Research ArticleArchery under the (electroencephalography-)hood: Theta-lateralization as a marker for motor learning
Introduction
From texting a message on a mobile phone, cutting vegetables to playing soccer, many aspects of our everyday life require learning and adaptation of motor skills. Modification of well-practiced activities to a changing environment is usually fast and specific training or even conscious intervention is rarely needed. Acquisition of entirely new and complex skills however may require extensive practice to master a potentially steep learning curve.
Many of such demanding motor abilities are more accurately performed with the dominant side of the body. Approximately 90 % of the population are right-handed (Papadatou-Pastou et al., 2020). Furthermore, a majority of soccer players prefer the right leg to kick a ball (van Melick et al., 2017). Eye-dominance, e.g., for fixating a target also shows this pattern with 71 % of subjects having right eye-dominance and 95 % of these also using the right hand for writing in a large survey-based study on 10,635 participants (McManus et al., 1999).
These behavioral findings correspond to structural and functional cerebral asymmetries. The central sulcus is deeper on the dominant left hemisphere in right-handers (Amunts et al., 2000). Left-right differences are also reported in the cortico-spinal tract (Hervé et al., 2009), the brainstem and cerebellum (Baizer, 2014). The basal ganglia have different morphology in right-handers vs non-right-handers (Jang et al., 2017). In addition, white matter tracts show significant left–right-differences (Jahanshad et al., 2010), which partially correlate to the degree of lateralization in tasks requiring visuospatial integration and fine motor control (Howells et al., 2018).
In addition to these structural findings, functional asymmetries in the motor system have been reported (Mutha et al., 2012, Floegel et al., 2017, Hodgson and Hudson, 2018, Pflug et al., 2019, Papitto et al., 2020). The functional role of the left hemisphere has especially been highlighted in the context of complex motor skills requiring high precision (Haaland and Harrington, 1996, Garry et al., 2004, Haaland et al., 2004, Helmich and Lausberg, 2014). This significance for acuity seems to be independent both of handedness (Serrien and Sovijärvi-Spapé, 2015) and of which hand is specifically used to perform the motor task – dominant, non-dominant or both (Grafton et al., 2002, Philip and Frey, 2016). Furthermore, left sided circuitry influences behavioral performance, also independent of handedness (Serrien and Sovijärvi-Spapé, 2016).
The mechanisms that lead to these structural, functional, and behavioral asymmetries are still largely unknown. Genetic factors play a significant role but do not explain the complete spectrum of findings. Jahanshad and colleagues (Jahanshad et al., 2010) for example found that genetic factors account for ∼ 33 % of variance in asymmetry in same-sex twin pairs. Early biophysical, molecular and bioelectrical asymmetries imply processes during embryogenesis (Vandenberg and Levin, 2013). However, clinical studies also suggest considerable plasticity across the lifespan in response to a lesion, intracranial surgery and rehabilitative therapy (Kleim and Jones, 2008, Plowman and Kleim, 2010, Roemmich and Bastian, 2018, Maier et al., 2019).
Such plasticity can also be observed after motor learning, which has been shown to induce structural changes in areas related to the specific task. However, these changes do not always correlate with improvement of performance (see review in Sampaio-Baptista et al., 2018). Due to experimental paradigms employing mostly unimanual tasks, many studies cannot distinguish whether or not such changes develop or enhance structural asymmetry. Furthermore, although differences become detectable already after only a few training sessions (Sampaio-Baptista et al., 2018), the structural alterations develop too slowly for direct observation during practice.
Using EEG (Electroencephalography), MEG (Magnetoencephalography) and fMRI (functional magnetic resonance imaging), many studies have investigated interhemispheric coupling during training and execution of tasks involving both sides of the body (see review in Rueda-Delgado et al., 2014). However, only few analyzed development of activation asymmetry in such a setting (Neuper et al., 1999, Velasques et al., 2007).
Due to limitations of the measurement equipment and logistical contraints, most studies have applied artificial experimental paradigms with limited ecological validity. Consequently, it remains unclear to what degree findings in typically highly overlearned tasks translate to acquisition of novel realistic motor skills.
Our study aims to investigate how such activity changes and specifically lateralization develops during the course of acquiring a new realistic motor skill – archery. Archery combines various aspects of motor planning and execution, attention as well as sensory and proprioceptive integration (Salazar et al., 1990, Vogt et al., 2017). At the same time, larger movements are limited to preparatory actions (Haywood, 2005). While initial progress is usually fast, mastering archery is sufficiently difficult to avoid ceiling effects (Haywood, 2005). Electroencephalography studies show differences between expert and novice participants as well as differences related to more fine-grained individual performance. Salazar et al. (1990) for example investigated EEG changes during archery and primarily report changes in the left hemisphere in the theta, alpha and beta band, which were related to performance and the latency to arrow release. Vogt et al. (2017) observed larger amplitudes and later onsets of readiness potentials in skilled vs less skilled archery novices. Another study (di Fronso et al., 2016) investigated EEG changes during pistol shooting in an elite shooter. These authors report global synchronization of cortical activity associated with optimal performance states, while suboptimal performance and reduced automaticity was related to increased activation in left temporal and frontal midline areas. Tombini et al. (2009) investigated EEG activation in relation to a 2D manual catching task. Motor learning and movement automation was linked to a reduction of theta event-related synchronization (ERS) in the anterior cingulate cortex (ACC) and a shift of alpha activity from bilateral to left superior parietal regions. Furthermore, theta ERS in the left SMA correlated with performance improvement. In golf putting, increased fronto-midline theta and also parietal alpha power was associated with better performance and higher expertise (Baumeister et al., 2008). In a similar study, Pitto et al. (2011) report higher theta synchronization and alpha and beta desychronization preceding successful trials in a virtual ball putting task.
