The effect of Parkinson's disease and Huntington's disease on human visuomotor learning

• Published in: The European journal of neuroscience Vol. 38; no. 6; pp. 2933 - 2940
• Main Authors: Gutierrez-Garralda, Juan Manuel, Moreno-Briseño, Pablo, Boll, Marie-Catherine, Morgado-Valle, Consuelo, Campos-Romo, Aurelio, Diaz, Rosalinda, Fernandez-Ruiz, Juan
• Format: Journal Article
• Language: English
• Published: Oxford Blackwell Publishing Ltd 01.09.2013; Blackwell
• Subjects: Adult; Adult and adolescent clinical studies; basal ganglia; Basal Ganglia - physiopathology; Biological and medical sciences; cerebellum; Degenerative and inherited degenerative diseases of the nervous system. Leukodystrophies. Prion diseases; Female; Humans; Huntington Disease - physiopathology; Huntington's disease; Learning - physiology; learning dissociation; Male; Medical sciences; Middle Aged; Neurology; Organic mental disorders. Neuropsychology; Parkinson Disease - physiopathology; Parkinson's disease; Psychology. Psychoanalysis. Psychiatry; Psychomotor Performance; Psychopathology. Psychiatry; sensorimotor learning; Cerebellum; Human; Nervous system diseases; Parkinson's disease; basal ganglia; Central nervous system; Huntington disease; Parkinson disease; learning dissociation; Basal ganglion; Huntington's disease; Encephalon; Genetic disease; Cerebral disorder; Learning; Acquisition process; Central nervous system disease; Degenerative disease; sensorimotor learning; Extrapyramidal syndrome; cerebellum
• ISSN: 0953-816X; 1460-9568
• DOI: 10.1111/ejn.12288

Visuomotor adaptation is often driven by error‐based (EB) learning in which signed errors update motor commands. There are, however, visuomotor tasks where signed errors are unavailable or cannot be mapped onto appropriate motor command changes, rendering EB learning ineffective; and yet, healthy subjects can learn in these EB learning‐free conditions. While EB learning depends on cerebellar integrity, the neural bases of EB‐independent learning are poorly understood. As basal ganglia are involved in learning mechanisms that are independent of signed error feedback, here we tested whether patients with basal ganglia lesions, including those with Huntington's disease and Parkinson's disease, would show impairments in a visuomotor learning task that prevents the use of EB learning. We employed two visuomotor throwing tasks that were similar, but were profoundly different in the resulting visual feedback. This difference was implemented through the introduction of either a lateral displacement of the visual field via a wedge prism (EB learning) or a horizontal reversal of the visual field via a dove prism (non‐EB learning). Our results show that patients with basal ganglia degeneration had normal EB learning in the wedge prism task, but were profoundly impaired in the reversing prism task that does not depend on the signed error signal feedback. These results represent the first evidence that human visuomotor learning in the absence of EB feedback depends on the integrity of the basal ganglia. Error‐based learning models cannot fully explain human visuomotor learning. (A) We have suggested that it can be dissociated in one dependent on error signal feedback and another that can lead to improvement without using the error signal. Here we tested in Huntington's disease and Parkinson's disease patients if basal ganglia lesions disrupt non‐error based sensorimotor learning while leaving error‐based learning unaffected. (B) The results show a dissociation between their normal performance on error‐based learning and the impaired performance on the non‐error based learning.