Interaction of parenting experiences and brain structure in the prediction of depressive symptoms in adolescents.

CONTEXT Although some evidence suggests that neuroanatomic abnormalities may confer risk for major depressive disorder, findings are inconsistent. One potential explanation for this is the moderating role of environmental context, with individuals differing in their biological sensitivity to context. OBJECTIVE To examine the influence of adverse parenting as an environmental moderator of the association between brain structure and depressive symptoms. DESIGN Cross-sectional measurement of brain structure, adverse parenting, and depressive symptoms in early adolescents. SETTING General community. PARTICIPANTS A total of 106 students aged 11 to 13 years (55 males [51%]), recruited from primary schools in Melbourne, Australia, and their mothers. Selection was based on affective temperament, aimed at producing a sample representing a broad range of risk for major depressive disorder. No participant evidenced current or past case-level depressive, substance use, or eating disorder. MAIN OUTCOME MEASURES (1) Volumetric measures of adolescents' amygdala, hippocampus, and anterior cingulate cortex (ACC); (2) frequency of observed maternal aggressive behavior during a mother-adolescent conflict-resolution interaction; and (3) adolescent depressive symptoms. RESULTS Boys with smaller right amygdalas reported more depressive symptoms. However, neither hippocampal volume nor asymmetry measures of limbic or paralimbic ACC were directly related to level of depressive symptoms. Importantly, frequency of maternal aggressive behaviors moderated the associations between both the amygdala and ACC, and adolescent symptoms. Particularly, in conditions of low levels of maternal aggressiveness, boys with larger right amygdalas, girls with smaller bilateral amygdalas, and both boys and girls with smaller left paralimbic ACC reported fewer symptoms. CONCLUSIONS These findings help elucidate the complex relationships between brain structure, environmental factors, and depressive symptoms. Further longitudinal research is required to examine how these factors contribute to the onset of case-level disorder, but given that family context risk factors are modifiable, our findings do suggest the potential utility of targeted early parenting interventions.

[1]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[2]  B. Everitt,et al.  Statistical methods for rates and proportions , 1973 .

[3]  Jacob Cohen,et al.  Applied multiple regression/correlation analysis for the behavioral sciences , 1979 .

[4]  L. Radloff.  The CES-D Scale , 1977 .

[5]  R. L. Burgess,et al.  Family interaction in abusive, neglectful, and normal families. , 1978, Child development.

[6]  K. O’leary,et al.  Multivariate assessment of conflict in distressed and nondistressed mother-adolescent dyads. , 1979, Journal of applied behavior analysis.

[7]  Daniel B Hier.  Sex differences in hemispheric specialization: Hypothesis for the excess of dyslexia in boys , 1979 .

[8]  Glenn D. Rosen,et al.  Planum temporale asymmetry, reappraisal since Geschwind and Levitsky , 1987, Neuropsychologia.

[9]  C. Jack,et al.  Anterior temporal lobes and hippocampal formations: normative volumetric measurements from MR images in young adults. , 1989, Radiology.

[10]  M. Forgatch.  Patterns and Outcome in Family Problem Solving: The Disrupting Effect of Negative Emotion. , 1989 .

[11]  L. Radloff.  The use of the Center for Epidemiologic Studies Depression Scale in adolescents and young adults , 1991, Journal of youth and adolescence.

[12]  Personality antecedents of depressive tendencies in 18-year-olds: a prospective study. , 1991, Journal of personality and social psychology.

[13]  F Andermann,et al.  Anatomic basis of amygdaloid and hippocampal volume measurement by magnetic resonance imaging , 1992, Neurology.

[14]  J. Sinacore.  Multiple regression: Testing and interpreting interactions , 1993 .

[15]  H. Hops,et al.  Methodological issues in direct observation: Illustrations with the living in familial environments (LIFE) coding system , 1995 .

[16]  D. Reiss,et al.  Genetic questions for environmental studies. Differential parenting and psychopathology in adolescence. , 1995, Archives of general psychiatry.

[17]  J. Rapoport,et al.  Quantitative MRI of the temporal lobe, amygdala, and hippocampus in normal human development: Ages 4–18 years , 1995, The Journal of comparative neurology.

[18]  R. Kessler,et al.  The effects of stressful life events on depression. , 1997, Annual review of psychology.

[19]  M. Raichle,et al.  Subgenual prefrontal cortex abnormalities in mood disorders , 1997, Nature.

[20]  Jagath C. Rajapakse,et al.  Sexual dimorphism of the developing human brain , 1997, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[21]  H. Hops,et al.  Family Support and Conflict: Prospective Relations to Adolescent Depression , 1997, Journal of abnormal child psychology.

