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

IF 3.4 2区 医学 Q2 NEUROIMAGING Neuroimage-Clinical Pub Date : 2024-01-01 DOI:10.1016/j.nicl.2024.103588
Hans-Christoph Aster , Maria Waltmann , Anika Busch , Marcel Romanos , Matthias Gamer , Betteke Maria van Noort , Anne Beck , Viola Kappel , Lorenz Deserno
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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.

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多动症患者的灵活奖赏学习能力受损与强化敏感性降低以及腹侧纹状体和顶叶皮层的神经信号有关
基于奖赏的学习和决策是理解注意力缺陷多动障碍(ADHD)症状的主要候选方法。然而,关于多动症的神经计算基础,目前只有有限的证据。这涉及到在动态变化的环境中灵活的行为适应能力,而这对多动症患者来说具有挑战性。之前的一项研究指出,青少年多动症患者的选择转换能力增强,同时内侧前额叶皮层的学习信号也受到干扰。
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来源期刊
Neuroimage-Clinical
Neuroimage-Clinical NEUROIMAGING-
CiteScore
7.50
自引率
4.80%
发文量
368
审稿时长
52 days
期刊介绍: NeuroImage: Clinical, a journal of diseases, disorders and syndromes involving the Nervous System, provides a vehicle for communicating important advances in the study of abnormal structure-function relationships of the human nervous system based on imaging. The focus of NeuroImage: Clinical is on defining changes to the brain associated with primary neurologic and psychiatric diseases and disorders of the nervous system as well as behavioral syndromes and developmental conditions. The main criterion for judging papers is the extent of scientific advancement in the understanding of the pathophysiologic mechanisms of diseases and disorders, in identification of functional models that link clinical signs and symptoms with brain function and in the creation of image based tools applicable to a broad range of clinical needs including diagnosis, monitoring and tracking of illness, predicting therapeutic response and development of new treatments. Papers dealing with structure and function in animal models will also be considered if they reveal mechanisms that can be readily translated to human conditions.
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