Hippocampal Volume as an Amplifier of the Effect of Social Context on Adolescent Depression

Recent models have focused on how brain-based individual differences in social sensitivity shape affective development in adolescence, when rates of depression escalate. Given the importance of the hippocampus in binding contextual and affective elements of experience, as well as its putative role in depression, we examined hippocampal volume as a moderator of the effects of social context on depressive symptoms in a sample of 209 Mexican-origin adolescents. Adolescents with larger versus smaller hippocampal volumes showed heightened sensitivity in their depressive symptoms to a protective factor inside the home (sense of family connectedness) and a risk factor outside the home (community crime exposure). These interactive effects uniquely predicted depressive symptoms and were greater for the left side, suggesting two independent social-contextual contributions to depression that were moderated by left hippocampal volume. Results elucidate complex brain-environment interplay in adolescent depression, offering clues about for whom and how social context plays a role.

[1]  K. Crowder,et al.  Exiting and Entering High-Poverty Neighborhoods: Latinos, Blacks and Anglos Compared , 2005 .

[2]  M. Yücel,et al.  Structural brain abnormalities in major depressive disorder: a selective review of recent MRI studies. , 2009, Journal of affective disorders.

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

[4]  Bernard Mazoyer,et al.  Meta-analyzing left hemisphere language areas: Phonology, semantics, and sentence processing , 2006, NeuroImage.

[5]  E. Nelson,et al.  The development of the ventral prefrontal cortex and social flexibility , 2011, Developmental Cognitive Neuroscience.

[6]  E. Rolls The hippocampus and memory , 1997 .

[7]  H. Kraemer,et al.  How do risk factors work together? Mediators, moderators, and independent, overlapping, and proxy risk factors. , 2001, The American journal of psychiatry.

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

[9]  R. Passingham The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

[10]  C. Hammen,et al.  Differential Exposure and Reactivity to Interpersonal Stress Predict Sex Differences in Adolescent Depression , 2006, Journal of clinical child and adolescent psychology : the official journal for the Society of Clinical Child and Adolescent Psychology, American Psychological Association, Division 53.

[11]  S. Shankman,et al.  Subthreshold depressive disorder in adolescents: predictors of escalation to full-syndrome depressive disorders. , 2009, Journal of the American Academy of Child and Adolescent Psychiatry.

[12]  Jens C. Pruessner,et al.  Self-esteem, locus of control, hippocampal volume, and cortisol regulation in young and old adulthood , 2005, NeuroImage.

[13]  M. Yücel,et al.  Mapping subcortical brain maturation during adolescence: evidence of hemisphere- and sex-specific longitudinal changes. , 2013, Developmental science.

[14]  S. Emans,et al.  Exposure to Violence and Victimization and Depression, Hopelessness, and Purpose in Life Among Adolescents Living in and Around Public Housing , 1995, Journal of developmental and behavioral pediatrics : JDBP.

[15]  Richard S. J. Frackowiak,et al.  Navigation-related structural change in the hippocampi of taxi drivers. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[16]  Sandra M. Neer,et al.  The Screen for Child Anxiety Related Emotional Disorders (SCARED): scale construction and psychometric characteristics. , 1997, Journal of the American Academy of Child and Adolescent Psychiatry.

[17]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[18]  M. Yücel,et al.  Hippocampal volume and sensitivity to maternal aggressive behavior: A prospective study of adolescent depressive symptoms , 2011, Development and Psychopathology.

[19]  S. Nolen-Hoeksema,et al.  The emergence of gender differences in depression during adolescence. , 1994, Psychological bulletin.

[20]  L. Squire Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. , 1992, Psychological review.

[21]  Laura M. Gonzalez,et al.  The Protective Role of Familism in the Lives of Latino Adolescents , 2015 .

[22]  Jennifer I. Lissemore,et al.  A longitudinal study of stress‐induced hippocampal volume changes in mice that are susceptible or resilient to chronic social defeat , 2014, Hippocampus.

[23]  J. Eliassen,et al.  Serotonin transporter gene moderates associations between mood, memory and hippocampal volume , 2013, Behavioural Brain Research.

