accumbens increased in size, the right accumbens decreased in size over the follow-up period.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Dennison et al., 2013 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Environmental enhancement has effects on brain development across the lifespan.

    “A wealth of animal studies indicates that environmental enhancement has effects on brain development across the lifespan (Halperin and Healey, 2011).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Halperin and Healey, 2011 source

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Adverse childhood environments are an important risk factor for the development of psychopathology later in life.

    “Adverse childhood environments represent an important risk factor for the development of psychopathology later in life (Heim and Nemeroff, 2001, Moran et al., 2004)”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Heim and Nemeroff, 2001 source

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    • cites Moran et al., 2004 source

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  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation

    Decreased levels of psychopathology are associated with attenuated growth of the amygdala and accelerated growth of the hippocampus during adolescence.

    “Our previous work has shown that decreased levels of psychopathology are associated with attenuated growth of the amygdala, and accelerated growth of the hippocampus, during adolescence (Whittle et al., 2013).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Whittle et al., 2013

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Neurobiological changes, particularly in brain structure, may mediate the relationship between adverse childhood environments and later psychopathology.

    “there is accumulating evidence that neurobiological changes (particularly with regard to brain structure) may mediate this relationship (Tupler and De Bellis, 2006).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Tupler and De Bellis, 2006

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    There is some evidence from animal studies that environmental enrichment has an effect on amygdala development.

    “there is some evidence from animal studies that environmental enrichment has an effect on amygdala development (Okuda et al., 2009).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Okuda et al., 2009

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Positive and aggressive maternal behavior do not exist on a continuum of positive to negative, but rather may reflect two different aspects of parenting behaviors that have distinct effects on children's brain development.

    “These results suggest that positive and aggressive maternal behavior do not exist on a continuum of positive to negative, but rather may reflect two different aspects of parenting behaviors that have distinct effects on children's brain development.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationown data

    The frequency of positive maternal behavior during early adolescence was associated with structural development of regions implicated in reward processes, emotional reactivity, and regulation, with some sex differences also being observed.

    “We found that the frequency of positive maternal behavior during early adolescence was associated with structural development of regions implicated in reward processes, emotional reactivity and regulation, with some sex differences also being observed.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Premisecitation

    The interaction between prefrontal structures and the amygdala is critical to emotion regulation.

    “There is also evidence that the interaction between prefrontal structures and the amygdala is critical to emotion regulation”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Banks et al., 2007 source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    Positive maternal behaviors are thought to shape the development of their children's ability to regulate emotion and behaviors.

    “given that positive maternal behaviors are thought to shape the development of their children's ability to regulate emotion and behaviors (Yap et al., 2010)”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Yap et al., 2010 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    The use of observed (as opposed to self-report) measures of maternal behavior is a strength of the study.

    “although the use of observed (as opposed to self-report) measures of maternal behavior is a strength of the study”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Study design and conductnone given

    Post-acquisition procedures were adopted to minimize, as much as possible, any scanner/sequence effects on the acquired images.

    “post-acquisition procedures were adopted to minimize, as much as possible, any scanner/sequence effects on the acquired images.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Premisecitation

    Prefrontal down-regulation of amygdala activity has been associated with the attenuation of negative affect during emotion regulation.

    “specifically prefrontal down-regulation of amygdala activity has been associated with the attenuation of negative affect during emotion regulation (Banks et al., 2007).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Banks et al., 2007 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    We did not assess other (or more specific) aspects of positive parenting (such as warmth, responsivity, and support) that may be important protective factors for other deleterious outcomes.

    “we did not assess other (or more specific) aspects of positive parenting (such as warmth, responsivity, and support) that may be important protective factors for other deleterious outcomes.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Premisecitation

    The amygdala is thought to be primarily involved in detection of, and reactivity to, emotionally salient stimuli.

    “The amygdala is thought to be primarily involved in detection of, and reactivity to, emotionally salient stimuli (Habel et al., 2005).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Habel et al., 2005

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductown data

    We were unable to include fathers in analyses, due to the low number of participating fathers in the study.

