Abstract
Adolescence is a transition period that is assumed to be characterized by increased sensitivity to reward. While there is growing research on reward processing in adolescents, investigations into the engagement of brain regions under different reward-related conditions in one sample of healthy adolescents, especially in a target age group, are missing. We aimed to identify brain regions preferentially activated in a reaction time task (monetary incentive delay (MID) task) and a simple guessing task (SGT) in a sample of 14-year-old adolescents (N = 54) using two commonly used reward paradigms. Functional magnetic resonance imaging was employed during the MID with big versus small versus no win conditions and the SGT with big versus small win and big versus small loss conditions. Analyses focused on changes in blood oxygen level–dependent contrasts during reward and punishment processing in anticipation and feedback phases. We found clear magnitude-sensitive response in reward-related brain regions such as the ventral striatum during anticipation in the MID task, but not in the SGT. This was also true for reaction times. The feedback phase showed clear reward-related, but magnitude-independent, response patterns, for example in the anterior cingulate cortex, in both tasks. Our findings highlight neural and behavioral response patterns engaged in two different reward paradigms in one sample of 14-year-old healthy adolescents and might be important for reference in future studies investigating reward and punishment processing in a target age group.
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References
Balleine B, Killcross S (1994) Effects of ibotenic acid lesions of the nucleus accumbens on instrumental action. Behav Brain Res 65:181–193
Berridge KC, Robinson TE, Aldridge JW (2009) Dissecting components of reward: ‘liking’, ‘wanting’, and learning. Curr Opin Pharmacol 9:65–73
Bjork JM, Knutson B, Fong GW, Caggiano DM, Bennett SM, Hommer DW (2004) Incentive-elicited brain activation in adolescents: similarities and differences from young adults. J Neurosci 24:1793–1802
Bjork JM, Knutson B, Hommer DW (2008) Incentive-elicited striatal activation in adolescent children of alcoholics. Addiction 103(8):1308–1319
Bjork JM, Smith AR, Chen G, Hommer DW (2010) Adolescents, adults and rewards: comparing motivational neurocircuitry recruitment using fMRI. PLoS One 5:e11440
Brown SA, Tapert SF, Granholm E, Delis DC (2000) Neurocognitive functioning of adolescents: effects of protracted alcohol use. Alcohol Clin Exp Res 24(2):164–171
Carter RM, Macinnes JJ, Huettel SA, Adcock RA (2009) Activation in the VTA and nucleus accumbens increases in anticipation of both gains and losses. Front Behav Neurosci 3:21
Corbit LH, Muir JL, Balleine BW (2001) The role of the nucleus accumbens in instrumental conditioning: evidence of a functional dissociation between accumbens core and shell. J Neurosci 21:3251–3260
Crews F, He J, Hodge C (2007) Adolescent cortical development: a critical period of vulnerability for addiction. Pharmacol Biochem Behav 86:189–199
Dahl RE (2004) Adolescent brain development: a period of vulnerabilities and opportunities.Keynote address. Ann NY Acad Sci 1021:1–22
Delgado MR, Locke HM, Stenger VA, Fiez JA (2003) Dorsal striatum responses to reward and punishment: effects of valence and magnitude manipulations. Cogn Affect Behav Neurosci 3:27–38
Ernst M, Nelson EE, McClure EB, Monk CS, Munson S, Eshel N, Zarahn E, Leibenluft E, Zametkin A, Towbin K, Blair J, Charney D, Pine DS (2004) Choice selection and reward anticipation: an fMRI study. Neuropsychologia 42:1585–1597
Ernst M, Nelson EE, Jazbec S, McClure EB, Monk CS et al (2005) Amygdala and nucleus accumbens in responses to receipt and omission of gains in adults and adolescents. Neuroimage 25:1279–1291
Galvan A, Hare TA, Parra CE, Penn J, Voss H et al (2006) Earlier development of the accumbens relative to orbitofrontal cortex might underlie risk-taking behavior in adolescents. J Neurosci 26:6885–6892
