Somatosensory electrical stimulation improves skill acquisition, consolidation, and transfer by increasing sensorimotor activity and connectivity

Author:

Veldman Menno P.1,Maurits Natasha M.23,Zijdewind Inge4ORCID,Maffiuletti Nicola A.5,van Middelkoop Stella1,Mizelle J. Chris6ORCID,Hortobágyi Tibor1

Affiliation:

1. University of Groningen, University Medical Center Groningen, Center for Human Movement Sciences, Groningen, The Netherlands

2. Department of Neurology, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands

3. University of Groningen, Neuroimaging Center, Groningen, The Netherlands

4. Department of Neuroscience, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands

5. Schulthess Klinik, Human Performance Lab, Zürich, Switzerland

6. Department of Kinesiology, East Carolina University, Greenville, North Carolina

Abstract

The interaction between the somatosensory and motor systems is important for normal human motor function and learning. Enhancing somatosensory input using somatosensory electrical stimulation (SES) can increase motor performance, but the neuronal mechanisms underlying these effects are largely unknown. With EEG, we examined whether skill acquisition, consolidation, and interlimb transfer after SES was related to increased activity in sensorimotor regions, as assessed by the N30 somatosensory evoked potential or rather increased connectivity between these regions, as assessed by the phase slope index (PSI). Right- and left-hand motor performance and EEG measures were taken before, immediately after, and 24 h ( day 2) after either SES ( n = 12; 5 men) or Control ( n = 12; 5 men). The results showed skill acquisition and consolidation in the stimulated right hand immediately after SES (6%) and on day 2 (9%) and interlimb transfer to the nonstimulated left hand on day 2 relative to Control (8%, all P < 0.05). Increases in N30 amplitudes correlated with skill acquisition while PSI from electrodes that represent the posterior parietal and primary somatosensory cortex to the electrode representing the primary motor cortex correlated with skill consolidation. In contrast, interlimb transfer did not correlate with the EEG-derived neurophysiological estimates obtained in the present study, which may indicate the involvement of subcortical structures in interlimb transfer after SES. In conclusion, weak peripheral somatosensory inputs in the form of SES improve skill acquisition, consolidation, and interlimb transfer that coincide with different cortical adaptations, including enhanced N30 amplitudes and PSI.NEW & NOTEWORTHY The relationship between adaptations in synaptic plasticity and motor learning following somatosensory electrical stimulation (SES) is incompletely understood. Here, we used for the first time a multifactorial approach that examined skill acquisition, consolidation, and interlimb transfer following 20 min of SES. In addition, we quantified sensorimotor integration and the magnitude and direction of connectivity with EEG. Following artificial electrical stimulation, increases in sensorimotor integration and connectivity were found to correlate with skill acquisition and consolidation, respectively.

Publisher

American Physiological Society

Subject

Physiology,General Neuroscience

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