[22]  H. Hops,et al.  Child responses to parental conflict and their effect on adjustment: A study of triadic relations. , 1998 .

[23]  B. O'Connor,et al.  SIMPLE: All-in-One Programs for Exploring Interactions in Moderated Multiple Regression , 1998 .

[24]  L. Sheeber,et al.  Family relationships of depressed adolescents: a multimethod assessment. , 1998, Journal of clinical child psychology.

[25]  C. Pantelis,et al.  Hippocampal volume in first-episode psychoses and chronic schizophrenia: a high-resolution magnetic resonance imaging study. , 1999, Archives of general psychiatry.

[26]  B. McEwen,et al.  Effects of adverse experiences for brain structure and function , 2000, Biological Psychiatry.

[27]  F. Gardner.  Methodological Issues in the Direct Observation of Parent–Child Interaction: Do Observational Findings Reflect the Natural Behavior of Participants? , 2000, Clinical child and family psychology review.

[28]  Michael Davis,et al.  The amygdala: vigilance and emotion , 2001, Molecular Psychiatry.

[29]  R. Kahn,et al.  Quantitative genetic modeling of variation in human brain morphology. , 2001, Cerebral cortex.

[30]  W. Drevets.  Neuroimaging and neuropathological studies of depression: implications for the cognitive-emotional features of mood disorders , 2001, Current Opinion in Neurobiology.

[31]  Stephen M. Smith,et al.  Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm , 2001, IEEE Transactions on Medical Imaging.

[32]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[33]  William D S Killgore,et al.  Sex-specific developmental changes in amygdala responses to affective faces , 2001, Neuroreport.

[34]  B. Fagot,et al.  Coercive family processes: A replication and extension of Patterson’s coercion model , 2001 .

[35]  H. Möller,et al.  Hippocampal changes in patients with a first episode of major depression. , 2002, The American journal of psychiatry.

[36]  Eric Vermetten,et al.  Childhood trauma associated with smaller hippocampal volume in women with major depression. , 2002, The American journal of psychiatry.

[37]  Marcus E Raichle,et al.  Volumetric reduction in left subgenual prefrontal cortex in early onset depression , 2002, Biological Psychiatry.

[38]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[39]  P. Maruff,et al.  Paracingulate morphologic differences in males with established schizophrenia: a magnetic resonance imaging morphometric study , 2002, Biological Psychiatry.

[40]  David R Rosenberg,et al.  Increased amygdala: hippocampal volume ratios associated with severity of anxiety in pediatric major depression. , 2003, Journal of child and adolescent psychopharmacology.

[41]  Garrett Fitzmaurice,et al.  Childhood and adolescent predictors of major depression in the transition to adulthood. , 2003, The American journal of psychiatry.

[42]  Hok Pan Yuen,et al.  Psychosis prediction: 12-month follow up of a high-risk (“prodromal”) group , 2003, Schizophrenia Research.

[43]  W. Drevets.  Neuroimaging Abnormalities in the Amygdala in Mood Disorders , 2003, Annals of the New York Academy of Sciences.

[44]  K. Luan Phan,et al.  Valence, gender, and lateralization of functional brain anatomy in emotion: a meta-analysis of findings from neuroimaging , 2003, NeuroImage.

[45]  Dennis Velakoulis,et al.  Morphology of the anterior cingulate cortex in young men at ultra-high risk of developing a psychotic illness. , 2003, The British journal of psychiatry : the journal of mental science.

[46]  Arthur W Toga,et al.  Anterior cingulate, gyrus rectus, and orbitofrontal abnormalities in elderly depressed patients: an MRI-based parcellation of the prefrontal cortex. , 2004, The American journal of psychiatry.

[47]  M. Sanders,et al.  The Development and Dissemination of the Triple P—Positive Parenting Program: A Multilevel, Evidence-Based System of Parenting and Family Support , 2002, Prevention Science.

[48]  V. Kusumakar,et al.  Hippocampal volume in early onset depression , 2004, BMC medicine.

[49]  Victoria Arango,et al.  Volumetric Analysis of the Prefrontal Cortex, Amygdala, and Hippocampus in Major Depression , 2004, Neuropsychopharmacology.

[50]  Hans-Jürgen Möller,et al.  Hippocampal and amygdala changes in patients with major depressive disorder and healthy controls during a 1-year follow-up. , 2004, The Journal of clinical psychiatry.

[51]  K. Lesch,et al.  CRSN Symposium : Focus on Depression , Part I Symposium du CRSN : le point sur la dépression , première partie Gene – environment interaction and the genetics of depression , 2004 .

[52]  Thomas F. Nugent,et al.  Dynamic mapping of human cortical development during childhood through early adulthood. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[53]  Jessica Turner,et al.  Sex-related hemispheric lateralization of amygdala function in emotionally influenced memory: an FMRI investigation. , 2004, Learning & memory.

