Neural responses to reward valence and magnitude from pre- to early adolescence

Reuma Gadassi Polack; Jessica A. Mollick; Hanna Keren; Jutta Joormann; Richard Watts

doi:10.1016/j.neuroimage.2023.120166

Neural responses to reward valence and magnitude from pre- to early adolescence

Reuma Gadassi Polack, Jessica A. Mollick, Hanna Keren, Jutta Joormann, Richard Watts

Bar-Ilan University - Azrieli Faculty of Medicine

Research output: Contribution to journal › Article › peer-review

3 Scopus citations

Abstract

Background: Neural activation during reward processing is thought to underlie critical behavioral changes that take place during the transition to adolescence (e.g., learning, risk-taking). Though literature on the neural basis of reward processing in adolescence is booming, important gaps remain. First, more information is needed regarding changes in functional neuroanatomy in early adolescence. Another gap is understanding whether sensitivity to different aspects of the incentive (e.g., magnitude and valence) changes during the transition into adolescence. We used fMRI from a large sample of preadolescent children to characterize neural responses to incentive valence vs. magnitude during anticipation and feedback, and their change over a period of two years. Methods: Data were taken from the Adolescent Cognitive and Brain Development^SM (ABCD®) study release 3.0. Children completed the Monetary Incentive Delay task at baseline (ages 9–10) and year 2 follow-up (ages 11–12). Based on data from two sites (N = 491), we identified activation-based Regions of Interest (ROIs; e.g., striatum, prefrontal regions, etc.) that were sensitive to trial type (win $5, win $0.20, neutral, lose $0.20, lose $5) during anticipation and feedback phases. Then, in an independent subsample (N = 1470), we examined whether these ROIs were sensitive to valence and magnitude and whether that sensitivity changed over two years. Results: Our results show that most ROIs involved in reward processing (including the striatum, prefrontal cortex, and insula) are specialized, i.e., mainly sensitive to either incentive valence or magnitude, and this sensitivity was consistent over a 2-year period. The effect sizes of time and its interactions were significantly smaller (0.002≤η²≤0.02) than the effect size of trial type (0.06≤η²≤0.30). Interestingly, specialization was moderated by reward processing phase but was stable across development. Biological sex and pubertal status differences were few and inconsistent. Developmental changes were mostly evident during success feedback, where neural reactivity increased over time. Conclusions: Our results suggest sub-specialization to valence vs. magnitude within many ROIs of the reward circuitry. Additionally, in line with theoretical models of adolescent development, our results suggest that the ability to benefit from success increases from pre- to early adolescence. These findings can inform educators and clinicians and facilitate empirical research of typical and atypical motivational behaviors during a critical time of development.

Original language	English
Article number	120166
Journal	NeuroImage
Volume	275
Early online date	12 May 2023
DOIs	https://doi.org/10.1016/j.neuroimage.2023.120166
State	Published - 15 Jul 2023

Bibliographical note

Publisher Copyright:
© 2023 The Author(s)

