. 2015 Dec;172(12):1215-23.

doi: 10.1176/appi.ajp.2015.14101298. Epub 2015 Jun 18.

The Brain's Response to Reward Anticipation and Depression in Adolescence: Dimensionality, Specificity, and Longitudinal Predictions in a Community-Based Sample

Argyris Stringaris¹, Pablo Vidal-Ribas Belil¹, Eric Artiges¹, Hervé Lemaitre¹, Fanny Gollier-Briant¹, Selina Wolke¹, Hélène Vulser¹, Ruben Miranda¹, Jani Penttilä¹, Maren Struve¹, Tahmine Fadai¹, Viola Kappel¹, Yvonne Grimmer¹, Robert Goodman¹, Luise Poustka¹, Patricia Conrod¹, Anna Cattrell¹, Tobias Banaschewski¹, Arun L W Bokde¹, Uli Bromberg¹, Christian Büchel¹, Herta Flor¹, Vincent Frouin¹, Juergen Gallinat¹, Hugh Garavan¹, Penny Gowland¹, Andreas Heinz¹, Bernd Ittermann¹, Frauke Nees¹, Dimitri Papadopoulos¹, Tomas Paus¹, Michael N Smolka¹, Henrik Walter¹, Rob Whelan¹, Jean-Luc Martinot¹, Gunter Schumann¹, Marie-Laure Paillère-Martinot¹; IMAGEN Consortium

Collaborators, Affiliations

Collaborators

IMAGEN Consortium:
J B Poline, Z Pausova, K Mann, G J Barker, C Lawrence, E Loth, M Rietschel, T W Robbins, L Reed, S Williams, A Lourdusamy, S Costafreda, A Cattrell, C Nymberg, L Topper, L Smith, S Havatzias, K Stueber, C Mallik, T K Clarke, D Stacey, C Peng Wong, H Werts, S Williams, C Andrew, S Desrivieres, S Zewdie, I Häke, N Ivanov, A Klär, J Reuter, C Palafox, C Hohmann, C Schilling, K Lüdemann, A Romanowski, A Ströhle, E Wolff, M Rapp, R Brühl, A Ihlenfeld, B Walaszek, F Schubert, C Connolly, J Jones, E Lalor, E McCabe, A NíShiothcháin, R Spanagel, F Leonardi-Essmann, W Sommer, S Vollstaedt-Klein, S Steiner, M Buehler, E Stolzenburg, C Schmal, F Schirmbeck, N Heym, C Newman, T Huebner, S Ripke, E Mennigen, K Muller, V Ziesch, L Lueken, J Yacubian, J Finsterbusch, N Bordas, Z Bricaud, A Galinowski, C Gourlan, Y Schwartz, C Lalanne, A Barbot, B Thyreau, J Dalley, A Mar, N Subramaniam, D Theobald, N Richmond, M de Rover, A Molander, E Jordan, E Robinson, L Hipolata, M Moreno, M Arroyo, D Stephens, T Ripley, H Crombag, Y Pena, M Lathrop, D Zelenika, S Heath, D Lanzerath, B Heinrichs, T Spranger, B Fuchs, C Speiser, F Resch, J Haffner, P Parzer, R Brunner, A Klaassen, I Klaassen, P Constant, X Mignon, T Thomsen, S Zysset, A Vestboe, J Ireland, J Rogers