[24]  U. Bronfenbrenner Ecology of the family as a context for human development: research perspectives , 1986 .

[25]  T. Yuan,et al.  Hippocampal Asymmetry: Differences in Structures and Functions , 2013, Neurochemical Research.

[26]  L. Fogg,et al.  Depression and Suicidal Ideation Among Mexican American School-Aged Children , 2005, Research and Theory for Nursing Practice.

[27]  M M Weissman,et al.  Depressed adolescents grown up. , 1999, JAMA.

[28]  L. Jancke,et al.  Identifying with fictive characters: structural brain correlates of the personality trait 'fantasy'. , 2014, Social cognitive and affective neuroscience.

[29]  R. Friedrich In Defense of Multiplicative Terms In Multiple Regression Equations , 1982 .

[30]  N. Vasic,et al.  Revisiting default mode network function in major depression: evidence for disrupted subsystem connectivity , 2013, Psychological Medicine.

[31]  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.

[32]  R. Dodhia A Review of Applied Multiple Regression/Correlation Analysis for the Behavioral Sciences (3rd ed.) , 2005 .

[33]  P. Blier,et al.  A Prospective, Longitudinal Study of the Effect of Remission on Cortical Thickness and Hippocampal Volume in Patients with Treatment-Resistant Depression , 2015, The international journal of neuropsychopharmacology.

[34]  Demis Hassabis,et al.  The construction system of the brain , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[35]  R. Nathan Spreng,et al.  The Common Neural Basis of Autobiographical Memory, Prospection, Navigation, Theory of Mind, and the Default Mode: A Quantitative Meta-analysis , 2009, Journal of Cognitive Neuroscience.

[36]  C. Petten Relationship between hippocampal volume and memory ability in healthy individuals across the lifespan: review and meta-analysis , 2004, Neuropsychologia.

[37]  J. Krebs,et al.  Memory for spatial and object-specific cues in food-storing and non-storing birds , 1994, Journal of Comparative Physiology A.

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

[39]  R A McCormick,et al.  Testing a tripartite model: I. Evaluating the convergent and discriminant validity of anxiety and depression symptom scales. , 1995, Journal of abnormal psychology.

[40]  E. Nelson,et al.  Social re-orientation and brain development: An expanded and updated view , 2015, Developmental Cognitive Neuroscience.

[41]  N. Adler,et al.  Biological sensitivity to context: the interactive effects of stress reactivity and family adversity on socioemotional behavior and school readiness. , 2010, Child development.

[42]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[43]  B. Milner,et al.  The role of the left hippocampal region in the acquisition and retention of story content , 1990, Neuropsychologia.

[44]  C. Hammen,et al.  Age and gender as determinants of stress exposure, generation, and reactions in youngsters: a transactional perspective. , 1999, Child development.

[45]  E. Maguire,et al.  The Human Hippocampus and Spatial and Episodic Memory , 2002, Neuron.

[46]  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.

[47]  Christian F. Doeller,et al.  Lateralized human hippocampal activity predicts navigation based on sequence or place memory , 2010, Proceedings of the National Academy of Sciences.

[48]  Anders M. Dale,et al.  Cortical volume and speed-of-processing are complementary in prediction of performance intelligence , 2005, Neuropsychologia.

[49]  D. Shaffer,et al.  NIMH Diagnostic Interview Schedule for Children Version IV (NIMH DISC-IV): description, differences from previous versions, and reliability of some common diagnoses. , 2000, Journal of the American Academy of Child and Adolescent Psychiatry.

[50]  E. Walker,et al.  Diagnostic and Statistical Manual of Mental Disorders , 2013 .

[51]  S. Dickerson,et al.  Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. , 2004, Psychological bulletin.

[52]  Ylva Østby,et al.  Dissociating memory processes in the developing brain: the role of hippocampal volume and cortical thickness in recall after minutes versus days. , 2012, Cerebral cortex.

[53]  Jay Belsky,et al.  Differential susceptibility to the environment: An evolutionary–neurodevelopmental theory , 2011, Development and Psychopathology.

[54]  M. Thase,et al.  Neural substrates of trait ruminations in depression. , 2014, Journal of abnormal psychology.