Funding

This project has received funding from the European Union's Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant agreement No. 786,064, and the National Institute of Mental Health Translational Developmental Neuroscience Training Grant (T32 #MH18268) awarded to RGP. Data used in the preparation of this article were obtained from the Adolescent Brain Cognitive Development® (ABCD) Study ( https://abcdstudy.org ), held in the NIMH Data Archive (NDA). This is a multisite, longitudinal study designed to recruit more than 10,000 children age 9–10 and follow them over 10 years into early adulthood. The ABCD Study® is supported by the National Institutes of Health and Additional Federal Partners under award numbers U01DA041048, U01DA050989, U01DA051016, U01DA041022, U01DA051018, U01DA051037, U01DA050987, U01DA041174, U01DA041106, U01DA041117, U01DA041028, U01DA041134, U01DA050988, U01DA051039, U01DA041156, U01DA041025, U01DA041120, U01DA051038, U01DA041148, U01DA041093, U01DA041089, U24DA041123, U24DA041147. A full list of supporters is available at https://abcdstudy.org/federal-partners.html . A listing of participating sites and a complete listing of the study investigators can be found at https://abcdstudy.org/consortiummembers /. ABCD consortium investigators designed and implemented the study and/or provided data but did not necessarily participate in analysis or writing of this report. This manuscript reflects the views of the authors and may not reflect the opinions or views of the NIH or ABCD consortium investigators. The ABCD data repository grows and changes over time. The ABCD data used in this report came from NDA Release 3.0 (doi: 10.15154/1.519.007 ). This project has received funding from the European Union's Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant agreement No. 786,064, and the National Institute of Mental Health Translational Developmental Neuroscience Training Grant (T32 #MH18268) awarded to RGP. Data used in the preparation of this article were obtained from the Adolescent Brain Cognitive Development® (ABCD) Study (https://abcdstudy.org), held in the NIMH Data Archive (NDA). This is a multisite, longitudinal study designed to recruit more than 10,000 children age 9–10 and follow them over 10 years into early adulthood. The ABCD Study® is supported by the National Institutes of Health and Additional Federal Partners under award numbers U01DA041048, U01DA050989, U01DA051016, U01DA041022, U01DA051018, U01DA051037, U01DA050987, U01DA041174, U01DA041106, U01DA041117, U01DA041028, U01DA041134, U01DA050988, U01DA051039, U01DA041156, U01DA041025, U01DA041120, U01DA051038, U01DA041148, U01DA041093, U01DA041089, U24DA041123, U24DA041147. A full list of supporters is available at https://abcdstudy.org/federal-partners.html. A listing of participating sites and a complete listing of the study investigators can be found at https://abcdstudy.org/consortiummembers/. ABCD consortium investigators designed and implemented the study and/or provided data but did not necessarily participate in analysis or writing of this report. This manuscript reflects the views of the authors and may not reflect the opinions or views of the NIH or ABCD consortium investigators. The ABCD data repository grows and changes over time. The ABCD data used in this report came from NDA Release 3.0 (doi:10.15154/1.519.007).

Funders	Funder number
National Institute Of Mental Health Translational Developmental Neuroscience	T32 #MH18268
National Institutes of Health	U01DA051039, U01DA051016, U01DA051038, U01DA051018, U01DA051037, :10.15154/1.519.007, U01DA041106, U01DA041117, U01DA041028, U01DA041148, U24DA041147, U01DA041048, U01DA041025, U24DA041123, U01DA041134, U01DA041156, U01DA041089, U01DA041022, U01DA041120, U01DA041174, U01DA050987, U01DA050988, U01DA050989, U01DA041093
National Institute of Mental Health
H2020 Marie Skłodowska-Curie Actions	786,064
Horizon 2020

Keywords

ABCD study
Adolescence
Functional magnetic resonance imaging
Monetary incentive delay task
Reward processing

Access to Document

10.1016/j.neuroimage.2023.120166

Cite this

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title = "Neural responses to reward valence and magnitude from pre- to early adolescence",

