Movement and sport sciences

Wolfgang Taube's research team explores diverse neuroscientific themes in the context of motor learning and motor control, spanning from elite athletes to individuals across different age groups and health conditions, including patients with various pathologies. Their primary focus lies on understanding the cortical inhibitory system. Initially, their interest stemmed from recognizing the undervalued role of inhibitory mechanisms, particularly in healthy populations and sports performance. However, their research trajectory has evolved towards investigating how targeted physical training interventions can enhance intracortical inhibition and modulation of intracortical inhibition, thereby improving motor performance. Consequently, their attention has shifted towards populations with compromised inhibitory control, such as seniors and patients.

To accomplish their goals, they employ a variety of multimodal scientific techniques, including transcranial magnetic stimulation (TMS), near-infrared spectroscopy (NIRS), (functional) magnetic resonance imaging (fMRI), magnetic resonance spectroscopy (MRS), and peripheral nerve stimulation (PNS).

For those interested in delving deeper into their research, the subsequent paragraph elaborates on the evolution of Taube’s research group. Initially focusing on sports and performance-related applications to alter GABAergic inhibition, their work has progressed towards "Sport as Medicine Approaches”, where GABAergic modulation is specifically targeted to address health issues.


The inhibitory system in healthy people

A vivid example to illustrate the importance of inhibitory mechanisms for sports-related performance is evident in our investigations into the 'focus of attention’. While it is widely recognized that an external focus of attention is generally more effective than an internal one, the underlying neural mechanisms have remained elusive. Through a series of experiments, we have shown that enhanced motor performance with an external focus of attention, including fine motor coordination, endurance, and explosive force tasks, are related to increases in intracortical inhibition [1, 2] and more pronounced surround inhibition [3]. This suggests that heightened inhibition may contribute to focusing neural activation, thereby enhancing the efficiency, economy, and goal-oriented nature of motor execution. Additionally, we have revealed through H-reflex conditioning by TMS that slower, indirect corticospinal pathways are inhibited when an external focus of attention is employed [4].

In a study comparing skilled piano players to novices, we observed distinct inhibitory patterns based on whether participants selectively activated a single finger or performed more intricate sequences of finger movements [5]. This task-specific modulation of intracortical inhibition is essential, as isolated finger actions require heightened inhibition to prevent adjacent finger muscle activity, while executing complex movement sequences benefits from reduced surround inhibition to enable synergistic activity.

Furthermore, our research illustrates that inhibitory control is muscle- and task-specific. We found that during dynamic contractions, minimal inhibition is crucial in the agonist muscle to offer high cortical drive, while the antagonist muscle requires elevated inhibition to prevent counterproductive co-activation [6]. This modulation was also evident in studies investigating postural control, where intracortical inhibition was better modulated in certain muscles compared to others and displayed age-related declines [7-9].

Recent longitudinal studies from our group demonstrate changes in intracortical inhibition after several weeks of motor learning. Notably, Mouthon and Taube [10] stand out as the first longitudinal study demonstrating an elevation in intracortical inhibition following prolonged balance training. Until then, it was thought impossible to upregulate GABAergic inhibition by training and/or motor learning. Building upon these findings, we have explored the potential of physical training interventions to specifically target up-regulation of reduced intracortical inhibitory capacity in seniors and patients [11, 12]. Our investigations show that elderly individuals can enhance their intracortical inhibition after several months of balance training, correlating with improvements in balance control [Kuhn et al., in revision]. This work was an important step towards the application of "Sport as Medicine”, in which GABAergic modulation is specifically targeted to address health issues.


Sport as Medicine

In our latest Swiss National Science Foundation (SNSF) project, a collaborative effort between Prof. Taube, Prof. Rasch and Prof. Xin from the EPFL, we demonstrated that after three months of balance learning, elderly participants not only significantly elevated their levels of intracortical inhibition during sleep but also reported improved subjective sleep quality, indicating a correlation between these two parameters [Scherrer et al., in preparation]. Given that aging and poor sleep quality are associated with reduced levels of intracortical inhibition, this project underscored the potential of balance learning to enhance sleeping behavior in elderly individuals in a cost-effective manner, without the negative side effects associated with standard medication-based treatments for sleep problems.

