Elite competitive swimmers exhibit higher motor cortical inhibition and superior sensorimotor skills in a water environment
Introduction
Practicing sensorimotor tasks leads to substantive structural [1,2] and functional [3,4] changes in the brain. These long-term experiment-related neurophysiological changes in the motor system are induced by specific physical activity [5], observation [6], and mental practice [7]. For example, long-term motor training in elite basketball players leads to cortical changes. Specifically, studies have reported that the activity in the inferior parietal lobule and inferior frontal gyrus in elite basketball players is higher than that in novices [8]. Our previous study also revealed that the somatosensory processing in sensorimotor cortical areas and reaction time for sensorimotor input were faster in expert baseball players than those in novices [9]. The results from these studies suggest that cortical reorganization and processing in various motor-related cortical areas occur in populations that are chronically engaged in specialized motor behaviors [5].
Long-term specific experiences can induce specific neural and behavioral changes. For example, there is clearer movement and increased activation in the primary motor cortex (M1) in tennis players when merely rehearsing movements using a tennis racket [7]. Studies have also revealed that the anticipation ability and cortical disinhibition in basketball players with long-term decision-making skills in basketball games are higher than those in novice basketball players [6]. These results suggest that long-term specific experience-related neurophysiological and behavioral changes are context-dependent. Several contextual cues during short-term motor learning, including task-related (e.g., force field and movement direction) and environment-related (e.g., room color) contexts, influence motor memory [[10], [11], [12], [13]]. Although previous studies have examined whether task-related contextual stimuli after long-term specific experiences induce behavioral and neurophysiological changes [7,[14], [15], [16], [17]], investigating environment-related contextual changes during motor learning remains challenging.
Water immersion (WI) induces peripheral responses (e.g., increased venous return and decreased antigravity muscle activity) [18,19] and central responses (e.g., increased cerebral blood flow and sensorimotor activity) [20,21]. The perceptual sensation for passive movements in water in competitive swimmers with long-term training experience in water environments is higher than that in novice swimmers, which may explain why tactile sensory input from water induces neural response in the somatosensory cortex [22]. Furthermore, previous studies revealed that WI facilitated sensorimotor integration [21] and continuous somatosensory input by water increased M1 excitability [23]. Therefore, swimmers may complement their superior motor skills with sensorimotor integration in water, which may lead to the identification of environment-related contextual changes.
Learning sensorimotor skills is accompanied by substantial neural changes in many brain regions, including the sensorimotor cortex, posterior parietal cortex, striatum, cerebellum, and M1 [24]. Of these, M1 has been widely investigated in the context of skill acquisition, and studies have revealed that cortical spinal neurons with high firing thresholds and cortical inhibition with cortical changes are sensitive to long-term motor experiences [25,26]. Therefore, in the present study, we focused on the sensorimotor system and assessed whether basic neurophysiological measures of M1 excitability, including intracortical inhibition, were altered in swimmers in a manner that contributed to their enhanced sensorimotor skills in a water environment.
We hypothesized that, compared to novices, elite swimmers would demonstrate superior, robust sensorimotor skills in the water and the recruitment of corticospinal and intracortical projections following environment-related behavioral and neurophysiological adaptations to long-term training in a water environment would be different between elite swimmers and novices.
Section snippets
Participants
Fourteen healthy right-handed non-swimmers (four females) and 14 swimmers (six females) aged 20–22 years were included in the present study (see Table 1 for participant characteristics). All of the participants were from the same university in Japan, and all of the swimmers belonged to the same university swimming team and had experience in competing at national or inter-college swim meets. FINA points were calculated from their own fastest record to evaluate the performance level in swimmers (//www.fina.org/content/fina-points
Behavioral data
We tested the differences in behavioral performance between swimmers and non-swimmers in land and water environments. Results from the three-factor mixed design ANOVA revealed that there was a significant “group” × “environment” interaction effect (F[2,52] = 5.376, p = 0.008, ηp2 = 0.171) and significant main effects of “environment” (F[1.360,35.349] = 4.667, p = 0.027, ηp2 = 0.152) and “group” (F[1,26] = 16.202, p < 0.001, ηp2 = 0.384) on the absolute error angles. However, there were no other
Discussion
The present study examined the effects of long-term training on sensorimotor skills and M1 inhibitory function in water environments. The main findings of the present study were 1) the sensorimotor skills of swimmers who continued long-term training in a water environment were superior and more robust than those of non-swimmers irrespective of the environment (e.g., baseline on land, during WI, and after WI on land) and 2) intracortical inhibition in water environments was increased in swimmers
Author statement
D.S. conceived the original idea and designed the framework. Y.Y., Y.B. and K.I. carried out the experiment and analyzed the data. D.S. wrote the original and revised manuscript with support from K.Y., H.O. and A.M. D.S. and A.M. supervise the project.
Acknowledgement
The study was supported by the JSPS Kakenhi (Grant Number JP18H03134 and 15K12712) and Yamaha Motor Foundation for Sports.
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