In our study, we focus on the aiming phase, during which movements are subtle, allowing for recording of brain activity with EEG. We are particularly interested in this phase due to its relevance for behavioral performance, i.e. the achieved score (Clarys et al., 1990). Given the active effort required to pull and stabilize the bow as well as retain posture and preparation of the shot (Hennessy and Parker, 1990), aiming is not limited to motor and sequence planning, but also integrates elements of motor execution and attention.
Electroencephalography offers a high temporal and good spatial resolution for most cortical and some sub-cortical areas (Piastra et al., 2021). It also allows recording during preparation aiming and shooting, which enables analysis of neuronal correlates of performance over the course of the shot and across training sessions. We hypothesize that the relation to performance should be clearest immediately before string release due to convergence of different streams of activity culminating in the decision to release the arrow, while preceding activity would show a weaker relation. During rest, no such relation would be expected.
In our study, we investigate oscillatory activity during motor activation and learning. Work ranging from basic neuroscience and animal models to computational neuroscience demonstrate an oscillatory signature of cortical processing common across the cortex in invasive EEG, scalp EEG and MEG (Başar et al., 2001, Lopes da Silva, 2013, Ribary et al., 2017, Lundqvist et al., 2020, Lundqvist et al., 2011): Phases of cortical processing shows increases in theta and gamma with a largely consistent relationship between theta phase and gamma amplitude. Alpha and beta power is typically negatively correlated with theta/gamma and especially elevated during top-down control and inhibition.
Especially in the motor system, the role of beta band oscillations is well established, showing increases during postural and tonic contraction, decreased before and during voluntary movement and a rebounding increase immediately after movement (Pogosyan et al., 2009, Engel and Fries, 2010, Joundi et al., 2012, Lopes da Silva, 2013). Furthermore, movement-related beta activity was also shown to explain some of the observed variance of immediate post-training motor performance (Espenhahn et al., 2019).
In our study, we focus on theta, alpha and beta, but not on gamma mainly due to practical reasons. Gamma activity exhibits comparably low amplitudes according to the 1/f power scaling of EEG or MEG (Buzsáki et al., 2012). In addition, the frequency spectrum of EMG-activity and related artifacts show considerable overlap with gamma (Komi and Viitasalo, 1976, Lopes da Silva, 2013). Although the aiming phase does not require extensive muscle activation, EMG from the tonic activation of e.g. neck muscles may still interfere with gamma.
Motivated by evidence of such oscillatory activation with the data highlighting the role of the left hemisphere for motor tasks requiring high accuracy and coordination largely independent of handedness (Haaland and Harrington, 1996, Grafton et al., 2002, Garry et al., 2004, Haaland et al., 2004, Helmich and Lausberg, 2014, Serrien and Sovijärvi-Spapé, 2015, Philip and Frey, 2016), we explore the relationship of improvement of motor skills with activation shifts to the left (dominant) hemisphere during aiming in the theta, alpha and beta range.
Section snippets
Participants
A total of 11 adult, right-handed and right-eye dominant healthy participants without previous archery experience were included. Average age was 33 (range 29–46) and three participants were women. The procedures of this study were reviewed and approved by the local IRB (Ethikkommittee der Medizinischen Fakultät Halle (Saale)). All participants provided their written informed consent. The sample size was based on logistical constraints and previous EEG studies with comparable research questions (
Scores
Scores per day (Fig. 2, Table 1) increased over training sessions (p = 0.02, df = 2, χ2 = 8.19, Friedman test, day 1 vs 3 p = 0.015, mean difference day 3–day 1: 1.18 (0.21–2.16), p > 0.1 for other comparisons, Tukey-Kramer test). Improvements from day 2 to day 3 were smaller in most cases. A significant performance decline was observed only in a single case due to muscle fatigue as reported by the participant. Improvement was generally smaller in participants who already achieved high scores
Discussion
The present study demonstrates the novel finding that learning archery, an ecological valid task, which reflects a complex motor skill, is associated with a left shift of theta during aiming. The left shift of theta activity is in turn related to improved performance. Right-handed and right eye-dominant participants trained archery in a highly structured and formalized procedure. Timing of shot preparations were instructed, while aiming and string release were under the participants’ control.
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Conflicts of interest
The authors declare no competing interests.
Ethics approval statement
The procedures of this study were reviewed and approved by the local IRB (Ethikkommittee der Medizinischen Fakultät Halle (Saale)).
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