Affiliation

¹ From the Department of Child and Adolescent Psychiatry, King's College London, Institute of Psychiatry, Psychology, and Neuroscience, London; INSERM, UMR 1000, Research Unit Imaging and Psychiatry, Service Hospitalier Frédéric Joliot, Orsay, France; University Paris-Sud 11, Orsay; Paris Descartes University, Sorbonne Paris Cité, Paris; AP-HP, Department of Adolescent Psychopathology and Medicine, Maison de Solenn, Cochin Hospital, Paris; Psychiatry Department 91G16, Orsay Hospital, Orsay; Neurospin, Commissariat à l'Energie Atomique et aux Energies Alternatives, Paris; Department of Social and Health Care, Psychosocial Services Adolescent Outpatient Clinic Kauppakatu 14, Lahti, Finland; Department of Psychiatry, University of Montreal, CHU Ste Justine Hospital, Montreal; Department of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Germany; Universitaetsklinikum Hamburg Eppendorf, Hamburg, Germany; Department of Child and Adolescent Psychiatry, Psychosomatics, and Psychotherapy, Charité-Universitätsmedizin, Berlin, Germany; Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Germany; Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland; MRC Social, Genetic, and Developmental Psychiatry Centre, London; Department of Psychiatry and Psychotherapy, Campus Charité Mitte, Charité-Universitätsmedizin, Berlin; Departments of Psychiatry and Psychology, University of Vermont, Burlington; School of Physics and Astronomy, University of Nottingham, Nottingham, United Kingdom; Physikalisch-Technische Bundesanstalt, Braunschweig and Berlin; Rotman Research Institute, University of Toronto, Toronto; Department of Psychiatry and Psychotherapy and the Neuroimaging Center, Department of Psychology, Technische Universität Dresden, Dresden, Germany.

PMID: 26085042
PMCID: PMC7614275
DOI: 10.1176/appi.ajp.2015.14101298

The Brain's Response to Reward Anticipation and Depression in Adolescence: Dimensionality, Specificity, and Longitudinal Predictions in a Community-Based Sample

Argyris Stringaris et al. Am J Psychiatry. 2015 Dec.

. 2015 Dec;172(12):1215-23.

doi: 10.1176/appi.ajp.2015.14101298. Epub 2015 Jun 18.

Authors

Collaborators

IMAGEN Consortium:
J B Poline, Z Pausova, K Mann, G J Barker, C Lawrence, E Loth, M Rietschel, T W Robbins, L Reed, S Williams, A Lourdusamy, S Costafreda, A Cattrell, C Nymberg, L Topper, L Smith, S Havatzias, K Stueber, C Mallik, T K Clarke, D Stacey, C Peng Wong, H Werts, S Williams, C Andrew, S Desrivieres, S Zewdie, I Häke, N Ivanov, A Klär, J Reuter, C Palafox, C Hohmann, C Schilling, K Lüdemann, A Romanowski, A Ströhle, E Wolff, M Rapp, R Brühl, A Ihlenfeld, B Walaszek, F Schubert, C Connolly, J Jones, E Lalor, E McCabe, A NíShiothcháin, R Spanagel, F Leonardi-Essmann, W Sommer, S Vollstaedt-Klein, S Steiner, M Buehler, E Stolzenburg, C Schmal, F Schirmbeck, N Heym, C Newman, T Huebner, S Ripke, E Mennigen, K Muller, V Ziesch, L Lueken, J Yacubian, J Finsterbusch, N Bordas, Z Bricaud, A Galinowski, C Gourlan, Y Schwartz, C Lalanne, A Barbot, B Thyreau, J Dalley, A Mar, N Subramaniam, D Theobald, N Richmond, M de Rover, A Molander, E Jordan, E Robinson, L Hipolata, M Moreno, M Arroyo, D Stephens, T Ripley, H Crombag, Y Pena, M Lathrop, D Zelenika, S Heath, D Lanzerath, B Heinrichs, T Spranger, B Fuchs, C Speiser, F Resch, J Haffner, P Parzer, R Brunner, A Klaassen, I Klaassen, P Constant, X Mignon, T Thomsen, S Zysset, A Vestboe, J Ireland, J Rogers

