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Impaired flexible reward learning in ADHD patients is associated with blunted reinforcement sensitivity and neural signals in ventral striatum and parietal cortex

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Waltmann,  Maria       
Department of Child and Adolescent Psychiatry, Psychotherapy and Psychosomatics, University Hospital Würzburg, Germany;
Department Neurology, MPI for Human Cognitive and Brain Sciences, Max Planck Society;

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Deserno,  Lorenz       
Department of Child and Adolescent Psychiatry, Psychotherapy and Psychosomatics, University Hospital Würzburg, Germany;
Department Neurology, MPI for Human Cognitive and Brain Sciences, Max Planck Society;
Department of Psychiatry and Psychotherapy, TU Dresden, Germany;

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Citation

Aster, H.-C., Waltmann, M., Busch, A., Romanos, M., Gamer, M., Maria van Noort, B., et al. (2024). Impaired flexible reward learning in ADHD patients is associated with blunted reinforcement sensitivity and neural signals in ventral striatum and parietal cortex. NeuroImage: Clinical, 42: 103588. doi:10.1016/j.nicl.2024.103588.


Cite as: https://hdl.handle.net/21.11116/0000-000E-A5B5-B
Abstract
Reward-based learning and decision-making are prime candidates to understand symptoms of attention deficit hyperactivity disorder (ADHD). However, only limited evidence is available regarding the neurocomputational underpinnings of the alterations seen in ADHD. This concerns flexible behavioral adaption in dynamically changing environments, which is challenging for individuals with ADHD. One previous study points to elevated choice switching in adolescent ADHD, which was accompanied by disrupted learning signals in medial prefrontal cortex.

Here, we investigated young adults with ADHD (n = 17) as compared to age- and sex-matched controls (n = 17) using a probabilistic reversal learning experiment during functional magnetic resonance imaging (fMRI). The task requires continuous learning to guide flexible behavioral adaptation to changing reward contingencies. To disentangle the neurocomputational underpinnings of the behavioral data, we used reinforcement learning (RL) models, which informed the analysis of fMRI data.

ADHD patients performed worse than controls particularly in trials before reversals, i.e., when reward contingencies were stable. This pattern resulted from ‘noisy’ choice switching regardless of previous feedback. RL modelling showed decreased reinforcement sensitivity and enhanced learning rates for negative feedback in ADHD patients. At the neural level, this was reflected in a diminished representation of choice probability in the left posterior parietal cortex in ADHD. Moreover, modelling showed a marginal reduction of learning about the unchosen option, which was paralleled by a marginal reduction in learning signals incorporating the unchosen option in the left ventral striatum.

Taken together, we show that impaired flexible behavior in ADHD is due to excessive choice switching (‘hyper-flexibility’), which can be detrimental or beneficial depending on the learning environment. Computationally, this resulted from blunted sensitivity to reinforcement of which we detected neural correlates in the attention-control network, specifically in the parietal cortex. These neurocomputational findings remain preliminary due to the relatively small sample size.