    “we were unable to include fathers in analyses, due to the low number of participating fathers in the study.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Others have found normative increases in the volume of the amygdala over the adolescent years.

    “others have found normative increases in the volume of this structure over the adolescent years (e.g., Ostby et al., 2009).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Ostby et al., 2009 source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    Shaw et al. (2006) found that adolescents with superior intellectual abilities exhibited greater cortical thinning in a number of cortical areas, including the OFC, into adulthood.

    “Specifically, Shaw et al. (2006), using a cohort-sequential design, found that adolescents with superior intellectual abilities exhibited greater cortical thinning in a number of cortical areas, including the OFC, into adulthood.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Shaw et al., 2006 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductnone given

    MRI scans were acquired multisite, with different imaging sequences acquired at each site.

    “as MRI scans were acquired multisite, with different imaging sequences acquired at each site”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductown data

    We cannot comment on whether positive parenting has non-linear effects on brain development, or whether the effects may extend into late adolescence and adulthood.

    “we cannot comment on whether positive parenting has non-linear effects on brain development, or whether the effects may extend into late adolescence and adulthood.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Low levels of psychopathology were associated with attenuated amygdala development from early to midadolescence.

    “our previous finding that low levels of psychopathology were associated with attenuated amygdala development from early to midadolescence (Whittle et al., 2013)”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Whittle et al., 2013

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    In other work with the current sample, greater thinning in the ACC was associated with higher temperamental effortful control.

    “Finally, in other work with the current sample, we have found that greater thinning in the ACC was associated with higher temperamental effortful control (Vijayakumar et al., in press-b).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Vijayakumar et al., in press-b

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductreasoning

    There is a possibility of scanner/sequence bias affecting volumetric and thickness estimates.

    “there is a possibility of scanner/sequence bias affecting volumetric and thickness estimates.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable).

    Interpretationreasoning

    Our results have implications for understanding the mechanisms underlying the relationship between positive parenting and reduced risk for a range of negative outcomes.

    “Our findings may have implications for understanding the mechanisms underlying the relationship between positive parenting and reduced risk for a range of negative outcomes.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: Positive parenting has been found to be associated with increased positive adolescent outcomes, and resilience against negative adolescent outcomes.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    Given our temperamental sampling strategy, our results may have restricted generalizability.

    “given our temperamental sampling strategy, our results may have restricted generalizability.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Sample sizes of approximately 80 and above are suggested to be adequately powered to detect small to medium effect sizes in these structures.

    “sample sizes of approximately 80 and above are suggested to be adequately powered to detect small to medium effect sizes in these structures (Morey et al., 2010).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Morey et al., 2010

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S4 (based).

    Study design and conductnone given

    It is very unlikely that the measure of positive maternal behavior interacted with scanner or sequence type in any way that might bias the reported results.

    “it is very unlikely that the measure of positive maternal behavior interacted with scanner or sequence type in any way that might bias the reported results.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Study design and conductnone given

    We did not control for multiple comparisons.

    “we did not control for multiple comparisons”
    Quote in the paperSubstantial claim
34 of 34

  • The paper relies on this without support.

    Little work has examined the effects of positive parenting on brain structure in children and adolescents.

    “Despite this evidence, to date, little work has been conducted that examines the effects of positive parenting on brain structure in children and adolescents.”

  • The paper relies on this without support.

    None of the existing research has assessed longitudinal measures of brain development.

    “Second, to our knowledge, none of the existing research has assessed longitudinal measures of brain development.”

  • The paper relies on this without support.

    The longitudinal associations between positive parenting and adolescent brain structure reflect causal effects of positive parenting rather than unmeasured confounding.

    “we have found, for the first time, longitudinal effects of positive parenting on structural development of the brain during adolescence.”

  • The paper relies on this without support.

    No other human study to date has reported an effect of positive parenting on amygdala structure.

    “Although no other human study to date has reported an effect of positive parenting on amygdala structure”

  • The paper relies on this without support.

