Like mother like daughter: putamen activation as a mechanism underlying intergenerational risk for depression

Abstract Having a depressed mother is one of the strongest predictors for developing depression in adolescence. Given the role of aberrant reward processing in the onset and maintenance of depression, we examined the association between mothers’ and their daughters’ neural response to the anticipation of reward and loss. Fifteen non-depressed mothers with a history of recurrent depression and their never-disordered daughters, and 23 mothers without past or current depression and their never-disordered daughters, underwent functional magnetic resonance imaging while performing the monetary incentive delay task. To assess mother-daughter concordance, we first identified ROIs involved in the anticipation of reward and loss across all mother-daughter pairs. Within each of these ROIs, we examined the association between mothers’ and daughters’ neural response, and the interaction between group status and mothers’ neural response in predicting daughters’ neural response. We found a significant association between mothers’ and daughters’ putamen response to the anticipation of loss, regardless of mother’s depression history. Furthermore, pubertal stage moderated the association between mother-daughter putamen concordance. Our findings suggest a unique role of the putamen in the maternal transmission of reward learning and have important implications for understanding disorders characterized by disturbances in reward learning and processing, such as major depression.

[1]  L. Wilbrecht,et al.  Risky decision-making in adolescent girls: The role of pubertal hormones and reward circuitry , 2016, Psychoneuroendocrinology.

[2]  Stephan J Sanders,et al.  Intergenerational Neuroimaging of Human Brain Circuitry , 2016, Trends in Neurosciences.

[3]  R. Kotov,et al.  Blunted Neural Response to Rewards as a Prospective Predictor of the Development of Depression in Adolescent Girls. , 2016, The American journal of psychiatry.

[4]  Katherine R. Luking,et al.  Reward Processing and Risk for Depression Across Development , 2016, Trends in Cognitive Sciences.

[5]  I. Gotlib,et al.  Concordant Patterns of Brain Structure in Mothers with Recurrent Depression and Their Never-Depressed Daughters , 2016, Developmental Neuroscience.

[6]  A. Reiss,et al.  Female-Specific Intergenerational Transmission Patterns of the Human Corticolimbic Circuitry , 2016, The Journal of Neuroscience.

[7]  T. Robbins Illuminating anhedonia , 2016, Science.

[8]  A. Hariri,et al.  Blunted Ventral Striatum Development in Adolescence Reflects Emotional Neglect and Predicts Depressive Symptoms , 2015, Biological Psychiatry.

[9]  H. Flor,et al.  Altered neural reward and loss processing and prediction error signalling in depression. , 2015, Social cognitive and affective neuroscience.

[10]  Taiki Takahashi,et al.  Reinforcement learning in depression: A review of computational research , 2015, Neuroscience & Biobehavioral Reviews.

[11]  A. V. van Duijvenvoorde,et al.  Longitudinal Changes in Adolescent Risk-Taking: A Comprehensive Study of Neural Responses to Rewards, Pubertal Development, and Risk-Taking Behavior , 2015, The Journal of Neuroscience.

[12]  Natalie L. Colich,et al.  HPA-axis reactivity interacts with stage of pubertal development to predict the onset of depression , 2015, Psychoneuroendocrinology.

[13]  I. Gotlib,et al.  Concordance of mother–daughter diurnal cortisol production: Understanding the intergenerational transmission of risk for depression , 2015, Biological Psychology.

[14]  Y. Nikolova,et al.  Stress-related anhedonia is associated with ventral striatum reactivity to reward and transdiagnostic psychiatric symptomatology , 2015, Psychological Medicine.

[15]  Sabine Peters,et al.  The link between testosterone and amygdala–orbitofrontal cortex connectivity in adolescent alcohol use , 2015, Psychoneuroendocrinology.

[16]  Thomas E. Nichols,et al.  Common genetic variants influence human subcortical brain structures , 2015, Nature.

[17]  M. Treadway,et al.  Reward processing dysfunction in major depression, bipolar disorder and schizophrenia , 2015, Current opinion in psychiatry.

