Neural basis of reward anticipation and its genetic determinants

Tianye Jia; Christine Macare; Sylvane Desrivières; Dante A Gonzalez; Chenyang Tao; Xiaoxi Ji; Barbara Ruggeri; Frauke Nees; Tobias Banaschewski; Gareth J Barker; Arun L W Bokde; Uli Bromberg; Christian Büchel; Patricia J Conrod; Rachel Dove; Vincent Frouin; Jürgen Gallinat; Hugh Garavan; Penny A Gowland; Andreas Heinz; Bernd Ittermann; Mark Lathrop; Hervé Lemaitre; Jean-Luc Martinot; Tomáš Paus; Zdenka Pausova; Jean-Baptiste Poline; Marcella Rietschel; Trevor Robbins; Michael N Smolka; Christian P Müller; Jianfeng Feng; Adrian Rothenfluh; Herta Flor; Gunter Schumann; IMAGEN Consortium

doi:10.1073/pnas.1503252113

Neural basis of reward anticipation and its genetic determinants

Tianye Jia, Christine Macare, Sylvane Desrivières, Dante A Gonzalez, Chenyang Tao, Xiaoxi Ji, Barbara Ruggeri, Frauke Nees, Tobias Banaschewski, Gareth J Barker, Arun L W Bokde, Uli Bromberg, Christian Büchel, Patricia J Conrod, Rachel Dove, Vincent Frouin, Jürgen Gallinat, Hugh Garavan, Penny A Gowland, Andreas HeinzBernd Ittermann, Mark Lathrop, Hervé Lemaitre, Jean-Luc Martinot, Tomáš Paus, Zdenka Pausova, Jean-Baptiste Poline, Marcella Rietschel, Trevor Robbins, Michael N Smolka, Christian P Müller, Jianfeng Feng, Adrian Rothenfluh, Herta Flor, Gunter Schumann, IMAGEN Consortium

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Abstract

Dysfunctional reward processing is implicated in various mental disorders, including attention deficit hyperactivity disorder (ADHD) and addictions. Such impairments might involve different components of the reward process, including brain activity during reward anticipation. We examined brain nodes engaged by reward anticipation in 1,544 adolescents and identified a network containing a core striatal node and cortical nodes facilitating outcome prediction and response preparation. Distinct nodes and functional connections were preferentially associated with either adolescent hyperactivity or alcohol consumption, thus conveying specificity of reward processing to clinically relevant behavior. We observed associations between the striatal node, hyperactivity, and the vacuolar protein sorting-associated protein 4A (VPS4A) gene in humans, and the causal role of Vps4 for hyperactivity was validated in Drosophila. Our data provide a neurobehavioral model explaining the heterogeneity of reward-related behaviors and generate a hypothesis accounting for their enduring nature.

Original language	English
Journal	Proceedings of the National Academy of Sciences of the United States of America
Early online date	21 Mar 2016
DOIs	https://doi.org/10.1073/pnas.1503252113
Publication status	E-pub ahead of print - 21 Mar 2016

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10.1073/pnas.1503252113

Jia et al PNAS (Final 20 Jan Ethic)Accepted author manuscript, 89 KBLicence: Other

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Jia, T., Macare, C., Desrivières, S., Gonzalez, D. A., Tao, C., Ji, X., Ruggeri, B., Nees, F., Banaschewski, T., Barker, G. J., Bokde, A. L. W., Bromberg, U., Büchel, C., Conrod, P. J., Dove, R., Frouin, V., Gallinat, J., Garavan, H., Gowland, P. A., ... IMAGEN Consortium (2016). Neural basis of reward anticipation and its genetic determinants. Proceedings of the National Academy of Sciences of the United States of America. Advance online publication. https://doi.org/10.1073/pnas.1503252113

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title = "Neural basis of reward anticipation and its genetic determinants",

abstract = "Dysfunctional reward processing is implicated in various mental disorders, including attention deficit hyperactivity disorder (ADHD) and addictions. Such impairments might involve different components of the reward process, including brain activity during reward anticipation. We examined brain nodes engaged by reward anticipation in 1,544 adolescents and identified a network containing a core striatal node and cortical nodes facilitating outcome prediction and response preparation. Distinct nodes and functional connections were preferentially associated with either adolescent hyperactivity or alcohol consumption, thus conveying specificity of reward processing to clinically relevant behavior. We observed associations between the striatal node, hyperactivity, and the vacuolar protein sorting-associated protein 4A (VPS4A) gene in humans, and the causal role of Vps4 for hyperactivity was validated in Drosophila. Our data provide a neurobehavioral model explaining the heterogeneity of reward-related behaviors and generate a hypothesis accounting for their enduring nature.",

