Neural correlates of sensorimotor adaptation: Thalamic contributions to learning from sensory prediction error

Understanding the neural mechanism of sensorimotor adaptation is essential to reveal how the brain learns from errors, a process driven by sensory prediction errors. While the previous literature has focused on cortical and cerebellar changes, the involvement of the thalamus has received less attent...

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Main Authors: Shirin Mahdavi, Axel Lindner, Carsten Schmidt-Samoa, Anna-Lena Müsch, Peter Dechent, Melanie Wilke
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:NeuroImage
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Online Access:http://www.sciencedirect.com/science/article/pii/S1053811924004245
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author Shirin Mahdavi
Axel Lindner
Carsten Schmidt-Samoa
Anna-Lena Müsch
Peter Dechent
Melanie Wilke
author_facet Shirin Mahdavi
Axel Lindner
Carsten Schmidt-Samoa
Anna-Lena Müsch
Peter Dechent
Melanie Wilke
author_sort Shirin Mahdavi
collection DOAJ
description Understanding the neural mechanism of sensorimotor adaptation is essential to reveal how the brain learns from errors, a process driven by sensory prediction errors. While the previous literature has focused on cortical and cerebellar changes, the involvement of the thalamus has received less attention. This functional magnetic resonance imaging study aims to explore the neural substrates of learning from sensory prediction errors with an additional focus on the thalamus. Thirty participants adapted their goal-directed reaches to visual feedback rotations introduced in a step-wise manner, while reporting their predicted visual consequences of their movements intermittently. We found that adaptation initially engaged the cerebellum and fronto-parietal cortical regions, which persisted as adaptation progressed. By the end of adaptation, additional regions within the fronto-parietal cortex and medial pulvinar of the thalamus were recruited. Another finding was the involvement of bilateral medial dorsal nuclei, which showed a positive correlation with the level of motor adaptation. Notably, the gradual shift in the predicted hand movement consequences was associated with activity in the cerebellum, motor cortex and thalamus (ventral lateral, medial dorsal, and medial pulvinar). Our study presents clear evidence for an involvement of the thalamus, both classical ‘motor’ and higher-order nuclei, in error-based motor learning.
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spelling doaj-art-2896df7362b34bef839946a7956c1cfc2025-08-20T02:49:05ZengElsevierNeuroImage1095-95722024-12-0130312092710.1016/j.neuroimage.2024.120927Neural correlates of sensorimotor adaptation: Thalamic contributions to learning from sensory prediction errorShirin Mahdavi0Axel Lindner1Carsten Schmidt-Samoa2Anna-Lena Müsch3Peter Dechent4Melanie Wilke5Department of Cognitive Neurology, University Medicine Göttingen, Göttingen, GermanyHertie-Institute for Clinical Brain Research, Division of Neuropsychology, University of Tübingen, Tübingen, Germany; Tübingen Center for Mental Health, Department of Psychiatry and Psychotherapy, University of Tübingen, Tübingen, GermanyDepartment of Cognitive Neurology, University Medicine Göttingen, Göttingen, Germany; MR-Research in Neurosciences, University Medicine Göttingen, Göttingen, GermanyDepartment of Cognitive Neurology, University Medicine Göttingen, Göttingen, GermanyDepartment of Cognitive Neurology, University Medicine Göttingen, Göttingen, Germany; MR-Research in Neurosciences, University Medicine Göttingen, Göttingen, GermanyDepartment of Cognitive Neurology, University Medicine Göttingen, Göttingen, Germany; Cognitive Neurology Group, Department of Cognitive Neuroscience, German Primate Center, Leibniz Institute for Primate Research, Göttingen, Germany; Corresponding author at: Department of Cognitive Neurology, Heart & Brain Center, University Medicine Göttingen, Robert-Koch-Strasse 42, Göttingen 37075, Germany.Understanding the neural mechanism of sensorimotor adaptation is essential to reveal how the brain learns from errors, a process driven by sensory prediction errors. While the previous literature has focused on cortical and cerebellar changes, the involvement of the thalamus has received less attention. This functional magnetic resonance imaging study aims to explore the neural substrates of learning from sensory prediction errors with an additional focus on the thalamus. Thirty participants adapted their goal-directed reaches to visual feedback rotations introduced in a step-wise manner, while reporting their predicted visual consequences of their movements intermittently. We found that adaptation initially engaged the cerebellum and fronto-parietal cortical regions, which persisted as adaptation progressed. By the end of adaptation, additional regions within the fronto-parietal cortex and medial pulvinar of the thalamus were recruited. Another finding was the involvement of bilateral medial dorsal nuclei, which showed a positive correlation with the level of motor adaptation. Notably, the gradual shift in the predicted hand movement consequences was associated with activity in the cerebellum, motor cortex and thalamus (ventral lateral, medial dorsal, and medial pulvinar). Our study presents clear evidence for an involvement of the thalamus, both classical ‘motor’ and higher-order nuclei, in error-based motor learning.http://www.sciencedirect.com/science/article/pii/S1053811924004245fMRIMotor learningSensory prediction errorThalamusVisuomotor adaptation
spellingShingle Shirin Mahdavi
Axel Lindner
Carsten Schmidt-Samoa
Anna-Lena Müsch
Peter Dechent
Melanie Wilke
Neural correlates of sensorimotor adaptation: Thalamic contributions to learning from sensory prediction error
NeuroImage
fMRI
Motor learning
Sensory prediction error
Thalamus
Visuomotor adaptation
title Neural correlates of sensorimotor adaptation: Thalamic contributions to learning from sensory prediction error
title_full Neural correlates of sensorimotor adaptation: Thalamic contributions to learning from sensory prediction error
title_fullStr Neural correlates of sensorimotor adaptation: Thalamic contributions to learning from sensory prediction error
title_full_unstemmed Neural correlates of sensorimotor adaptation: Thalamic contributions to learning from sensory prediction error
title_short Neural correlates of sensorimotor adaptation: Thalamic contributions to learning from sensory prediction error
title_sort neural correlates of sensorimotor adaptation thalamic contributions to learning from sensory prediction error
topic fMRI
Motor learning
Sensory prediction error
Thalamus
Visuomotor adaptation
url http://www.sciencedirect.com/science/article/pii/S1053811924004245
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