Goodman R, Ford T, Richards H, Gatward R, Meltzer H (2000) The development and well-being assessment: description and initial validation of an integrated assessment of child and adolescent psychopathology. J Child Psychol Psychiatry 41:645–655
Kirsch P, Schienle A, Stark R, Sammer G, Blecker C, Walter B, Ott U, Burkart J, Vaitl D (2003) Anticipation of reward in a nonaversive differential conditioning paradigm and the brain reward system: an event-related fMRI study. NeuroImage 20:1086–1095
Knutson B, Greer SM (2008) Anticipatory affect: neural correlates and consequences for choice. Phil Trans B R Soc B 363:3771–3786
Knutson B, Westdorp A, Kaiser E, Hommer D (2000) FMRI visualization of brain activity during a monetary incentive delay task. NeuroImage 12:20–27
Knutson B, Adams CM, Fong GW, Hommer D (2001a) Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J Neuroscience 21:RC159
Knutson B, Fong GW, Adams CM, Varner JL, Hommer D (2001b) Dissociation of reward anticipation and outcome with event-related fMRI. NeuroReport 12:3683–3687
Schumann G, Loth E, Banaschewski T, Barbot A, Barker G, Büchel C, Conrod PJ, Dalley JW, Flor H, Gallinat J, Garavan H, Heinz A, Itterman B, Lathrop M, Mallik C, Mann K, Martinot J-L, Paus T, Poline J-B, Robbins TW, Rietschel M, Reed L, Smolka M, Spanagel R, Speiser C, Stephens DN, Ströhle A, Struve M, The IMAGEN consortium (2010) The IMAGEN study: reinforcement-related behaviour in normal brain function and psychopathology. Mol Psychiatry 15:1128–1139
Steinberg L (2009) A behavioral scientist looks at the science of adolescent brain development. Brain Cogn 72:160–164
Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15(1):273–289
Van Leijenhorst L, Moor BG, Op de Macks ZA, Rombouts SA, Westenberg PM, Crone EA (2010) Adolescent risky decision-making: neurocognitive development of reward and control regions. Neuroimage 51:345–355
Yacubian J, Gläscher J, Schroeder K, Sommer T, Braus DF, Büchel C (2006) Dissociable systems for gain- and loss-related value predictions and errors of prediction in the human brain. J Neurosci 26:9530–9537
Yacubian J, Sommer T, Schroeder K, Gläscher J, Braus DF, Büchel C (2007) Subregions of the ventral striatum show preferential coding of reward magnitude and probability. NeuroImage 38:557–563
Zink CF, Pagnoni G, Martin-Skurski ME, Chappelow JC, Berns GS (2004) Human striatal responses to monetary reward depend on saliency. Neuron 42:509–517
Acknowledgments
Support of this study was provided by the IMAGEN project, which receives research funding from the European Community’s Sixth Framework Program (LSHM-CT-2007-037286) and coordinated project ADAMS (242257) as well as the UK-NIHR-Biomedical Research Centre Mental Health, the MRC-Addiction Research Cluster “Genomic Biomarkers”, and the MRC program grant “Developmental pathways into adolescent substance abuse” (93558). This research was also supported by the German Ministry of Education and Research (BMBF grant # 01EV0711). This manuscript reflects only the author’s views and the Community is not liable for any use that may be made of the information contained therein. TB served in an advisory or consultancy role for Bristol-Myers Sqibb, Develco Pharma, Lilly, Medice, Novartis, Shire and Viforpharma. He received conference attendance support and conference support or received speaker’s fee by Lilly, Janssen McNeil, Medice, Novartis, Shire, UCB. He is/has been involved in clinical trials conducted by Lilly, Shire and Novartis. The present work is unrelated to the above grants and relationships. AH has received research funding from the German Research Foundation and the Bernstein Center for Computational Neuroscience Berlin (German Federal Ministry of Education and Research), Eli Lilly & Company, Janssen-Cilag and Bristol-Myers Squibb. AH has received Speaker Honoraria from Janssen-Cilag, Johnson & Johnson, Lilly, Pfizer and Servier.
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Frauke Nees and Sabine Vollstädt-Klein shared first authorship.
Members of the IMAGEN consortium are listed in the Appendix.