[55]  Larry A. Tupler,et al.  Segmented Hippocampal Volume in Children and Adolescents with Posttraumatic Stress Disorder , 2006, Biological Psychiatry.

[56]  Stella W. Y. Chan,et al.  Hippocampal volume in vulnerability and resilience to depression. , 2016, Journal of affective disorders.

[57]  J. Price,et al.  Neurocircuitry of Mood Disorders , 2010, Neuropsychopharmacology.

[58]  E. Crone,et al.  Understanding adolescence as a period of social–affective engagement and goal flexibility , 2012, Nature Reviews Neuroscience.

[59]  Robin I. M. Dunbar,et al.  The social brain hypothesis and its implications for social evolution , 2009, Annals of human biology.

[60]  M. Greicius,et al.  Resting-state functional connectivity reflects structural connectivity in the default mode network. , 2009, Cerebral cortex.

[61]  S. Nolen-Hoeksema,et al.  Age, gender, race, socioeconomic status, and birth cohort differences on the children's depression inventory: a meta-analysis. , 2002, Journal of abnormal psychology.

[62]  Nicholas B. Allen,et al.  The emergence of depression in adolescence: Development of the prefrontal cortex and the representation of reward , 2008, Neuroscience & Biobehavioral Reviews.

[63]  M. Fava,et al.  Effect of age at onset on the course of major depressive disorder. , 2007, The American journal of psychiatry.

[64]  L. Staib,et al.  Hippocampal volume reduction in major depression. , 2000, The American journal of psychiatry.

[65]  Adriana Galvan,et al.  The adolescent brain. , 2008, Developmental review : DR.

[66]  D. Fergusson,et al.  Adolescent depression, adult mental health and psychosocial outcomes at 30 and 35 years , 2016, Psychological Medicine.

[67]  Brian Avants,et al.  Medial temporal structures and memory functions in adolescents with heavy cannabis use. , 2011, Journal of psychiatric research.

[68]  Kiralee M. Hayashi,et al.  Dynamic mapping of normal human hippocampal development , 2006, Hippocampus.

[69]  J. Glowinski,et al.  Hippocampo‐prefrontal cortex pathway: Anatomical and electrophysiological characteristics , 2000, Hippocampus.

[70]  Andreas Papassotiropoulos,et al.  Dynamic Modulation of Amygdala–Hippocampal Connectivity by Emotional Arousal , 2014, The Journal of Neuroscience.

[71]  S. Guerra,et al.  Asthma genetics: from linear to multifactorial approaches. , 2008, Annual review of medicine.

[72]  M. Yücel,et al.  Linking the serotonin transporter gene, family environments, hippocampal volume and depression onset: A prospective imaging gene × environment analysis. , 2015, Journal of abnormal psychology.

[73]  E. Maguire,et al.  Patterns of hippocampal‐cortical interaction dissociate temporal lobe memory subsystems , 2000, Hippocampus.

[74]  A. Guyer,et al.  Adolescent neurobiological susceptibility to social context , 2015, Developmental Cognitive Neuroscience.

[75]  A. Senthilselvan,et al.  Social, demographic, and health outcomes in the 10 years following adolescent depression. , 2013, The Journal of adolescent health : official publication of the Society for Adolescent Medicine.

[76]  T. Paus,et al.  Why do many psychiatric disorders emerge during adolescence? , 2008, Nature Reviews Neuroscience.

[77]  C. Aneshensel,et al.  The neighborhood context of adolescent mental health. , 1996, Journal of health and social behavior.

[78]  M. Yücel,et al.  Interaction of parenting experiences and brain structure in the prediction of depressive symptoms in adolescents. , 2008, Archives of general psychiatry.

[79]  G. MacQueen,et al.  A meta-analysis examining clinical predictors of hippocampal volume in patients with major depressive disorder. , 2009, Journal of psychiatry & neuroscience : JPN.

[80]  Ricardo Villarreal,et al.  Factorial Invariance of a Pan-Hispanic Familism Scale , 2005 .

[81]  B. McEwen,et al.  The neuroendocrinology of stress and aging: the glucocorticoid cascade hypothesis. , 1986, Endocrine reviews.