    Abnormalities in the structure and function of the amygdala, OFC, and ACC have been found in both adolescent and adult depression.

    “Abnormalities in the structure and function of all of the regions associated with positive parenting in the current study (i.e., amygdala, OFC, ACC) have been found in both adolescent and adult depression.”

  • The paper relies on this without support.

    Reliability for some FreeSurfer delineated structures (particularly the amygdala and nucleus accumbens) is relatively low.

    “it has been suggested that reliability for some FreeSurfer delineated structures (particularly the amygdala and nucleus accumbens) is relatively low”

  • The paper relies on this without support.

    Positive parenting has been found to be associated with increased positive adolescent outcomes, and resilience against negative adolescent outcomes.

    “Given that positive parenting has been found to be associated with increased positive adolescent outcomes, and resilience against negative adolescent outcomes”
7 of 7

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Cites

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Research works printed but not linked: 4

  1. Ellis, 2001, Revision of the Early Adolescent Temperament Questionnaire. 2001 Biennial Meeting of the Society for Research in Child Development; Minneapolis, Minnesota
  2. Hops, 1995, Methodological issues in direct observation: illustration with the living in familial environments (life) coding system, J. Clin. Child Psychol., 24, 193, 10.1207/s15374424jccp2402_7 · DOI
  3. Lorenzetti, 2009, Structural brain abnormalities in major depressive disorder: a selective review of recent MRI studies, J. Affect. Disord., 117, 1, 10.1016/j.jad.2008.11.021 · DOI · Paper page
  4. Schwarz, 2012, Parental behaviors during family interactions predict changes in depression and anxiety during adolescence, J. Abnorm. Psychol., 40, 59, 10.1007/s10802-011-9542-2 · DOI · Paper page

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Related

Authors
Whittle, S., Simmons, J. G., Dennison, M., Vijayakumar, N., Schwartz, O., Yap, M. B. H., Sheeber, L., & Allen, N. B.
Affiliations
  • The University of Melbourne (AU)
  • Oregon Research Institute (US)
Corresponding author
Allen, Nicholas B.
ORCID
Venue
Developmental Cognitive Neuroscience
Publisher
Elsevier BV
Published
2014-04
Volume
8
Pages
7-17
ISSN
1878-9293 (ISSN-L)
DOI
10.1016/j.dcn.2013.10.006
PMC
PMC6990097
OpenAlex
W1972771337
Cited by
279
References
84
Citations by year
2026: 13 · 2025: 19 · 2024: 20 · 2023: 22 · 2022: 34 · 2021: 51 · 2020: 20 · 2019: 20 · 2018: 21 · 2017: 24 · 2016: 18 · 2015: 12 · 2014: 4
FWCI
12.61
Type
journal article
Language
en
Open access
Licence
Locations
  • Developmental Cognitive Neuroscience (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • Minerva Access (University of Melbourne) (submittedVersion, cc-by-nc-nd)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Deakin Research Online (Deakin University) (submittedVersion)
  • Figshare (submittedVersion, cc-by)
  • Minerva Access (University of Melbourne) (submittedVersion)
Funders
  • Colonial Foundation
  • National Health and Medical Research Council (350241)
  • Australian Research Council (DP0878136)
  • University of Melbourne
Topics
  • Social Sciences › Psychology › Clinical Psychology › Child and Adolescent Psychosocial and Emotional Development
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
Keywords
positive parenting, maternal behavior, adolescent brain development, structural brain development, amygdala volume, cortical thinning, anterior cingulate cortex, orbitofrontal cortex, mother-adolescent interaction, protective factors
MeSH terms
Adolescent, Amygdala, Brain, Child, Child, Preschool, Female, Gyrus Cinguli, Hippocampus, Humans, Longitudinal Studies, Magnetic Resonance Imaging, Male, Maternal Behavior, Mother-Child Relations, Mothers, Reward, Sex Characteristics, Parenting, Prefrontal Cortex, Adolescent Development

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