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Appendix
Appendix
IMAGEN Consortium
King’s College, Institute of Psychiatry, London, UK
G. Schumann
P. Conrod
L. Reed
G. Barker
S. Williams
E. Loth
M. Struve
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 (Coordination office)
Department of Psychiatry and Psychotherapy, Campus Charité Mitte, Charité–Universitätsmedizin Berlin, Berlin, Germany
A. Heinz
J. Gallinat
I. Häke
N. Ivanov
A. Klär
J. Reuter
C. Palafox
C. Hohmann
C. Schilling
K. Lüdemann
A. Romanowski
A. Ströhle
E. Wolff
M. Rapp
Physikalisch-Technische Bundesanstalt, Berlin, Germany
B. Ittermann
R. Brühl
A. Ihlenfeld
B. Walaszek
F. Schubert
Institute of Neuroscience, Trinity College, Dublin, Ireland
H. Garavan
C. Connolly
J. Jones
E. Lalor
E. McCabe
A. Ní Shiothcháin
R. Whelan
Department of Psychopharmacology, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
R. Spanagel,
F. Leonardi-Essmann,
W. Sommer
Department of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
H. Flor
F. Nees
Department of Child and Adolescent Psychiatry, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
T. Banaschewski
L. Poustka
S. Steiner
Department of Addictive Behaviour and Addiction Medicine, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
K. Mann
M. Buehler
S. Vollstaedt-Klein
Department of Genetic Epidemiology in Psychiatry, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
M. Rietschel
E. Stolzenburg
C. Schmal
F. Schirmbeck
Brain and Body Centre, University of Nottingham, Nottingham, UK
T. Paus
P. Gowland
N. Heym
C. Lawrence
C. Newman
Z. Pausova
Technische Universitaet Dresden, Dresden, Germany
M. Smolka
T. Huebner
S. Ripke
E. Mennigen
K. Muller
V. Ziesch
Department of Systems Neuroscience, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
C. Büchel
U. Bromberg
T. Fadai
L. Lueken
J. Yacubian
J. Finsterbusch
Institut National de la Sante´ et de la Recherche Médicale, Service Hospitalier Frédéric Joliot, Orsay, France
J.-L. Martinot
E. Artiges
N. Bordas
S. de Bournonville
Z. Bricaud
F. Gollier Briand
H. Lemaitre
J. Massicotte
R. Miranda
M.-L. Paillere Martinot
J. Penttilä
Neurospin, Commissariat à l0Energie Atomique, Paris, France
J.-B. Poline
A. Barbot
Y. Schwartz
C. Lalanne
V. Frouin
B. Thyreau
Department of Experimental Psychology, Behavioural and Clinical Neurosciences Institute, University of Cambridge, Cambridge, UK
J. Dalley
A. Mar
T. Robbins
N. Subramaniam
D. Theobald
N. Richmond
M. de Rover
A. Molander
E. Jordan
E. Robinson
L. Hipolata
M. Moreno
M. Arroyo
University of Sussex, Brighton, UK
D. Stephens
T. Ripley
H. Crombag
Y. Pena
Centre National de Genotypage, Evry, France (CNG)
M. Lathrop
D. Zelenika
S. Heath
German Centre for Ethics in Medicine, Bonn (DZEM), Germany
D. Lanzerath
B. Heinrichs
T. Spranger
Gesellschaft fuer Ablauforganisation m.b.H. (Munich) (GABO), Germany
B. Fuchs
C. Speiser
Klinik für Kinder- und Jugendpsychiatrie, Zentrum für Psychosoziale Medizin, Universitätsklinikum Heidelberg, Germany
F. Resch
J. Haffner
P. Parzer
R. Brunner
Scito, Paris, France
A. Klaassen
I. Klaassen
PERTIMM, Asnières-Sur-Seine, France
P. Constant
X. Mignon
NordicNeuroLabs, Bergen, Norway
T. Thomsen
S. Zysset
A. Vestboe
Delosis Ltd, London, UK
J. Ireland
J. Rogers
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Nees, F., Vollstädt-Klein, S., Fauth-Bühler, M. et al. A target sample of adolescents and reward processing: same neural and behavioral correlates engaged in common paradigms?. Exp Brain Res 223, 429–439 (2012). https://doi.org/10.1007/s00221-012-3272-8
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DOI: https://doi.org/10.1007/s00221-012-3272-8