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High‐precision voluntary movements are largely independent of preceding vertex potentials elicited by sudden sensory events

KEY POINTS: Salient and sudden sensory events generate a remarkably large response in the human brain, the vertex wave (VW). The VW is coupled with a modulation of a voluntarily‐applied isometric force. In the present study, we tested whether the VW is also related to executing high‐precision moveme...

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Autores principales: Kilintari, M., Bufacchi, R. J., Novembre, G., Guo, Y., Haggard, P., Iannetti, G. D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6092281/
https://www.ncbi.nlm.nih.gov/pubmed/29726629
http://dx.doi.org/10.1113/JP275715
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author Kilintari, M.
Bufacchi, R. J.
Novembre, G.
Guo, Y.
Haggard, P.
Iannetti, G. D.
author_facet Kilintari, M.
Bufacchi, R. J.
Novembre, G.
Guo, Y.
Haggard, P.
Iannetti, G. D.
author_sort Kilintari, M.
collection PubMed
description KEY POINTS: Salient and sudden sensory events generate a remarkably large response in the human brain, the vertex wave (VW). The VW is coupled with a modulation of a voluntarily‐applied isometric force. In the present study, we tested whether the VW is also related to executing high‐precision movements. The execution of a voluntary high‐precision movement remains relatively independent of the brain activity reflected by the preceding VW. The apparent relationship between the positive VW and movement onset time is explained by goal‐related but stimulus‐independent neural activities. These results highlight the need to consider such goal‐related but stimulus‐independent neural activities when attempting to relate event‐related potential amplitude with perceptual and behavioural performance. ABSTRACT: Salient and fast‐rising sensory events generate a large biphasic vertex wave (VW) in the human electroencephalogram (EEG). We recently reported that the VW is coupled with a modulation of concomitantly‐applied isometric force. In the present study, in five experiments, we tested whether the VW is also related to high‐precision visuomotor control. We obtained three results. First, the saliency‐induced increase in VW amplitude was paralleled by a modulation in two of the five extracted movement parameters: a reduction in the onset time of the voluntary movement (P < 0.005) and an increase in movement accuracy (P < 0.005). Second, spontaneous trial‐by‐trial variability in vertex wave amplitude, for a given level of stimulus saliency, was positively correlated with movement onset time (P < 0.001 in four out of five experiments). Third, this latter trial‐by‐trial correlation was explained by a widespread EEG negativity independent of the occurrence of the positive VW, although overlapping in time with it. These results indicate that (i) the execution of a voluntary high‐precision movement remains relatively independent of the neural processing reflected by the preceding VW, with (ii) the exception of movement onset time, for which saliency‐based contextual effects are dissociated from trial‐by‐trial effects. These results also indicate that (iii) attentional effects can produce spurious correlations between event‐related potentials (ERPs) and behavioural measures. Although sudden salient stimuli trigger characteristic EEG responses coupled with distinct reactive components within an ongoing isometric task, the results of the present study indicate that the execution of a subsequent voluntary movement appears largely protected from such saliency‐based modulation, with the exception of movement onset time.
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spelling pubmed-60922812018-08-20 High‐precision voluntary movements are largely independent of preceding vertex potentials elicited by sudden sensory events Kilintari, M. Bufacchi, R. J. Novembre, G. Guo, Y. Haggard, P. Iannetti, G. D. J Physiol Neuroscience KEY POINTS: Salient and sudden sensory events generate a remarkably large response in the human brain, the vertex wave (VW). The VW is coupled with a modulation of a voluntarily‐applied isometric force. In the present study, we tested whether the VW is also related to executing high‐precision movements. The execution of a voluntary high‐precision movement remains relatively independent of the brain activity reflected by the preceding VW. The apparent relationship between the positive VW and movement onset time is explained by goal‐related but stimulus‐independent neural activities. These results highlight the need to consider such goal‐related but stimulus‐independent neural activities when attempting to relate event‐related potential amplitude with perceptual and behavioural performance. ABSTRACT: Salient and fast‐rising sensory events generate a large biphasic vertex wave (VW) in the human electroencephalogram (EEG). We recently reported that the VW is coupled with a modulation of concomitantly‐applied isometric force. In the present study, in five experiments, we tested whether the VW is also related to high‐precision visuomotor control. We obtained three results. First, the saliency‐induced increase in VW amplitude was paralleled by a modulation in two of the five extracted movement parameters: a reduction in the onset time of the voluntary movement (P < 0.005) and an increase in movement accuracy (P < 0.005). Second, spontaneous trial‐by‐trial variability in vertex wave amplitude, for a given level of stimulus saliency, was positively correlated with movement onset time (P < 0.001 in four out of five experiments). Third, this latter trial‐by‐trial correlation was explained by a widespread EEG negativity independent of the occurrence of the positive VW, although overlapping in time with it. These results indicate that (i) the execution of a voluntary high‐precision movement remains relatively independent of the neural processing reflected by the preceding VW, with (ii) the exception of movement onset time, for which saliency‐based contextual effects are dissociated from trial‐by‐trial effects. These results also indicate that (iii) attentional effects can produce spurious correlations between event‐related potentials (ERPs) and behavioural measures. Although sudden salient stimuli trigger characteristic EEG responses coupled with distinct reactive components within an ongoing isometric task, the results of the present study indicate that the execution of a subsequent voluntary movement appears largely protected from such saliency‐based modulation, with the exception of movement onset time. John Wiley and Sons Inc. 2018-06-28 2018-08-15 /pmc/articles/PMC6092281/ /pubmed/29726629 http://dx.doi.org/10.1113/JP275715 Text en © 2018 The Authors. The Journal of Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Neuroscience
Kilintari, M.
Bufacchi, R. J.
Novembre, G.
Guo, Y.
Haggard, P.
Iannetti, G. D.
High‐precision voluntary movements are largely independent of preceding vertex potentials elicited by sudden sensory events
title High‐precision voluntary movements are largely independent of preceding vertex potentials elicited by sudden sensory events
title_full High‐precision voluntary movements are largely independent of preceding vertex potentials elicited by sudden sensory events
title_fullStr High‐precision voluntary movements are largely independent of preceding vertex potentials elicited by sudden sensory events
title_full_unstemmed High‐precision voluntary movements are largely independent of preceding vertex potentials elicited by sudden sensory events
title_short High‐precision voluntary movements are largely independent of preceding vertex potentials elicited by sudden sensory events
title_sort high‐precision voluntary movements are largely independent of preceding vertex potentials elicited by sudden sensory events
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6092281/
https://www.ncbi.nlm.nih.gov/pubmed/29726629
http://dx.doi.org/10.1113/JP275715
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