[54]  Michael Marriott,et al.  Lower hippocampal volume in patients suffering from depression: a meta-analysis. , 2004, The American journal of psychiatry.

[55]  D. Pizzagalli,et al.  Functional but not structural subgenual prefrontal cortex abnormalities in melancholia , 2004 .

[56]  Robert Barber,et al.  Hippocampal volume change in depression: Late- and early-onset illness compared , 2004, British Journal of Psychiatry.

[57]  Michael F Egan,et al.  A susceptibility gene for affective disorders and the response of the human amygdala. , 2005, Archives of general psychiatry.

[58]  C. Zahn-Waxler,et al.  Parental socialization of emotion expression: gender differences and relations to child adjustment. , 2005, Emotion.

[59]  Giovanni B. Cassano,et al.  The mood spectrum: improving the diagnosis of bipolar disorder. , 2005 .

[60]  B. Ellis,et al.  Printed in the United States of America DOI: 10.10170S0954579405050145 , 2022 .

[61]  H. Kim,et al.  Childhood Temperament and Family Environment as Predictors of Internalizing and Externalizing Trajectories From Ages 5 to 17 , 2005, Journal of abnormal child psychology.

[62]  Avshalom Caspi,et al.  Nature × nurture: Genetic vulnerabilities interact with physical maltreatment to promote conduct problems , 2005, Development and Psychopathology.

[63]  L. Lengua,et al.  Bidirectional Associations between Temperament and Parenting and the Prediction of Adjustment Problems in Middle Childhood. , 2005 .

[64]  Deborah A. Yurgelun-Todd,et al.  Amygdala and hippocampus volumes in pediatric major depression , 2005, Biological Psychiatry.

[65]  Avshalom Caspi,et al.  Gene–environment interactions in psychiatry: joining forces with neuroscience , 2006, Nature Reviews Neuroscience.

[66]  Patricia Desmond,et al.  Hippocampal and amygdala volumes according to psychosis stage and diagnosis: a magnetic resonance imaging study of chronic schizophrenia, first-episode psychosis, and ultra-high-risk individuals. , 2006, Archives of general psychiatry.

[67]  Jair C. Soares,et al.  Smaller Cingulate Volumes in Unipolar Depressed Patients , 2006, Biological Psychiatry.

[68]  Dennis Velakoulis,et al.  The influence of sulcal variability on morphometry of the human anterior cingulate and paracingulate cortex , 2006, NeuroImage.

[69]  Jay Belsky,et al.  For Better and For Worse , 2007 .

[70]  R. Olvera,et al.  Medial temporal lobe abnormalities in pediatric unipolar depression , 2007, Neuroscience Letters.

[71]  John Suckling,et al.  Brain Imaging Correlates of Depressive Symptom Severity and Predictors of Symptom Improvement After Antidepressant Treatment , 2007, Biological Psychiatry.

[72]  Dick J. Veltman,et al.  Intrapair Differences in Hippocampal Volume in Monozygotic Twins Discordant for the Risk for Anxiety and Depression , 2007, Biological Psychiatry.

[73]  Paul M. Thompson,et al.  Sexual dimorphism of brain developmental trajectories during childhood and adolescence , 2007, NeuroImage.

[74]  M. Yücel,et al.  Neuroanatomical correlates of temperament in early adolescents. , 2008, Journal of the American Academy of Child and Adolescent Psychiatry.

[75]  N. Allen,et al.  Maternal socialization of positive affect: the impact of invalidation on adolescent emotion regulation and depressive symptomatology. , 2008, Child development.

[76]  Dennis Velakoulis,et al.  Variability of the paracingulate sulcus and morphometry of the medial frontal cortex: Associations with cortical thickness, surface area, volume, and sulcal depth , 2008, Human brain mapping.

[77]  S. Kennedy,et al.  Volumetric neuroimaging investigations in mood disorders: bipolar disorder versus major depressive disorder. , 2008, Bipolar disorders.

[78]  M. Yücel,et al.  Prefrontal and amygdala volumes are related to adolescents' affective behaviors during parent–adolescent interactions , 2008, Proceedings of the National Academy of Sciences.

[79]  Philip R. Szeszko,et al.  Amygdala and Hippocampal Volumes in Familial Early Onset Major Depressive Disorder , 2008, Biological Psychiatry.

[80]  J. Asarnow,et al.  Adolescent Emotional Development and the Emergence of Depressive Disorders: Adolescent mood disorders and familial processes , 2008 .

[81]  Mary G. Burke.  Adolescent Emotional Development and the Emergence of Depressive Disorders , 2009 .