Reward and Punishment Sensitivity are Associated with Cross-disorder Traits

Christel M. Portengen; Emma Sprooten; Marcel P. Zwiers; Pieter J. Hoekstra; Andrea Dietrich; Nathalie E. Holz; Pascal M. Aggensteiner; Tobias Banaschewski; Ulrike M.E. Schulze; Melanie C. Saam; M.C. Craig; Arjun Sethi; Paramala Santosh; Ilyas Sagar Ouriaghli; Josefina Castro-Fornieles; Mireia Rosa; Celso Arango; María José Penzol; Julia E. Werhahn; Daniel Brandeis; Susanne Walitza; Marianne Oldehinkel; Barbara Franke; Jan K. Buitelaar; Jilly Naaijen

doi:10.1016/j.psychres.2021.113795

Reward and Punishment Sensitivity are Associated with Cross-disorder Traits

Christel M. Portengen, Emma Sprooten, Marcel P. Zwiers, Pieter J. Hoekstra, Andrea Dietrich, Nathalie E. Holz, Pascal M. Aggensteiner, Tobias Banaschewski, Ulrike M.E. Schulze, Melanie C. Saam, M.C. Craig, Arjun Sethi, Paramala Santosh, Ilyas Sagar Ouriaghli, Josefina Castro-Fornieles, Mireia Rosa, Celso Arango, María José Penzol, Julia E. Werhahn, Daniel BrandeisSusanne Walitza, Marianne Oldehinkel, Barbara Franke, Jan K. Buitelaar, Jilly Naaijen

School of Psychology

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

Abstract

Reversal learning deficits following reward and punishment processing are observed across disruptive behaviors (DB) and attention-deficit/hyperactivity disorder (ADHD), and have been associated with callous-unemotional (CU) traits. However, it remains unknown to what extent these altered reinforcement sensitivities are linked to the co-occurrence of oppositional traits, ADHD symptoms, and CU traits. Reward and punishment sensitivity and perseverative behavior were therefore derived from a probabilistic reversal learning task to investigate reinforcement sensitivity in participants with DB (n=183, ODD=62, CD=10, combined=57, age-range 8-18), ADHD (n=144, age-range 11-28), and controls (n=191, age-range 8-26). The SNAP-IV and Conners rating scales were used to assess oppositional and ADHD traits. The Inventory of CU traits was used to assess CU traits. Decreased reward sensitivity was associated with ADHD symptom severity (p=0.018) if corrected for oppositional symptoms. ADHD symptomatology interacted with oppositional behavior on perseveration (p=0.019), with the former aggravating the effect of oppositional behavior on perseveration and vice versa. Within a pooled sample, reversal learning alterations were associated with the severity of ADHD symptoms, underpinned by hyposensitivity to reward and increased perseveration. These results show ADHD traits, as opposed to oppositional behavior and CU traits, is associated with decreased reward-based learning in adolescents and adults.

_{© 2021, Christel M. Portengen, Emma Sprooten, Marcel P. Zwiers, Pieter J. Hoekstra, Andrea Dietrich, Nathalie E. Holz, Pascal M. Aggensteiner, Tobias Banaschewski, Ulrike M.E. Schulze, Melanie C. Saam, Michael C. Craig, Arjun Sethi, Paramala Santosh, Ilyas Sagar Ouriaghli, Josefina Castro-Fornieles, Mireia Rosa, Celso Arango, María José Penzol, Julia E. Werhahn, Daniel Brandeis Susanne Walitza, Marianne Oldehinkel, Barbara Franke, Jan K. Buitelaar, Jilly Naaijen. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. See}_{http://creativecommons.org/licenses/by/4.0/}

Original language	English
Journal	Psychiatry Research
DOIs	https://doi.org/10.1016/j.psychres.2021.113795
Publication status	Published - 8 Apr 2021

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10.1016/j.psychres.2021.113795

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Portengen, C. M., Sprooten, E., Zwiers, M. P., Hoekstra, P. J., Dietrich, A., Holz, N. E., Aggensteiner, P. M., Banaschewski, T., Schulze, U. M. E., Saam, M. C., Craig, M. C., Sethi, A., Santosh, P., Ouriaghli, I. S., Castro-Fornieles, J., Rosa, M., Arango, C., Penzol, M. J., Werhahn, J. E., ... Naaijen, J. (2021). Reward and Punishment Sensitivity are Associated with Cross-disorder Traits. Psychiatry Research. https://doi.org/10.1016/j.psychres.2021.113795

