Modulation of error-sensitivity during a prism adaptation task in people with cerebellar degeneration

Ritsuko Hanajima, Reza Shadmehr, Shinya Ohminami, Ryosuke Tsutsumi, Yuichiro Shirota, Takahiro Shimizu, Nobuyuki Tanaka, Yasuo Terao, Shoji Tsuji, Yoshikazu Ugawa, Motoaki Uchimura, Masato Inoue, Shigeru Kitazawa

Research output: Contribution to journalArticle

Abstract

Cerebellar damage can profoundly impair human motor adaptation. For example, if reaching movements are perturbed abruptly, cerebellar damage impairs the ability to learn from the perturbation-induced errors. Interestingly, if the perturbation is imposed gradually over many trials, people with cerebellar damage may exhibit improved adaptation. However, this result is controversial, since the differential effects of gradual vs. abrupt protocols have not been observed in all studies. To examine this question, we recruited patients with pure cerebellar ataxia due to cerebellar cortical atrophy (n = 13) and asked them to reach to a target while viewing the scene through wedge prisms. The prisms were computer controlled, making it possible to impose the full perturbation abruptly in one trial, or build up the perturbation gradually over many trials. To control visual feedback, we employed shutter glasses that removed visual feedback during the reach, allowing us to measure trial-by-trial learning from error (termed error-sensitivity), and trial-by-trial decay of motor memory (termed forgetting). We found that the patients benefited significantly from the gradual protocol, improving their performance with respect to the abrupt protocol by exhibiting smaller errors during the exposure block, and producing larger aftereffects during the postexposure block. Trial-by-trial analysis suggested that this improvement was due to increased error-sensitivity in the gradual protocol. Therefore, cerebellar patients exhibited an improved ability to learn from error if they experienced those errors gradually. This improvement coincided with increased error-sensitivity and was present in both groups of subjects, suggesting that control of error-sensitivity may be spared despite cerebellar damage.

Original languageEnglish (US)
Pages (from-to)2460-2471
Number of pages12
JournalJournal of Neurophysiology
Volume114
Issue number4
DOIs
StatePublished - Aug 26 2015

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Sensory Feedback
Aptitude
Cerebellar Ataxia
Atrophy
Glass
Learning

Keywords

  • Cerebellar cortex
  • Cerebellum
  • Degenerative ataxia

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

Cite this

Modulation of error-sensitivity during a prism adaptation task in people with cerebellar degeneration. / Hanajima, Ritsuko; Shadmehr, Reza; Ohminami, Shinya; Tsutsumi, Ryosuke; Shirota, Yuichiro; Shimizu, Takahiro; Tanaka, Nobuyuki; Terao, Yasuo; Tsuji, Shoji; Ugawa, Yoshikazu; Uchimura, Motoaki; Inoue, Masato; Kitazawa, Shigeru.

In: Journal of Neurophysiology, Vol. 114, No. 4, 26.08.2015, p. 2460-2471.

Research output: Contribution to journalArticle

Hanajima, R, Shadmehr, R, Ohminami, S, Tsutsumi, R, Shirota, Y, Shimizu, T, Tanaka, N, Terao, Y, Tsuji, S, Ugawa, Y, Uchimura, M, Inoue, M & Kitazawa, S 2015, 'Modulation of error-sensitivity during a prism adaptation task in people with cerebellar degeneration', Journal of Neurophysiology, vol. 114, no. 4, pp. 2460-2471. https://doi.org/10.1152/jn.00145.2015
Hanajima, Ritsuko ; Shadmehr, Reza ; Ohminami, Shinya ; Tsutsumi, Ryosuke ; Shirota, Yuichiro ; Shimizu, Takahiro ; Tanaka, Nobuyuki ; Terao, Yasuo ; Tsuji, Shoji ; Ugawa, Yoshikazu ; Uchimura, Motoaki ; Inoue, Masato ; Kitazawa, Shigeru. / Modulation of error-sensitivity during a prism adaptation task in people with cerebellar degeneration. In: Journal of Neurophysiology. 2015 ; Vol. 114, No. 4. pp. 2460-2471.
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