On the Effects of Impulsivity and Compulsivity on Neural Correlates of Model-based Performance

Overview

Journal Sci Rep

Specialty Science

Date 2024 Sep 10

PMID 39256477

Authors

Kerstin Duck

Raoul Wullhorst

Rebecca Overmeyer

Tanja Endrass

Affiliations

Soon will be listed here.

Abstract

Impaired goal-directed behavior is associated with a range of mental disorders, implicating underlying transdiagnostic factors. While compulsivity has been linked to reduced model-based (MB) control, impulsivity has rarely been studied in the context of reinforcement learning despite its links to reward processing and cognitive control. This study investigated the neural mechanisms underlying MB control and the influence of impulsivity and compulsivity, using EEG data from 238 individuals during a two-step decision making task. Single-trial analyses revealed a modulation of the feedback-related negativity (FRN), where amplitudes were higher after common transitions and positive reward prediction error (RPE), indicating a valence effect. Meanwhile, enhanced P3 amplitudes after rare transitions and both positive and negative RPE possibly reflect surprise. In a second step, we regressed the mean b values of the effect of RPE on the EEG signals onto self-reported impulsivity and compulsivity and behavioral MB control (w). The effect of RPE on FRN-related activity was mainly associated with higher w scores, linking the FRN to MB control. Crucially, the modulation of the P3 by RPE was negatively associated with compulsivity, pointing to a deficient mental model in highly compulsive individuals.

References

Hoptman M . Impulsivity and aggression in schizophrenia: a neural circuitry perspective with implications for treatment. CNS Spectr. 2015; 20(3):280-6. PMC: 4441843. DOI: 10.1017/S1092852915000206. View

Doll B, Simon D, Daw N . The ubiquity of model-based reinforcement learning. Curr Opin Neurobiol. 2012; 22(6):1075-81. PMC: 3513648. DOI: 10.1016/j.conb.2012.08.003. View

Jimura K, Chushak M, Braver T . Impulsivity and self-control during intertemporal decision making linked to the neural dynamics of reward value representation. J Neurosci. 2013; 33(1):344-57. PMC: 3711626. DOI: 10.1523/JNEUROSCI.0919-12.2013. View

Kool W, Cushman F, Gershman S . When Does Model-Based Control Pay Off?. PLoS Comput Biol. 2016; 12(8):e1005090. PMC: 5001643. DOI: 10.1371/journal.pcbi.1005090. View

Polich J . Updating P300: an integrative theory of P3a and P3b. Clin Neurophysiol. 2007; 118(10):2128-48. PMC: 2715154. DOI: 10.1016/j.clinph.2007.04.019. View

Gonner S, Leonhart R, Ecker W . [The German version of the obsessive-compulsive inventory-revised: a brief self-report measure for the multidimensional assessment of obsessive-compulsive symptoms]. Psychother Psychosom Med Psychol. 2007; 57(9-10):395-404. DOI: 10.1055/s-2007-970894. View

Dayan P, Niv Y . Reinforcement learning: the good, the bad and the ugly. Curr Opin Neurobiol. 2008; 18(2):185-96. DOI: 10.1016/j.conb.2008.08.003. View

Dir A, Coskunpinar A, Cyders M . A meta-analytic review of the relationship between adolescent risky sexual behavior and impulsivity across gender, age, and race. Clin Psychol Rev. 2014; 34(7):551-62. DOI: 10.1016/j.cpr.2014.08.004. View

Donamayor N, Ebrahimi C, Arndt V, Weiss F, Schlagenhauf F, Endrass T . Goal-Directed and Habitual Control in Human Substance Use: State of the Art and Future Directions. Neuropsychobiology. 2022; 81(5):403-417. DOI: 10.1159/000527663. View

10.

Gu R, Feng X, Broster L, Yuan L, Xu P, Luo Y . Valence and magnitude ambiguity in feedback processing. Brain Behav. 2017; 7(5):e00672. PMC: 5434181. DOI: 10.1002/brb3.672. View

11.

Culbreth A, Westbrook A, Daw N, Botvinick M, Barch D . Reduced model-based decision-making in schizophrenia. J Abnorm Psychol. 2016; 125(6):777-787. PMC: 4980177. DOI: 10.1037/abn0000164. View

12.

Wurm F, Ernst B, Steinhauser M . The influence of internal models on feedback-related brain activity. Cogn Affect Behav Neurosci. 2020; 20(5):1070-1089. PMC: 7497542. DOI: 10.3758/s13415-020-00820-6. View

13.

Zuhlsdorff K, Lopez-Cruz L, Dutcher E, Jones J, Pama C, Sawiak S . Sex-dependent effects of early life stress on reinforcement learning and limbic cortico-striatal functional connectivity. Neurobiol Stress. 2022; 22:100507. PMC: 9731893. DOI: 10.1016/j.ynstr.2022.100507. View

14.

Cools R, Blackwell A, Clark L, Menzies L, Cox S, Robbins T . Tryptophan depletion disrupts the motivational guidance of goal-directed behavior as a function of trait impulsivity. Neuropsychopharmacology. 2005; 30(7):1362-73. DOI: 10.1038/sj.npp.1300704. View

15.

Petzold J, Kienast A, Lee Y, Pooseh S, London E, Goschke T . Baseline impulsivity may moderate L-DOPA effects on value-based decision-making. Sci Rep. 2019; 9(1):5652. PMC: 6449394. DOI: 10.1038/s41598-019-42124-x. View

16.

Liu C, Rotaru K, Chamberlain S, Yucel M, Grant J, Lee R . Distress-driven impulsivity interacts with trait compulsivity in association with problematic drinking: A two-sample study. Front Psychiatry. 2022; 13:938275. PMC: 9530652. DOI: 10.3389/fpsyt.2022.938275. View

17.

Cyders M . Impulsivity and the sexes: measurement and structural invariance of the UPPS-P Impulsive Behavior Scale. Assessment. 2011; 20(1):86-97. DOI: 10.1177/1073191111428762. View

18.

Rommerskirchen L, Lange L, Osinsky R . The reward positivity reflects the integrated value of temporally threefold-layered decision outcomes. Psychophysiology. 2021; 58(5):e13789. DOI: 10.1111/psyp.13789. View

19.

Gillan C, Kalanthroff E, Evans M, Weingarden H, Jacoby R, Gershkovich M . Comparison of the Association Between Goal-Directed Planning and Self-reported Compulsivity vs Obsessive-Compulsive Disorder Diagnosis. JAMA Psychiatry. 2019; 77(1):77-85. PMC: 6802255. DOI: 10.1001/jamapsychiatry.2019.2998. View

20.

Sebold M, Deserno L, Nebe S, Nebe S, Schad D, Garbusow M . Model-based and model-free decisions in alcohol dependence. Neuropsychobiology. 2014; 70(2):122-31. DOI: 10.1159/000362840. View