Mismatch or allostatic load? Timing of life adversity differentially shapes gray matter volume and anxious temperament

Traditionally, adversity was defined as the accumulation of environmental events (allostatic load). Recently however, a mismatch between the early and the later (adult) environment (mismatch) has been hypothesized to be critical for disease development, a hypothesis that has not yet been tested explicitly in humans. We explored the impact of timing of life adversity (childhood and past year) on anxiety and depression levels (N = 833) and brain morphology (N = 129). Both remote (childhood) and proximal (recent) adversities were differentially mirrored in morphometric changes in areas critically involved in emotional processing (i.e. amygdala/hippocampus, dorsal anterior cingulate cortex, respectively). The effect of adversity on affect acted in an additive way with no evidence for interactions (mismatch). Structural equation modeling demonstrated a direct effect of adversity on morphometric estimates and anxiety/depression without evidence of brain morphology functioning as a mediator. Our results highlight that adversity manifests as pronounced changes in brain morphometric and affective temperament even though these seem to represent distinct mechanistic pathways. A major goal of future studies should be to define critical time periods for the impact of adversity and strategies for intervening to prevent or reverse the effects of adverse childhood life experiences.

[1]  V. Arolt,et al.  Differing brain structural correlates of familial and environmental risk for major depressive disorder revealed by a combined VBM/pattern recognition approach , 2015, Psychological Medicine.

[2]  Rebecca S. Schreiber,et al.  Benefits of adversity?! How life history affects the behavioral profile of mice varying in serotonin transporter genotype , 2015, Front. Behav. Neurosci..

[3]  Melissa T. Merrick,et al.  Childhood adversity and adult chronic disease: an update from ten states and the District of Columbia, 2010. , 2015, American journal of preventive medicine.

[4]  Spenser R Radtke,et al.  Reduced hippocampal and medial prefrontal gray matter mediate the association between reported childhood maltreatment and trait anxiety in adulthood and predict sensitivity to future life stress , 2014, Biology of Mood & Anxiety Disorders.

[5]  D. Hermans,et al.  A review on human reinstatement studies: an overview and methodological challenges , 2014, Learning & memory.

[6]  J. Raduà,et al.  Gray matter abnormalities in childhood maltreatment: a voxel-wise meta-analysis. , 2014, The American journal of psychiatry.

[7]  V. Arolt,et al.  Hippocampal Atrophy in Major Depression: a Function of Childhood Maltreatment Rather than Diagnosis? , 2014, Neuropsychopharmacology.

[8]  Jakob Hartmann,et al.  Evidence supporting the match/mismatch hypothesis of psychiatric disorders , 2014, European Neuropsychopharmacology.

[9]  T. Insel The NIMH Research Domain Criteria (RDoC) Project: precision medicine for psychiatry. , 2014, The American journal of psychiatry.

[10]  M. Craske,et al.  Fear extinction and relapse: state of the art. , 2013, Annual review of clinical psychology.

[11]  Theo Vos,et al.  The Long-Term Health Consequences of Child Physical Abuse, Emotional Abuse, and Neglect: A Systematic Review and Meta-Analysis , 2012, PLoS medicine.

[12]  Mathias V. Schmidt,et al.  Mismatch or cumulative stress: Toward an integrated hypothesis of programming effects , 2012, Physiology & Behavior.

[13]  Rajita Sinha,et al.  Cumulative Adversity and Smaller Gray Matter Volume in Medial Prefrontal, Anterior Cingulate, and Insula Regions , 2012, Biological Psychiatry.

[14]  R. Davidson,et al.  Social influences on neuroplasticity: stress and interventions to promote well-being , 2012, Nature Neuroscience.

[15]  Walter Heindel,et al.  Limbic Scars: Long-Term Consequences of Childhood Maltreatment Revealed by Functional and Structural Magnetic Resonance Imaging , 2012, Biological Psychiatry.

[16]  Martin H. Teicher,et al.  Childhood maltreatment is associated with reduced volume in the hippocampal subfields CA3, dentate gyrus, and subiculum , 2012, Proceedings of the National Academy of Sciences.

[17]  Michael S. Gaffrey,et al.  Maternal support in early childhood predicts larger hippocampal volumes at school age , 2012, Proceedings of the National Academy of Sciences.

[18]  J. Homberg The stress-coping (mis)match hypothesis for nature×nurture interactions , 2012, Brain Research.

[19]  Udo Dannlowski,et al.  Facial emotion processing in major depression: a systematic review of neuroimaging findings , 2011, Biology of Mood & Anxiety Disorders.

[20]  M. Schmidt Animal models for depression and the mismatch hypothesis of disease , 2011, Psychoneuroendocrinology.

[21]  A. Mechelli,et al.  Effects of stressful life events on human brain structure: A longitudinal voxel-based morphometry study , 2011, Stress.

[22]  T. Egner,et al.  Emotional processing in anterior cingulate and medial prefrontal cortex , 2011, Trends in Cognitive Sciences.

[23]  Jun-ichiro Kawahara,et al.  Selective bias in retrospective self-reports of negative mood states , 2011, Anxiety, stress, and coping.

[24]  A. Aleman,et al.  Reduced Medial Prefrontal Cortex Volume in Adults Reporting Childhood Emotional Maltreatment , 2010, Biological Psychiatry.

[25]  T. Insel,et al.  Wesleyan University From the SelectedWorks of Charles A . Sanislow , Ph . D . 2010 Research Domain Criteria ( RDoC ) : Toward a New Classification Framework for Research on Mental Disorders , 2018 .

