Modulation of error-sensitivity during a prism adaptation task in people with cerebellar degeneration
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 cerebe...
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Veröffentlicht in: | Journal of neurophysiology 2015-10, Vol.114 (4), p.2460-2471 |
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creator | 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 |
description | 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. |
doi_str_mv | 10.1152/jn.00145.2015 |
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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.</description><identifier>ISSN: 0022-3077</identifier><identifier>EISSN: 1522-1598</identifier><identifier>DOI: 10.1152/jn.00145.2015</identifier><identifier>PMID: 26311179</identifier><language>eng</language><publisher>United States: American Physiological Society</publisher><subject>Adaptation, Physiological - physiology ; Adaptation, Psychological - physiology ; Adult ; Aged ; Atrophy ; Cerebellar Ataxia - physiopathology ; Cerebellar Ataxia - psychology ; Computers ; Feedback, Psychological - physiology ; Feedback, Sensory - physiology ; Female ; Humans ; Learning - physiology ; Lenses ; Male ; Memory - physiology ; Middle Aged ; Motor Activity - physiology ; Nervous System Pathophysiology ; Photic Stimulation - methods ; Psychomotor Performance - physiology ; Spinocerebellar Degenerations - physiopathology ; Spinocerebellar Degenerations - psychology ; Visual Perception - physiology</subject><ispartof>Journal of neurophysiology, 2015-10, Vol.114 (4), p.2460-2471</ispartof><rights>Copyright © 2015 the American Physiological Society.</rights><rights>Copyright © 2015 the American Physiological Society 2015 American Physiological Society</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c387t-dac54f144d91c94e8418829aa2e964476198154f1a63757e632a026f79241ab53</citedby><cites>FETCH-LOGICAL-c387t-dac54f144d91c94e8418829aa2e964476198154f1a63757e632a026f79241ab53</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,3026,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26311179$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hanajima, Ritsuko</creatorcontrib><creatorcontrib>Shadmehr, Reza</creatorcontrib><creatorcontrib>Ohminami, Shinya</creatorcontrib><creatorcontrib>Tsutsumi, Ryosuke</creatorcontrib><creatorcontrib>Shirota, Yuichiro</creatorcontrib><creatorcontrib>Shimizu, Takahiro</creatorcontrib><creatorcontrib>Tanaka, Nobuyuki</creatorcontrib><creatorcontrib>Terao, Yasuo</creatorcontrib><creatorcontrib>Tsuji, Shoji</creatorcontrib><creatorcontrib>Ugawa, Yoshikazu</creatorcontrib><creatorcontrib>Uchimura, Motoaki</creatorcontrib><creatorcontrib>Inoue, Masato</creatorcontrib><creatorcontrib>Kitazawa, Shigeru</creatorcontrib><title>Modulation of error-sensitivity during a prism adaptation task in people with cerebellar degeneration</title><title>Journal of neurophysiology</title><addtitle>J Neurophysiol</addtitle><description>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.</description><subject>Adaptation, Physiological - physiology</subject><subject>Adaptation, Psychological - physiology</subject><subject>Adult</subject><subject>Aged</subject><subject>Atrophy</subject><subject>Cerebellar Ataxia - physiopathology</subject><subject>Cerebellar Ataxia - psychology</subject><subject>Computers</subject><subject>Feedback, Psychological - physiology</subject><subject>Feedback, Sensory - physiology</subject><subject>Female</subject><subject>Humans</subject><subject>Learning - physiology</subject><subject>Lenses</subject><subject>Male</subject><subject>Memory - physiology</subject><subject>Middle Aged</subject><subject>Motor Activity - physiology</subject><subject>Nervous System Pathophysiology</subject><subject>Photic Stimulation - methods</subject><subject>Psychomotor Performance - physiology</subject><subject>Spinocerebellar Degenerations - physiopathology</subject><subject>Spinocerebellar Degenerations - psychology</subject><subject>Visual Perception - physiology</subject><issn>0022-3077</issn><issn>1522-1598</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkU1P4zAQhi3ECgrLkSvykUuKx7Hj5IKEEOwisdrL7tlyk0nrktrBdor49yS0IDjNaObROx8vIefA5gCSX63dnDEQcs4ZyAMyG2s8A1mVh2TG2JjnTKljchLjmjGmJONH5JgXOQCoakbwj2-GziTrHfUtxRB8yCK6aJPd2vRKmyFYt6SG9sHGDTWN6dMOTyY-Uetoj77vkL7YtKI1Blxg15lAG1yiw_DO_iQ_WtNFPNvHU_L__u7f7e_s8e-vh9ubx6zOS5WyxtRStCBEU0FdCSwFlCWvjOFYFUKoAqoSJsIUuZIKi5wbxotWVVyAWcj8lFzvdPthscGmRpeC6fS4-saEV-2N1d87zq700m-1KMb3CRgFLvcCwT8PGJPe2FhPBzn0Q9SguJQgeD7NynZoHXyMAdvPMcD0ZI1eO_1ujZ6sGfmLr7t90h9e5G-1CIte</recordid><startdate>20151001</startdate><enddate>20151001</enddate><creator>Hanajima, Ritsuko</creator><creator>Shadmehr, Reza</creator><creator>Ohminami, Shinya</creator><creator>Tsutsumi, Ryosuke</creator><creator>Shirota, Yuichiro</creator><creator>Shimizu, Takahiro</creator><creator>Tanaka, Nobuyuki</creator><creator>Terao, Yasuo</creator><creator>Tsuji, Shoji</creator><creator>Ugawa, Yoshikazu</creator><creator>Uchimura, Motoaki</creator><creator>Inoue, Masato</creator><creator>Kitazawa, Shigeru</creator><general>American Physiological Society</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20151001</creationdate><title>Modulation of error-sensitivity during a prism adaptation task in people with cerebellar degeneration</title><author>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</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c387t-dac54f144d91c94e8418829aa2e964476198154f1a63757e632a026f79241ab53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Adaptation, Physiological - physiology</topic><topic>Adaptation, Psychological - physiology</topic><topic>Adult</topic><topic>Aged</topic><topic>Atrophy</topic><topic>Cerebellar Ataxia - physiopathology</topic><topic>Cerebellar Ataxia - psychology</topic><topic>Computers</topic><topic>Feedback, Psychological - physiology</topic><topic>Feedback, Sensory - physiology</topic><topic>Female</topic><topic>Humans</topic><topic>Learning - physiology</topic><topic>Lenses</topic><topic>Male</topic><topic>Memory - physiology</topic><topic>Middle Aged</topic><topic>Motor Activity - physiology</topic><topic>Nervous System Pathophysiology</topic><topic>Photic Stimulation - methods</topic><topic>Psychomotor Performance - physiology</topic><topic>Spinocerebellar Degenerations - physiopathology</topic><topic>Spinocerebellar Degenerations - psychology</topic><topic>Visual Perception - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hanajima, Ritsuko</creatorcontrib><creatorcontrib>Shadmehr, Reza</creatorcontrib><creatorcontrib>Ohminami, Shinya</creatorcontrib><creatorcontrib>Tsutsumi, Ryosuke</creatorcontrib><creatorcontrib>Shirota, Yuichiro</creatorcontrib><creatorcontrib>Shimizu, Takahiro</creatorcontrib><creatorcontrib>Tanaka, Nobuyuki</creatorcontrib><creatorcontrib>Terao, Yasuo</creatorcontrib><creatorcontrib>Tsuji, Shoji</creatorcontrib><creatorcontrib>Ugawa, Yoshikazu</creatorcontrib><creatorcontrib>Uchimura, Motoaki</creatorcontrib><creatorcontrib>Inoue, Masato</creatorcontrib><creatorcontrib>Kitazawa, Shigeru</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of neurophysiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hanajima, Ritsuko</au><au>Shadmehr, Reza</au><au>Ohminami, Shinya</au><au>Tsutsumi, Ryosuke</au><au>Shirota, Yuichiro</au><au>Shimizu, Takahiro</au><au>Tanaka, Nobuyuki</au><au>Terao, Yasuo</au><au>Tsuji, Shoji</au><au>Ugawa, Yoshikazu</au><au>Uchimura, Motoaki</au><au>Inoue, Masato</au><au>Kitazawa, Shigeru</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Modulation of error-sensitivity during a prism adaptation task in people with cerebellar degeneration</atitle><jtitle>Journal of neurophysiology</jtitle><addtitle>J Neurophysiol</addtitle><date>2015-10-01</date><risdate>2015</risdate><volume>114</volume><issue>4</issue><spage>2460</spage><epage>2471</epage><pages>2460-2471</pages><issn>0022-3077</issn><eissn>1522-1598</eissn><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.</abstract><cop>United States</cop><pub>American Physiological Society</pub><pmid>26311179</pmid><doi>10.1152/jn.00145.2015</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Adaptation, Physiological - physiology Adaptation, Psychological - physiology Adult Aged Atrophy Cerebellar Ataxia - physiopathology Cerebellar Ataxia - psychology Computers Feedback, Psychological - physiology Feedback, Sensory - physiology Female Humans Learning - physiology Lenses Male Memory - physiology Middle Aged Motor Activity - physiology Nervous System Pathophysiology Photic Stimulation - methods Psychomotor Performance - physiology Spinocerebellar Degenerations - physiopathology Spinocerebellar Degenerations - psychology Visual Perception - physiology |
title | Modulation of error-sensitivity during a prism adaptation task in people with cerebellar degeneration |
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