[82]  M. Lei,et al.  Enhanced Susceptibility to Context: A Promising Perspective on the Interplay of Genes and the Social Environment , 2013 .

[83]  N. Allen,et al.  Association between serotonin transporter genotype, brain structure and adolescent-onset major depressive disorder: a longitudinal prospective study , 2014, Translational Psychiatry.

[84]  M. Kovacs The Children's Depression, Inventory (CDI). , 1985, Psychopharmacology bulletin.

[85]  M. Yücel,et al.  Childhood maltreatment and psychopathology affect brain development during adolescence. , 2013, Journal of the American Academy of Child and Adolescent Psychiatry.

[86]  J. Csernansky,et al.  Hippocampal atrophy in recurrent major depression. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[87]  Alfonso Barrós-Loscertales,et al.  Behavioral Inhibition System activity is associated with increased amygdala and hippocampal gray matter volume: A voxel-based morphometry study , 2006, NeuroImage.

[88]  Martin Styner,et al.  A comparison of automated segmentation and manual tracing for quantifying hippocampal and amygdala volumes , 2009, NeuroImage.

[89]  D. Barch,et al.  Preschool is a sensitive period for the influence of maternal support on the trajectory of hippocampal development , 2016, Proceedings of the National Academy of Sciences.

[90]  Carl A Latkin,et al.  Stressful neighborhoods and depression: a prospective study of the impact of neighborhood disorder. , 2003, Journal of health and social behavior.

[91]  Aaron Curry,et al.  Pathways to depression: the impact of neighborhood violent crime on inner-city residents in Baltimore, Maryland, USA. , 2008, Social science & medicine.

[92]  E. Perez-stable,et al.  Hispanic Familism and Acculturation: What Changes and What Doesn't? , 1987 .

[93]  J. P. Hamilton,et al.  Decreased hippocampal volume in healthy girls at risk of depression. , 2010, Archives of general psychiatry.

[94]  B. Ravnkilde,et al.  Hippocampal volume and depression: a meta-analysis of MRI studies. , 2004, The American journal of psychiatry.

[95]  Rosalie A. Torres Stone,et al.  Acculturative stress, social support, and coping: relations to psychological adjustment among Mexican American college students. , 2007, Cultural diversity & ethnic minority psychology.

[96]  H Meltzer,et al.  The Strengths and Difficulties Questionnaire: a pilot study on the validity of the self-report version , 2003, International review of psychiatry.

[97]  Jodie B. Ullman,et al.  Familism and psychological health: the intervening role of closeness and social support. , 2014, Cultural diversity & ethnic minority psychology.

[98]  E. Crone,et al.  Hippocampal volume and internalizing behavior problems in adolescence , 2013, European Neuropsychopharmacology.

[99]  J. Giedd,et al.  Brain development in children and adolescents: Insights from anatomical magnetic resonance imaging , 2006, Neuroscience & Biobehavioral Reviews.

[100]  W. Boyce Differential Susceptibility of the Developing Brain to Contextual Adversity and Stress , 2016, Neuropsychopharmacology.

[101]  E. Leibenluft,et al.  Distinct neural signatures of threat learning in adolescents and adults , 2011, Proceedings of the National Academy of Sciences.

[102]  Abraham Z. Snyder,et al.  A unified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: reliability and validation against manual measurement of total intracranial volume , 2004, NeuroImage.

[103]  Stephen Maren,et al.  Hippocampal involvement in contextual modulation of fear extinction , 2007, Hippocampus.

[104]  C. Cutrona,et al.  Neighborhood Characteristics and Depression , 2006, Current directions in psychological science.

[105]  Hong-wei Dong,et al.  Are the Dorsal and Ventral Hippocampus Functionally Distinct Structures? , 2010, Neuron.

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

[107]  A. Fuligni,et al.  Dimensions of family connectedness among adolescents with Mexican, Chinese, and European backgrounds. , 2006, Developmental psychology.

[108]  S. Tonegawa,et al.  Bidirectional switch of the valence associated with a hippocampal contextual memory engram , 2014, Nature.