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Age-related changes in the bimanual advantage and in brain oscillatory activity during tapping movements suggest a decline in processing sensory reafference

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Abstract

Deficits in the processing of sensory reafferences have been suggested as accounting for age-related decline in motor coordination. Whether sensory reafferences are accurately processed can be assessed based on the bimanual advantage in tapping: because of tapping with an additional hand increases kinesthetic reafferences, bimanual tapping is characterized by a reduced inter-tap interval variability than unimanual tapping. A suppression of the bimanual advantage would thus indicate a deficit in sensory reafference. We tested whether elderly indeed show a reduced bimanual advantage by measuring unimanual (UM) and bimanual (BM) self-paced tapping performance in groups of young (n = 29) and old (n = 27) healthy adults. Electroencephalogram was recorded to assess the underlying patterns of oscillatory activity, a neurophysiological mechanism advanced to support the integration of sensory reafferences. Behaviorally, there was a significant interaction between the factors tapping condition and age group at the level of the inter-tap interval variability, driven by a lower variability in BM than UM tapping in the young, but not in the elderly group. This result indicates that in self-paced tapping, the bimanual advantage is absent in elderly. Electrophysiological results revealed an interaction between tapping condition and age group on low beta band (14–20 Hz) activity. Beta activity varied depending on the tapping condition in the elderly but not in the young group. Source estimations localized this effect within left superior parietal and left occipital areas. We interpret our results in terms of engagement of different mechanisms in the elderly depending on the tapping mode: a ‘kinesthetic’ mechanism for UM and a ‘visual imagery’ mechanism for BM tapping movement.

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Acknowledgments

This work was supported by a grant from the Rhône-Alpes Region to ES, CL, MPD and JB (Research Cluster Fund No. 08 013981 01) and from the Swiss National Science Foundation to LS (#320030_143348). Cartool software (http://sites.google.com/site/fbmlab/cartool) has been programmed by Denis Brunet, from the Functional Brain Mapping Laboratory, Geneva, Switzerland, and supported by the Center for Biomedical Imaging (CIBM) of Geneva and Lausanne. Recordings were performed in the Laboratory for Experimental Research on Behavior (www.unil.ch/lerb) at the University of Lausanne, Switzerland, and at the Faculty of Psychology and Educational Sciences at the University of Geneva, Switzerland (www.unige.ch/fapse). The authors wish to thank Fosco Bernarsconi for his assistance with the analyses and the volunteers for their participation.

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Authors and Affiliations

  1. Institute of Sport Sciences (GRISSUL), University of Lausanne, Quartier UNIL-Mouline, Bâtiment Géopolis, 1015, Lausanne, Switzerland

    Etienne Sallard & Jérôme Barral

  2. Neurology Unit, Department of Medicine, Faculty of Sciences, University of Fribourg, 1700, Fribourg, Switzerland

    Lucas Spierer

  3. Faculty of Psychology and Educational Sciences, Center for the Interdisciplinary Study of Gerontology and Vulnerability, University of Geneva, Geneva, Switzerland

    Catherine Ludwig

  4. Faculty of Medicine, INSERM U1039, La Tronche, France

    Marie-Pierre Deiber

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  1. Etienne Sallard
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  2. Lucas Spierer
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  3. Catherine Ludwig
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Correspondence to Etienne Sallard.

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Sallard, E., Spierer, L., Ludwig, C. et al. Age-related changes in the bimanual advantage and in brain oscillatory activity during tapping movements suggest a decline in processing sensory reafference. Exp Brain Res 232, 469–479 (2014). https://doi.org/10.1007/s00221-013-3754-3

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