Impaired implicit learning and feedback processing after stroke

Abstract

The ability to learn is assumed to support successful recovery and rehabilitation therapy after stroke. Hence, learning impairments may reduce the recovery potential. Here, the hypothesis is tested that stroke survivors have deficits in feedback-driven implicit learning. Stroke survivors (n=30) and healthy age-matched control subjects (n=21) learned a probabilistic classification task with brain activation measured using functional magnetic resonance imaging in a subset of these individuals (17 stroke and 10 controls). Stroke subjects learned slower than controls to classify cues. After being rewarded with a smiley face, they were less likely to give the same response when the cue was repeated. Stroke subjects showed reduced brain activation in putamen, pallidum, thalamus, frontal and prefrontal cortices and cerebellum when compared with controls. Lesion analysis identified those stroke survivors as learning-impaired who had lesions in frontal areas, putamen, thalamus, caudate and insula. Lesion laterality had no effect on learning efficacy or brain activation. These findings suggest that stroke survivors have deficits in reinforcement learning that may be related to dysfunctional processing of feedback-based decision-making, reward signals and working memory. AbstractThe ability to learn is assumed to support successful recovery and rehabilitation therapy after stroke. Hence, learning impairments may reduce the recovery potential.Here, the hypothesis is tested that stroke survivors have deficits in feedback-driven implicit learning. Stroke survivors (n=30) and healthy age-matched control subjects (n=21) learned a probabilistic classification task with brain activation measured using functional magnetic resonance imaging in a subset of these individuals (17 stroke and 10 controls). Stroke subjects learned slower than controls to classify cues. After being rewarded with a smiley face, they were less likely to give the same response when the cue was repeated. Stroke subjects showed reduced brain activation in putamen, pallidum, thalamus, frontal and prefrontal cortices and cerebellum when compared with controls. Lesion analysis identified those stroke survivors as learningimpaired who had lesions in frontal areas, putamen, thalamus, caudate and insula.Lesion laterality had no effect on learning efficacy or brain activation. These findings suggest that stroke survivors have deficits in reinforcement learning that may be related to dysfunctional processing of feedback-based decision-making, reward signals and working memory.

Reward network dysfunction is associated with cognitive impairment after stroke

“…Therefore, we additionally investigated the extent to which reinforcement learning ability is preserved in stroke patients, specifically, whether this ability depended on reward system functionality. In the analysis of the learning rate between the blocks of the MID, severe learning deficits were found in the stroke group compared to the control group ( Boyd et al, 2009 , Lam et al, 2016 ) ( Fig. 4 C, 4F).…”

“…However, the impairments in learning processes detected in this study cannot be explained by the previously described lesion pattern. Learning deficits in stroke patients have recently been shown to be independent from lesion localization and affected hemisphere ( Lam et al, 2016 , Marsh et al, 2020 , Marsh et al, 2022 ). This is supported by the fact that impairments identified herein go beyond pure motor learning skills.…”

“…A crucial factor for effective rehabilitation outcome of stroke patients is the preserved motor learning ability ( Dahms et al, 2020 , Kitago and Krakauer, 2013 , Krakauer, 2006 , Lam et al, 2016 ). Several studies have shown that learning tasks performed under reward conditions substantially improve motor learning adaptation in stroke patients ( Lam et al, 2016 , Quattrocchi et al, 2017 , Subramanian et al, 2010 , van Vliet and Wulf, 2006 ).…”

Effects of virtual reality‐based cognitive interventions on cognitive function and activity of daily living among stroke patients: Systematic review and meta‐analysis

“…Stroke rehabilitation is a long‐term process for both physical and psychological adaptation; it takes time for the participants not only to gain familiarity with the changed body but also to accept the subsequent daily impacts and practical help (Dworzynski et al., 2015). Prolonged rehabilitation is expected, especially when cognitive impairments further compromise their learning capacities (Lam et al., 2016). More studies with longer intervention duration incorporating ADL components are needed to generalize improvement to everyday functioning.…”

Endogenous dopamine transmission is crucial for motor skill recovery after stroke

“…These results suggest that stroke is associated with dysfunction of the dopaminergic system whichmust have functional consequences. It may explain why implicit learning is impaired after stroke in humans ( Lam et al, 2016 ). In mice, stroke impaired motivation in a lever-pressing task and reduced the incentive value of reward ( Linden et al, 2015 ).…”