The brain’s response to reward anticipation and depression in adolescence: dimensionality, specificity and longitudinal predictions in a community-based sample

OBJECTIVE The authors examined whether alterations in the brain's reward network operate as a mechanism across the spectrum of risk for depression. They then tested whether these alterations are specific to anhedonia as compared with low mood and whether they are predictive of depressive outcomes. METHOD Functional MRI was used to collect blood-oxygen-level-dependent (BOLD) responses to anticipation of reward in the monetary incentive task in 1,576 adolescents in a community-based sample. Adolescents with current subthreshold depression and clinical depression were compared with matched healthy subjects. In addition, BOLD responses were compared across adolescents with anhedonia, low mood, or both symptoms, cross-sectionally and longitudinally. RESULTS Activity in the ventral striatum was reduced in participants with subthreshold and clinical depression relative to healthy comparison subjects. Low ventral striatum activation predicted transition to subthreshold or clinical depression in previously healthy adolescents at 2-year follow-up. Brain responses during reward anticipation decreased in a graded manner between healthy adolescents, adolescents with current or future subthreshold depression, and adolescents with current or future clinical depression. Low ventral striatum activity was associated with anhedonia but not low mood; however, the combined presence of both symptoms showed the strongest reductions in the ventral striatum in all analyses. CONCLUSIONS The findings suggest that reduced striatal activation operates as a mechanism across the risk spectrum for depression. It is associated with anhedonia in healthy adolescents and is a behavioral indicator of positive valence systems, consistent with predictions based on the Research Domain Criteria.

[1]  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.

[2]  M. Rietschel,et al.  DRD2/ANKK1 Polymorphism Modulates the Effect of Ventral Striatal Activation on Working Memory Performance , 2014, Neuropsychopharmacology.

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

[4]  Christopher G. Davey,et al.  Functional brain imaging studies of youth depression: A systematic review☆ , 2013, NeuroImage: Clinical.

[5]  M. Rietschel,et al.  DRD 2 / ANKK 1 Polymorphism Modulates the Effect of Ventral Striatal Activation on Working Memory Performance , 2014 .

[6]  Weina Zhang,et al.  The neural correlates of reward-related processing in major depressive disorder: a meta-analysis of functional magnetic resonance imaging studies. , 2013, Journal of affective disorders.

[7]  Michael P Milham,et al.  Striatum-based circuitry of adolescent depression and anhedonia. , 2013, Journal of the American Academy of Child and Adolescent Psychiatry.

[8]  A. Stringaris,et al.  The Value of Measuring Impact Alongside Symptoms in Children and Adolescents: A Longitudinal Assessment in a Community Sample , 2013, Journal of abnormal child psychology.

[9]  David Cucurell,et al.  Neurophysiological Differences in Reward Processing in Anhedonics , 2022 .

[10]  J. Salamone,et al.  The Mysterious Motivational Functions of Mesolimbic Dopamine , 2012, Neuron.

[11]  R. Shelton,et al.  Effort-based decision-making in major depressive disorder: a translational model of motivational anhedonia. , 2012, Journal of abnormal psychology.

[12]  N. Ryan,et al.  Anhedonia predicts poorer recovery among youth with selective serotonin reuptake inhibitor treatment-resistant depression. , 2012, Journal of the American Academy of Child and Adolescent Psychiatry.

[13]  D. Shohamy,et al.  Ventromedial prefrontal-subcortical systems and the generation of affective meaning , 2012, Trends in Cognitive Sciences.

[14]  Christian E. Waugh,et al.  Anticipatory pleasure predicts motivation for reward in major depression. , 2012, Journal of abnormal psychology.

[15]  R. Dahl,et al.  Research Review: altered reward function in adolescent depression: what, when and how? , 2012, Journal of child psychology and psychiatry, and allied disciplines.

[16]  D. Zald,et al.  Reconsidering anhedonia in depression: Lessons from translational neuroscience , 2011, Neuroscience & Biobehavioral Reviews.

[17]  S. Collishaw,et al.  The ‘DAWBA bands’ as an ordered-categorical measure of child mental health: description and validation in British and Norwegian samples , 2011, Social Psychiatry and Psychiatric Epidemiology.

[18]  M. Rietschel,et al.  The IMAGEN study: reinforcement-related behaviour in normal brain function and psychopathology , 2010, Molecular Psychiatry.

[19]  Edmund Sonuga-Barke,et al.  Hyporesponsive Reward Anticipation in the Basal Ganglia following Severe Institutional Deprivation Early in Life , 2010, Journal of Cognitive Neuroscience.

[20]  The effects of anhedonia and depression on hedonic responses , 2010, Psychiatry Research.

[21]  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 .

[22]  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.

[23]  Jan Wacker,et al.  The role of the nucleus accumbens and rostral anterior cingulate cortex in anhedonia: Integration of resting EEG, fMRI, and volumetric techniques , 2009, NeuroImage.

[24]  J. Buckner,et al.  Implications of the DSM's emphasis on sadness and anhedonia in major depressive disorder , 2008, Psychiatry Research.

[25]  J B Poline,et al.  Dopaminergic function in depressed patients with affective flattening or with impulsivity: [18F]Fluoro-l-dopa positron emission tomography study with voxel-based analysis , 2007, Psychiatry Research: Neuroimaging.

[26]  C. Carter,et al.  Reward-related decision-making in pediatric major depressive disorder: an fMRI study. , 2006, Journal of child psychology and psychiatry, and allied disciplines.

[27]  R. Dahl,et al.  Neural systems of positive affect: Relevance to understanding child and adolescent depression? , 2005, Development and Psychopathology.

[28]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

[29]  S. Haber,et al.  Imaging Human Mesolimbic Dopamine Transmission with Positron Emission Tomography. Part II: Amphetamine-Induced Dopamine Release in the Functional Subdivisions of the Striatum , 2003, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[30]  J. Pardo,et al.  Brain activity in ventromedial prefrontal cortex correlates with individual differences in negative affect , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[31]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[32]  R. Goodman,et al.  Psychometric properties of the strengths and difficulties questionnaire. , 2001, Journal of the American Academy of Child and Adolescent Psychiatry.

[33]  Brian Knutson,et al.  Anticipation of Increasing Monetary Reward Selectively Recruits Nucleus Accumbens , 2001, The Journal of Neuroscience.

[34]  H. Meltzer,et al.  The Development and Well-Being Assessment: description and initial validation of an integrated assessment of child and adolescent psychopathology. , 2000, Journal of child psychology and psychiatry, and allied disciplines.

[35]  J. Martinot,et al.  A prognostic study of clinical dimensions in adolescent-onset psychoses. , 2000, Schizophrenia bulletin.

[36]  D. Pine,et al.  Adolescent depressive symptoms as predictors of adult depression: moodiness or mood disorder? , 1999, The American journal of psychiatry.

[37]  A. Petersen,et al.  A self-report measure of pubertal status: Reliability, validity, and initial norms , 1988, Journal of youth and adolescence.

[38]  J. Cuzick A Wilcoxon-type test for trend. , 1985, Statistics in medicine.