[26]  C. Spitzer,et al.  Die deutsche Version des Childhood Trauma Questionnaire (CTQ): Erste Befunde zu den psychometrischen Kennwerten , 2010 .

[27]  C. Hammen,et al.  Hippocampal Changes Associated with Early-Life Adversity and Vulnerability to Depression , 2010, Biological Psychiatry.

[28]  Margaret A. Sheridan,et al.  A Review of Adversity, The Amygdala and the Hippocampus: A Consideration of Developmental Timing , 2009, Front. Hum. Neurosci..

[29]  B. Quinn,et al.  Prolonged institutional rearing is associated with atypically large amygdala volume and difficulties in emotion regulation. , 2010, Developmental science.

[30]  P. Whalen,et al.  The Structural Integrity of an Amygdala–Prefrontal Pathway Predicts Trait Anxiety , 2009, The Journal of Neuroscience.

[31]  Gustavo Turecki,et al.  Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse , 2009, Nature Neuroscience.

[32]  K. McLaughlin,et al.  Mechanisms linking stressful life events and mental health problems in a prospective, community-based sample of adolescents. , 2009, The Journal of adolescent health : official publication of the Society for Adolescent Medicine.

[33]  D. Fergusson,et al.  Burden and consequences of child maltreatment in high-income countries , 2008, The Lancet.

[34]  F. Seguin,et al.  Effects of stress throughout the lifespan on the brain, behaviour and cognition , 2009 .

[35]  R. DeRubeis,et al.  Cognitive therapy vs. medications for depression: Treatment outcomes and neural mechanisms , 2009 .

[36]  R. DeRubeis,et al.  Cognitive therapy versus medication for depression: treatment outcomes and neural mechanisms , 2008, Nature Reviews Neuroscience.

[37]  Graeme D. Jackson,et al.  Selection of the control group for VBM analysis: Influence of covariates, matching and sample size , 2008, NeuroImage.

[38]  Gary H. Glover,et al.  Resilience after 9/11: Multimodal neuroimaging evidence for stress-related change in the healthy adult brain , 2008, NeuroImage.

[39]  Eric Vermetten,et al.  Structural and functional plasticity of the human brain in posttraumatic stress disorder. , 2008, Progress in brain research.

[40]  C. Conrad Chronic Stress-induced Hippocampal Vulnerability: The Glucocorticoid Vulnerability Hypothesis , 2008, Reviews in the neurosciences.

[41]  J. Bremner,et al.  Functional neuroimaging studies in posttraumatic stress disorder: review of current methods and findings , 2007, Depression and anxiety.

[42]  P. Gluckman,et al.  Early life events and their consequences for later disease: A life history and evolutionary perspective , 2007, American journal of human biology : the official journal of the Human Biology Council.

[43]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[44]  E. Gordon,et al.  Early Life Stress and Morphometry of the Adult Anterior Cingulate Cortex and Caudate Nuclei , 2006, Biological Psychiatry.

[45]  J. Gross,et al.  The cognitive control of emotion , 2005, Trends in Cognitive Sciences.

[46]  E. Paykel,et al.  Life events and affective disorders , 2003, Acta psychiatrica Scandinavica. Supplementum.

[47]  B. McEwen Mood disorders and allostatic load , 2003, Biological Psychiatry.

[48]  A. Caspi,et al.  Influence of Life Stress on Depression: Moderation by a Polymorphism in the 5-HTT Gene , 2003, Science.

[49]  M. Newcomb,et al.  Development and validation of a brief screening version of the Childhood Trauma Questionnaire. , 2003, Child abuse & neglect.

[50]  A. Caspi,et al.  Influence of Life Stress on Depression: Moderation by a Polymorphism in the 5-HTT Gene , 2003, Science.

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

[52]  Karl J. Friston,et al.  Distributional Assumptions in Voxel-Based Morphometry , 2002, NeuroImage.

[53]  Bremner Jd Neuroimaging of childhood trauma. , 2002 .

[54]  M. Wilcox,et al.  Maternal depression: a child's first adverse life event. , 2002, Seminars in clinical neuropsychiatry.

[55]  J. Bremner Neuroimaging of childhood trauma. , 2002, Seminars in clinical neuropsychiatry.

[56]  C. Nemeroff,et al.  The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies , 2001, Biological Psychiatry.

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

[58]  D. Sheehan,et al.  The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. , 1998, The Journal of clinical psychiatry.

[59]  R. Buchanan,et al.  The Effect of Clozapine on Plasma Norepinephrine: Relationship to Clinical Efficacy , 1994, Neuropsychopharmacology.

[60]  M. Browne,et al.  Alternative Ways of Assessing Model Fit , 1992 .

[61]  T. Brugha,et al.  The List of Threatening Experiences: the reliability and validity of a brief life events questionnaire , 1990, Acta psychiatrica Scandinavica.

[62]  K. Nuechterlein,et al.  A prospective study of stressful life events and schizophrenic relapse. , 1989, Journal of abnormal psychology.

[63]  T. Brugha,et al.  The List of Threatening Experiences: a subset of 12 life event categories with considerable long-term contextual threat , 1985, Psychological Medicine.

[64]  C. Spielberger,et al.  Manual for the state-trait anxiety inventory (form Y) : "self-evaluation questionnaire" , 1983 .

[65]  C. Spielberger,et al.  Manual for the State-Trait Anxiety Inventory , 1970 .