[18]  E. Bora Neurodevelopmental origin of cognitive impairment in schizophrenia , 2014, Psychological Medicine.

[19]  Heather T. Pane,et al.  Major depression in mothers predicts reduced ventral striatum activation in adolescent female offspring with and without depression. , 2014, Journal of abnormal psychology.

[20]  D. Pizzagalli,et al.  Depression, stress, and anhedonia: toward a synthesis and integrated model. , 2014, Annual review of clinical psychology.

[21]  J. Flint,et al.  The Genetics of Major Depression , 2014, Neuron.

[22]  R. Dahl,et al.  Reduced reward anticipation in youth at high-risk for unipolar depression: A preliminary study , 2013, Developmental Cognitive Neuroscience.

[23]  Eva H. Telzer,et al.  Reduced nucleus accumbens reactivity and adolescent depression following early-life stress , 2013, Neuroscience.

[24]  P. Dayan,et al.  Mapping anhedonia onto reinforcement learning: a behavioural meta-analysis , 2013, Biology of Mood & Anxiety Disorders.

[25]  N. Ryan,et al.  Neural response to reward as a predictor of increases in depressive symptoms in adolescence , 2013, Neurobiology of Disease.

[26]  F. Turkheimer,et al.  Nature or Nurture? Determining the Heritability of Human Striatal Dopamine Function: an [18F]-DOPA PET Study , 2013, Neuropsychopharmacology.

[27]  W. K. Simmons,et al.  A “Taste” of What is to Come: Reward Sensitivity as a Potential Endophenotype for Major Depressive Disorder , 2012, Biological Psychiatry.

[28]  E. Palazidou The neurobiology of depression. , 2012, British medical bulletin.

[29]  Bregtje Gunther Moor,et al.  Developmental Cognitive Neuroscience Testosterone Levels Correspond with Increased Ventral Striatum Activation in Response to Monetary Rewards in Adolescents , 2022 .

[30]  I. Gotlib,et al.  Handbook of Depression , 2011 .

[31]  J. Roiser,et al.  Reward and Punishment Processing in Depression , 2010, Biological Psychiatry.

[32]  I. Gotlib,et al.  Emotion identification in girls at high risk for depression. , 2010, Journal of child psychology and psychiatry, and allied disciplines.

[33]  J. P. Hamilton,et al.  Neural processing of reward and loss in girls at risk for major depression. , 2010, Archives of general psychiatry.

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

[35]  Leah H. Somerville,et al.  A time of change: Behavioral and neural correlates of adolescent sensitivity to appetitive and aversive environmental cues , 2010, Brain and Cognition.

[36]  M. Phillips,et al.  Healthy adolescents' neural response to reward: associations with puberty, positive affect, and depressive symptoms. , 2010, Journal of the American Academy of Child and Adolescent Psychiatry.

[37]  Jeffrey L. Birk,et al.  Reduced caudate and nucleus accumbens response to rewards in unmedicated individuals with major depressive disorder. , 2009, The American journal of psychiatry.

[38]  D. Klein,et al.  Emotional reactivity in depression: diminished responsiveness to anticipated reward but not to anticipated punishment or to nonreward or avoidance , 2009, Depression and anxiety.

[39]  Mark W. Woolrich,et al.  Robust group analysis using outlier inference , 2008, NeuroImage.

[40]  Brian Knutson,et al.  Neural Responses to Monetary Incentives in Major Depression , 2008, Biological Psychiatry.

[41]  A. Meyer-Lindenberg,et al.  Heritability of Brain Morphology Related to Schizophrenia: A Large-Scale Automated Magnetic Resonance Imaging Segmentation Study , 2008, Biological Psychiatry.

[42]  K. Lambert Handbook of Emotion Regulation , 2007 .

[43]  B. Balleine,et al.  The Role of the Dorsal Striatum in Reward and Decision-Making , 2007, The Journal of Neuroscience.

[44]  Lisa Talbot,et al.  Biased processing of emotional information in girls at risk for depression. , 2007, Journal of abnormal psychology.