@article{09f9d89987ab4d3bac341ea384a13ae2,

title = "Reward and Punishment Sensitivity are Associated with Cross-disorder Traits",

abstract = "Reversal learning deficits following reward and punishment processing are observed across disruptive behaviors (DB) and attention-deficit/hyperactivity disorder (ADHD), and have been associated with callous-unemotional (CU) traits. However, it remains unknown to what extent these altered reinforcement sensitivities are linked to the co-occurrence of oppositional traits, ADHD symptoms, and CU traits. Reward and punishment sensitivity and perseverative behavior were therefore derived from a probabilistic reversal learning task to investigate reinforcement sensitivity in participants with DB (n=183, ODD=62, CD=10, combined=57, age-range 8-18), ADHD (n=144, age-range 11-28), and controls (n=191, age-range 8-26). The SNAP-IV and Conners rating scales were used to assess oppositional and ADHD traits. The Inventory of CU traits was used to assess CU traits. Decreased reward sensitivity was associated with ADHD symptom severity (p=0.018) if corrected for oppositional symptoms. ADHD symptomatology interacted with oppositional behavior on perseveration (p=0.019), with the former aggravating the effect of oppositional behavior on perseveration and vice versa. Within a pooled sample, reversal learning alterations were associated with the severity of ADHD symptoms, underpinned by hyposensitivity to reward and increased perseveration. These results show ADHD traits, as opposed to oppositional behavior and CU traits, is associated with decreased reward-based learning in adolescents and adults.{\textcopyright} 2021, Christel M. Portengen, Emma Sprooten, Marcel P. Zwiers, Pieter J. Hoekstra, Andrea Dietrich, Nathalie E. Holz, Pascal M. Aggensteiner, Tobias Banaschewski, Ulrike M.E. Schulze, Melanie C. Saam, Michael C. Craig, Arjun Sethi, Paramala Santosh, Ilyas Sagar Ouriaghli, Josefina Castro-Fornieles, Mireia Rosa, Celso Arango, Mar{\'i}a Jos{\'e} Penzol, Julia E. Werhahn, Daniel Brandeis Susanne Walitza, Marianne Oldehinkel, Barbara Franke, Jan K. Buitelaar, Jilly Naaijen. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. See http://creativecommons.org/licenses/by/4.0/ ",

author = "Portengen, {Christel M.} and Emma Sprooten and Zwiers, {Marcel P.} and Hoekstra, {Pieter J.} and Andrea Dietrich and Holz, {Nathalie E.} and Aggensteiner, {Pascal M.} and Tobias Banaschewski and Schulze, {Ulrike M.E.} and Saam, {Melanie C.} and M.C. Craig and Arjun Sethi and Paramala Santosh and Ouriaghli, {Ilyas Sagar} and Josefina Castro-Fornieles and Mireia Rosa and Celso Arango and Penzol, {Mar{\'i}a Jos{\'e}} and Werhahn, {Julia E.} and Daniel Brandeis and Susanne Walitza and Marianne Oldehinkel and Barbara Franke and Buitelaar, {Jan K.} and Jilly Naaijen",

year = "2021",

month = apr,

day = "8",

doi = "10.1016/j.psychres.2021.113795",

language = "English",

journal = "Psychiatry Research",

issn = "0165-1781",

publisher = "Elsevier",

}

Portengen, CM, Sprooten, E, Zwiers, MP, Hoekstra, PJ, Dietrich, A, Holz, NE, Aggensteiner, PM, Banaschewski, T, Schulze, UME, Saam, MC, Craig, MC, Sethi, A, Santosh, P, Ouriaghli, IS, Castro-Fornieles, J, Rosa, M, Arango, C, Penzol, MJ, Werhahn, JE, Brandeis, D, Walitza, S, Oldehinkel, M, Franke, B, Buitelaar, JK & Naaijen, J 2021, 'Reward and Punishment Sensitivity are Associated with Cross-disorder Traits', Psychiatry Research. https://doi.org/10.1016/j.psychres.2021.113795

TY - JOUR

T1 - Reward and Punishment Sensitivity are Associated with Cross-disorder Traits

AU - Portengen, Christel M.

AU - Sprooten, Emma

AU - Zwiers, Marcel P.

AU - Hoekstra, Pieter J.

AU - Dietrich, Andrea

AU - Holz, Nathalie E.

AU - Aggensteiner, Pascal M.

AU - Banaschewski, Tobias

AU - Schulze, Ulrike M.E.

AU - Saam, Melanie C.

AU - Craig, M.C.

AU - Sethi, Arjun

AU - Santosh, Paramala

AU - Ouriaghli, Ilyas Sagar

AU - Castro-Fornieles, Josefina

AU - Rosa, Mireia

AU - Arango, Celso

AU - Penzol, María José

AU - Werhahn, Julia E.

AU - Brandeis, Daniel

AU - Walitza, Susanne

AU - Oldehinkel, Marianne

AU - Franke, Barbara

AU - Buitelaar, Jan K.