author = "Tianye Jia and Christine Macare and Sylvane Desrivi{\`e}res and Gonzalez, {Dante A} and Chenyang Tao and Xiaoxi Ji and Barbara Ruggeri and Frauke Nees and Tobias Banaschewski and Barker, {Gareth J} and Bokde, {Arun L W} and Uli Bromberg and Christian B{\"u}chel and Conrod, {Patricia J} and Rachel Dove and Vincent Frouin and J{\"u}rgen Gallinat and Hugh Garavan and Gowland, {Penny A} and Andreas Heinz and Bernd Ittermann and Mark Lathrop and Herv{\'e} Lemaitre and Jean-Luc Martinot and Tom{\'a}{\v s} Paus and Zdenka Pausova and Jean-Baptiste Poline and Marcella Rietschel and Trevor Robbins and Smolka, {Michael N} and M{\"u}ller, {Christian P} and Jianfeng Feng and Adrian Rothenfluh and Herta Flor and Gunter Schumann and {IMAGEN Consortium}",

year = "2016",

month = mar,

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doi = "10.1073/pnas.1503252113",

language = "English",

journal = "Proceedings of the National Academy of Sciences of the United States of America",

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Jia, T , Macare, C , Desrivières, S, Gonzalez, DA, Tao, C, Ji, X, Ruggeri, B, Nees, F, Banaschewski, T, Barker, GJ, Bokde, ALW, Bromberg, U, Büchel, C, Conrod, PJ, Dove, R, Frouin, V, Gallinat, J, Garavan, H, Gowland, PA, Heinz, A, Ittermann, B, Lathrop, M, Lemaitre, H, Martinot, J-L, Paus, T, Pausova, Z, Poline, J-B, Rietschel, M, Robbins, T, Smolka, MN, Müller, CP, Feng, J, Rothenfluh, A, Flor, H, Schumann, G & IMAGEN Consortium 2016, 'Neural basis of reward anticipation and its genetic determinants', Proceedings of the National Academy of Sciences of the United States of America. https://doi.org/10.1073/pnas.1503252113

TY - JOUR

T1 - Neural basis of reward anticipation and its genetic determinants

AU - Jia, Tianye

AU - Macare, Christine

AU - Desrivières, Sylvane

AU - Gonzalez, Dante A

AU - Tao, Chenyang

AU - Ji, Xiaoxi

AU - Ruggeri, Barbara

AU - Nees, Frauke

AU - Banaschewski, Tobias

AU - Barker, Gareth J

AU - Bokde, Arun L W

AU - Bromberg, Uli

AU - Büchel, Christian

AU - Conrod, Patricia J

AU - Dove, Rachel

AU - Frouin, Vincent

AU - Gallinat, Jürgen

AU - Garavan, Hugh

AU - Gowland, Penny A

AU - Heinz, Andreas

AU - Ittermann, Bernd

AU - Lathrop, Mark

AU - Lemaitre, Hervé

AU - Martinot, Jean-Luc

AU - Paus, Tomáš

AU - Pausova, Zdenka

AU - Poline, Jean-Baptiste

AU - Rietschel, Marcella

AU - Robbins, Trevor

AU - Smolka, Michael N

AU - Müller, Christian P

AU - Feng, Jianfeng

AU - Rothenfluh, Adrian

AU - Flor, Herta

AU - Schumann, Gunter

AU - IMAGEN Consortium

PY - 2016/3/21

Y1 - 2016/3/21

N2 - Dysfunctional reward processing is implicated in various mental disorders, including attention deficit hyperactivity disorder (ADHD) and addictions. Such impairments might involve different components of the reward process, including brain activity during reward anticipation. We examined brain nodes engaged by reward anticipation in 1,544 adolescents and identified a network containing a core striatal node and cortical nodes facilitating outcome prediction and response preparation. Distinct nodes and functional connections were preferentially associated with either adolescent hyperactivity or alcohol consumption, thus conveying specificity of reward processing to clinically relevant behavior. We observed associations between the striatal node, hyperactivity, and the vacuolar protein sorting-associated protein 4A (VPS4A) gene in humans, and the causal role of Vps4 for hyperactivity was validated in Drosophila. Our data provide a neurobehavioral model explaining the heterogeneity of reward-related behaviors and generate a hypothesis accounting for their enduring nature.

AB - Dysfunctional reward processing is implicated in various mental disorders, including attention deficit hyperactivity disorder (ADHD) and addictions. Such impairments might involve different components of the reward process, including brain activity during reward anticipation. We examined brain nodes engaged by reward anticipation in 1,544 adolescents and identified a network containing a core striatal node and cortical nodes facilitating outcome prediction and response preparation. Distinct nodes and functional connections were preferentially associated with either adolescent hyperactivity or alcohol consumption, thus conveying specificity of reward processing to clinically relevant behavior. We observed associations between the striatal node, hyperactivity, and the vacuolar protein sorting-associated protein 4A (VPS4A) gene in humans, and the causal role of Vps4 for hyperactivity was validated in Drosophila. Our data provide a neurobehavioral model explaining the heterogeneity of reward-related behaviors and generate a hypothesis accounting for their enduring nature.

U2 - 10.1073/pnas.1503252113

DO - 10.1073/pnas.1503252113

M3 - Article

C2 - 27001827

SN - 0027-8424

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

ER -

Neural basis of reward anticipation and its genetic determinants

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