[45]  Mitsuo Kawato,et al.  Heterarchical reinforcement-learning model for integration of multiple cortico-striatal loops: fMRI examination in stimulus-action-reward association learning , 2006, Neural Networks.

[46]  E. Nestler,et al.  The Mesolimbic Dopamine Reward Circuit in Depression , 2006, Biological Psychiatry.

[47]  M. Kawato,et al.  Different neural correlates of reward expectation and reward expectation error in the putamen and caudate nucleus during stimulus-action-reward association learning. , 2006, Journal of neurophysiology.

[48]  Karl J. Friston,et al.  Dissociable Roles of Ventral and Dorsal Striatum in Instrumental Conditioning , 2004, Science.

[49]  Mark W. Woolrich,et al.  Multilevel linear modelling for FMRI group analysis using Bayesian inference , 2004, NeuroImage.

[50]  Stephen M. Smith,et al.  General multilevel linear modeling for group analysis in FMRI , 2003, NeuroImage.

[51]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[52]  Stephen M. Smith,et al.  Temporal Autocorrelation in Univariate Linear Modeling of FMRI Data , 2001, NeuroImage.

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

[54]  Brian Knutson,et al.  FMRI Visualization of Brain Activity during a Monetary Incentive Delay Task , 2000, NeuroImage.

[55]  E J Costello,et al.  Puberty and depression: the roles of age, pubertal status and pubertal timing , 1998, Psychological Medicine.

[56]  N. Ryan,et al.  Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): initial reliability and validity data. , 1997, Journal of the American Academy of Child and Adolescent Psychiatry.

[57]  M. Hofer Hidden regulators in attachment, separation, and loss. , 1994, Monographs of the Society for Research in Child Development.

[58]  M. Taylor,et al.  The Genetics of Mood Disorders. , 1991, The American journal of psychiatry.

[59]  S. Faraone,et al.  The genetics of mood disorders , 1990 .

[60]  J M Tanner,et al.  Variations in pattern of pubertal changes in girls. , 1969, Archives of disease in childhood.

[61]  R. Mccall,et al.  The Genetic and Environmental Origins of Learning Abilities and Disabilities in the Early School , 2007, Monographs of the Society for Research in Child Development.

[62]  M. Toth Mechanisms of Non-Genetic Inheritance and Psychiatric Disorders , 2015, Neuropsychopharmacology.

[63]  R. Kotov,et al.  Blunted neural response to rewards prospectively predicts depression in adolescent girls. , 2013, Psychophysiology.

[64]  Serge A R B Rombouts,et al.  What motivates the adolescent? Brain regions mediating reward sensitivity across adolescence. , 2010, Cerebral cortex.

[65]  Jeffrey L. Birk,et al.  Reduced Caudate and Nucleus Accumbens Response to Rewards in Unmedicated Subjects with Major Depressive Disorder , 2009 .

[66]  I. Gotlib,et al.  Interpretation of Ambiguous Information in Girls at Risk for Depression , 2009, Journal of abnormal child psychology.

[67]  Peter J Cooper,et al.  Maternal depression and psychiatric outcomes in adolescent offspring: a 13-year longitudinal study. , 2007, Journal of affective disorders.

[68]  S. Calkins,et al.  Caregiver Influences on Emerging Emotion Regulation: Biological and Environmental Transactions in Early Development. , 2007 .

[69]  S. Calkins,et al.  Caregiver influences on emerging emotion regulation , 2007 .

[70]  James J. Gross,et al.  Handbook of emotion regulation , 2007 .

[71]  M. Kawato,et al.  Association Learning Caudate Nucleus During Stimulus-Action-Reward and Reward Expectation Error in the Putamen and Different Neural Correlates of Reward Expectation , 2006 .

[72]  B. Knowlton,et al.  Learning and memory functions of the Basal Ganglia. , 2002, Annual review of neuroscience.

[73]  I. Gotlib,et al.  Children of parents with depression. , 1999 .

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