abstract = "Background: Neural activation during reward processing is thought to underlie critical behavioral changes that take place during the transition to adolescence (e.g., learning, risk-taking). Though literature on the neural basis of reward processing in adolescence is booming, important gaps remain. First, more information is needed regarding changes in functional neuroanatomy in early adolescence. Another gap is understanding whether sensitivity to different aspects of the incentive (e.g., magnitude and valence) changes during the transition into adolescence. We used fMRI from a large sample of preadolescent children to characterize neural responses to incentive valence vs. magnitude during anticipation and feedback, and their change over a period of two years. Methods: Data were taken from the Adolescent Cognitive and Brain DevelopmentSM (ABCD{\textregistered}) study release 3.0. Children completed the Monetary Incentive Delay task at baseline (ages 9–10) and year 2 follow-up (ages 11–12). Based on data from two sites (N = 491), we identified activation-based Regions of Interest (ROIs; e.g., striatum, prefrontal regions, etc.) that were sensitive to trial type (win $5, win $0.20, neutral, lose $0.20, lose $5) during anticipation and feedback phases. Then, in an independent subsample (N = 1470), we examined whether these ROIs were sensitive to valence and magnitude and whether that sensitivity changed over two years. Results: Our results show that most ROIs involved in reward processing (including the striatum, prefrontal cortex, and insula) are specialized, i.e., mainly sensitive to either incentive valence or magnitude, and this sensitivity was consistent over a 2-year period. The effect sizes of time and its interactions were significantly smaller (0.002≤η2≤0.02) than the effect size of trial type (0.06≤η2≤0.30). Interestingly, specialization was moderated by reward processing phase but was stable across development. Biological sex and pubertal status differences were few and inconsistent. Developmental changes were mostly evident during success feedback, where neural reactivity increased over time. Conclusions: Our results suggest sub-specialization to valence vs. magnitude within many ROIs of the reward circuitry. Additionally, in line with theoretical models of adolescent development, our results suggest that the ability to benefit from success increases from pre- to early adolescence. These findings can inform educators and clinicians and facilitate empirical research of typical and atypical motivational behaviors during a critical time of development.",

keywords = "ABCD study, Adolescence, Functional magnetic resonance imaging, Monetary incentive delay task, Reward processing",

author = "{Gadassi Polack}, Reuma and Mollick, {Jessica A.} and Hanna Keren and Jutta Joormann and Richard Watts",

note = "Publisher Copyright: {\textcopyright} 2023 The Author(s)",

year = "2023",

month = jul,

day = "15",

doi = "10.1016/j.neuroimage.2023.120166",

language = "אנגלית",

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AU - Gadassi Polack, Reuma

AU - Mollick, Jessica A.

AU - Keren, Hanna

AU - Joormann, Jutta

AU - Watts, Richard

PY - 2023/7/15

Y1 - 2023/7/15

N2 - Background: Neural activation during reward processing is thought to underlie critical behavioral changes that take place during the transition to adolescence (e.g., learning, risk-taking). Though literature on the neural basis of reward processing in adolescence is booming, important gaps remain. First, more information is needed regarding changes in functional neuroanatomy in early adolescence. Another gap is understanding whether sensitivity to different aspects of the incentive (e.g., magnitude and valence) changes during the transition into adolescence. We used fMRI from a large sample of preadolescent children to characterize neural responses to incentive valence vs. magnitude during anticipation and feedback, and their change over a period of two years. Methods: Data were taken from the Adolescent Cognitive and Brain DevelopmentSM (ABCD®) study release 3.0. Children completed the Monetary Incentive Delay task at baseline (ages 9–10) and year 2 follow-up (ages 11–12). Based on data from two sites (N = 491), we identified activation-based Regions of Interest (ROIs; e.g., striatum, prefrontal regions, etc.) that were sensitive to trial type (win $5, win $0.20, neutral, lose $0.20, lose $5) during anticipation and feedback phases. Then, in an independent subsample (N = 1470), we examined whether these ROIs were sensitive to valence and magnitude and whether that sensitivity changed over two years. Results: Our results show that most ROIs involved in reward processing (including the striatum, prefrontal cortex, and insula) are specialized, i.e., mainly sensitive to either incentive valence or magnitude, and this sensitivity was consistent over a 2-year period. The effect sizes of time and its interactions were significantly smaller (0.002≤η2≤0.02) than the effect size of trial type (0.06≤η2≤0.30). Interestingly, specialization was moderated by reward processing phase but was stable across development. Biological sex and pubertal status differences were few and inconsistent. Developmental changes were mostly evident during success feedback, where neural reactivity increased over time. Conclusions: Our results suggest sub-specialization to valence vs. magnitude within many ROIs of the reward circuitry. Additionally, in line with theoretical models of adolescent development, our results suggest that the ability to benefit from success increases from pre- to early adolescence. These findings can inform educators and clinicians and facilitate empirical research of typical and atypical motivational behaviors during a critical time of development.

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Neural responses to reward valence and magnitude from pre- to early adolescence

Abstract

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Keywords

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