AU - Naaijen, Jilly

PY - 2021/4/8

Y1 - 2021/4/8

N2 - Reversal learning deficits following reward and punishment processing are observed across disruptive behaviors (DB) and attention-deficit/hyperactivity disorder (ADHD), and have been associated with callous-unemotional (CU) traits. However, it remains unknown to what extent these altered reinforcement sensitivities are linked to the co-occurrence of oppositional traits, ADHD symptoms, and CU traits. Reward and punishment sensitivity and perseverative behavior were therefore derived from a probabilistic reversal learning task to investigate reinforcement sensitivity in participants with DB (n=183, ODD=62, CD=10, combined=57, age-range 8-18), ADHD (n=144, age-range 11-28), and controls (n=191, age-range 8-26). The SNAP-IV and Conners rating scales were used to assess oppositional and ADHD traits. The Inventory of CU traits was used to assess CU traits. Decreased reward sensitivity was associated with ADHD symptom severity (p=0.018) if corrected for oppositional symptoms. ADHD symptomatology interacted with oppositional behavior on perseveration (p=0.019), with the former aggravating the effect of oppositional behavior on perseveration and vice versa. Within a pooled sample, reversal learning alterations were associated with the severity of ADHD symptoms, underpinned by hyposensitivity to reward and increased perseveration. These results show ADHD traits, as opposed to oppositional behavior and CU traits, is associated with decreased reward-based learning in adolescents and adults.© 2021, Christel M. Portengen, Emma Sprooten, Marcel P. Zwiers, Pieter J. Hoekstra, Andrea Dietrich, Nathalie E. Holz, Pascal M. Aggensteiner, Tobias Banaschewski, Ulrike M.E. Schulze, Melanie C. Saam, Michael C. Craig, Arjun Sethi, Paramala Santosh, Ilyas Sagar Ouriaghli, Josefina Castro-Fornieles, Mireia Rosa, Celso Arango, María José Penzol, Julia E. Werhahn, Daniel Brandeis Susanne Walitza, Marianne Oldehinkel, Barbara Franke, Jan K. Buitelaar, Jilly Naaijen. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. See http://creativecommons.org/licenses/by/4.0/

AB - Reversal learning deficits following reward and punishment processing are observed across disruptive behaviors (DB) and attention-deficit/hyperactivity disorder (ADHD), and have been associated with callous-unemotional (CU) traits. However, it remains unknown to what extent these altered reinforcement sensitivities are linked to the co-occurrence of oppositional traits, ADHD symptoms, and CU traits. Reward and punishment sensitivity and perseverative behavior were therefore derived from a probabilistic reversal learning task to investigate reinforcement sensitivity in participants with DB (n=183, ODD=62, CD=10, combined=57, age-range 8-18), ADHD (n=144, age-range 11-28), and controls (n=191, age-range 8-26). The SNAP-IV and Conners rating scales were used to assess oppositional and ADHD traits. The Inventory of CU traits was used to assess CU traits. Decreased reward sensitivity was associated with ADHD symptom severity (p=0.018) if corrected for oppositional symptoms. ADHD symptomatology interacted with oppositional behavior on perseveration (p=0.019), with the former aggravating the effect of oppositional behavior on perseveration and vice versa. Within a pooled sample, reversal learning alterations were associated with the severity of ADHD symptoms, underpinned by hyposensitivity to reward and increased perseveration. These results show ADHD traits, as opposed to oppositional behavior and CU traits, is associated with decreased reward-based learning in adolescents and adults.© 2021, Christel M. Portengen, Emma Sprooten, Marcel P. Zwiers, Pieter J. Hoekstra, Andrea Dietrich, Nathalie E. Holz, Pascal M. Aggensteiner, Tobias Banaschewski, Ulrike M.E. Schulze, Melanie C. Saam, Michael C. Craig, Arjun Sethi, Paramala Santosh, Ilyas Sagar Ouriaghli, Josefina Castro-Fornieles, Mireia Rosa, Celso Arango, María José Penzol, Julia E. Werhahn, Daniel Brandeis Susanne Walitza, Marianne Oldehinkel, Barbara Franke, Jan K. Buitelaar, Jilly Naaijen. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. See http://creativecommons.org/licenses/by/4.0/

UR - https://kclpure.kcl.ac.uk/portal/en/publications/reward-and-punishment-sensitivity-are-associated-with-crossdisorder-traits(71f91ee0-0fbf-495b-a820-2390c3b3adae).html

U2 - 10.1016/j.psychres.2021.113795

DO - 10.1016/j.psychres.2021.113795

M3 - Article

SN - 0165-1781

JO - Psychiatry Research

JF - Psychiatry Research

ER -

Reward and Punishment Sensitivity are Associated with Cross-disorder Traits

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