Affiliation

¹ From the Department of Child and Adolescent Psychiatry, King's College London, Institute of Psychiatry, Psychology, and Neuroscience, London; INSERM, UMR 1000, Research Unit Imaging and Psychiatry, Service Hospitalier Frédéric Joliot, Orsay, France; University Paris-Sud 11, Orsay; Paris Descartes University, Sorbonne Paris Cité, Paris; AP-HP, Department of Adolescent Psychopathology and Medicine, Maison de Solenn, Cochin Hospital, Paris; Psychiatry Department 91G16, Orsay Hospital, Orsay; Neurospin, Commissariat à l'Energie Atomique et aux Energies Alternatives, Paris; Department of Social and Health Care, Psychosocial Services Adolescent Outpatient Clinic Kauppakatu 14, Lahti, Finland; Department of Psychiatry, University of Montreal, CHU Ste Justine Hospital, Montreal; Department of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Germany; Universitaetsklinikum Hamburg Eppendorf, Hamburg, Germany; Department of Child and Adolescent Psychiatry, Psychosomatics, and Psychotherapy, Charité-Universitätsmedizin, Berlin, Germany; Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Germany; Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland; MRC Social, Genetic, and Developmental Psychiatry Centre, London; Department of Psychiatry and Psychotherapy, Campus Charité Mitte, Charité-Universitätsmedizin, Berlin; Departments of Psychiatry and Psychology, University of Vermont, Burlington; School of Physics and Astronomy, University of Nottingham, Nottingham, United Kingdom; Physikalisch-Technische Bundesanstalt, Braunschweig and Berlin; Rotman Research Institute, University of Toronto, Toronto; Department of Psychiatry and Psychotherapy and the Neuroimaging Center, Department of Psychology, Technische Universität Dresden, Dresden, Germany.

PMID: 26085042
PMCID: PMC7614275
DOI: 10.1176/appi.ajp.2015.14101298

Abstract

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.

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Figures

**Figure 1. BOLD Response to Anticipation of Reward in Adolescents With Clinical Depression (N=22) and Subthreshold Depression (N=101)^a**
^a Blood-oxygen-level-dependent (BOLD) response, overlaid on a T₁-weighted structural brain image, is decreased in both groups compared with a matched healthy comparison group (N=123). The image in panel A is centered at x=6, y=15, z=-2, and panel B at x=-12, y=14, z=-2. The color bar represents t values.

**Figure 2. Standardized BOLD Response in Adolescents Who Were Healthy at Baseline and Either Remained Healthy at 2-Year FollowUp or Developed Subthreshold or Clinical Depression**

Figure 3. Standardized BOLD Response in Left and Right Ventral Striatum in Adolescents From the Community-Based Sample With No Depressive Symptoms, With Low Mood Only, With Anhedonia Only, or With Both Symptoms
a Left: β=20.28, p=0.006; right: β=20.18, p=0.019. b Left: β=20.27, p=0.006; right: β=20.15, p=0.027.

See this image and copyright information in PMC

References

1. Forbes EE, Dahl RE. Research review: altered reward function in adolescent depression: what, when, and how? J Child Psychol Psychiatry. 2012;53:3–15. - PMC - PubMed
1. Kerestes R, Davey CG, Stephanou K, et al. Functional brain imaging studies of youth depression: a systematic review. Neuroimage Clin. 2014;4:209–231. - PMC - PubMed
1. Olino TM, McMakin DL, Morgan JK, et al. Reduced reward anticipation in youth at high-risk for unipolar depression: a preliminary study. Dev Cogn Neurosci. 2014;8:55–64. - PMC - PubMed
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The Brain's Response to Reward Anticipation and Depression in Adolescence: Dimensionality, Specificity, and Longitudinal Predictions in a Community-Based Sample

Collaborators

Affiliation

The Brain's Response to Reward Anticipation and Depression in Adolescence: Dimensionality, Specificity, and Longitudinal Predictions in a Community-Based Sample

Authors

Collaborators

Affiliation

Abstract

Figures

References

Publication types

MeSH terms

Grants and funding

LinkOut - more resources

Full Text Sources

Medical