Moreover, in this SNSF project, we adopted a multi-modal approach employing complementary methods to assess the GABAergic system. Alongside the paired-pulse transcranial magnetic stimulation (TMS) paradigm, we utilized magnetic resonance spectroscopy (MRS), which revealed significant increases in GABA concentration in the sensorimotor network following balance learning [Xinyu et al., in revision]. To our knowledge, this is the first study to comprehensively examine changes in intracortical inhibition (SICI) and alterations in cortical GABA concentration (MRS) over an extended training period in elderly individuals. Building on these results, we propose that the elevated GABA levels assessed with MRS indicate an increased 'capacity for inhibition' following balance learning, whereas SICI measured with TMS during balancing reflects the enhanced 'ability to modulate inhibition'. This marks the first demonstration that both the 'capacity of inhibition' and the 'ability to modulate inhibition' can be modified through balance learning, with these changes closely linked to functional connectivity (evaluated with functional magnetic resonance imaging - fMRI) and balance performance.

In our preceding SNSF project, we also included a cohort of elderly participants undergoing three months of resistance training instead of balance learning. In contrast to the balance learning and control groups, we found that strength training exerted the most significant effect on brain metabolism, as evidenced by a significant reduction in brain lactate concentration. This suggests a shift towards oxidative phosphorylation from glycolysis for energy production. Interestingly, the distinct adaptations following balance and resistance training were also mirrored in their effects on sleep: while the balance training group reported better subjective sleep quality, deemed the most clinically relevant parameter, participants in the strength training group exhibited improved objectively assessed sleep. This indicates that although both training interventions positively impacted sleep, the underlying mechanisms differed substantially [Scherrer et al., in preparation].

Lastly, not only people with sleep problems display reduced inhibitory capacities, but also people suffering from certain kind of depressions, ADHD, dystonia, certain forms of dementia or pain. With respect to the latter, it is widely acknowledged that dysfunction within the GABAergic system may serve as one of the fundamental mechanisms contributing to chronic nonspecific pain. While GABAergic medications demonstrate clinical efficacy in pain management, they often entail significant unwanted side effects, notably sedation. Thus, we were hypothesizing that balance training would not only have a positive impact on the cortical inhibitory system (SICI) in a 62-year-old individual experiencing widespread chronic pain, but also on pain perception. Following two baseline assessments, the patient underwent two periods of balance training lasting 4 weeks each, separated by detraining phases lasting 2 months each. Intracortical inhibition (i.e., SICI), pain levels, and overall well-being were evaluated at baseline, post-intervention, and post-detraining phases. Our findings revealed a significant enhancement and more finely-tuned modulation of intracortical inhibition after the initial 4-week balance training period, accompanied by pain relief and improvements in sleep quality and mood. However, following the 2-month detraining phase, all parameters returned to baseline levels. Subsequently, during a second 4-week balance training period, intracortical inhibition was further elevated, surpassing the values observed during the initial training phase. Correspondingly, pain, sleep, and mood scores showed further improvement. Nevertheless, after the second detraining phase, all measurements reverted to values close to baseline levels. These results substantiate the notion that the GABAergic system plays a crucial role in pain processing and perception. Moreover, balance training emerges as an effective approach not only for augmenting intracortical inhibition but also for alleviating pain and enhancing overall well-being and sleep in individuals with chronic nonspecific pain (Taube et al., manuscript in preparation).


Contributions to Science

Over the past years, Wolfgang Taube has emerged as a world-leading expert in postural control and balance training, focusing on elucidating the underlying neural mechanisms [1]. A significant contribution to science has been his adaptation of challenging electrophysiological techniques, traditionally employed in static conditions in hospital patients, to dynamic, functionally relevant movements. Taube pioneered the application of H-reflex conditioning by transcranial magnetic stimulation (TMS) during demanding postural tasks [2], as well as the utilization of TMS during drop jumps [3]. Moreover, his research group advanced the H-reflex conditioning technique developed by Jens Bo Nielsen (Copenhagen) by incorporating TMS over the cervicomedullary junction, enabling assessment of the efficiency of corticomotoneuronal synapses [4].

In recent years, Taube's research focus has shifted towards investigating the inhibitory (GABAergic) system, yielding significant insights. His group has highlighted the importance of assessing the modulatory capacity of the inhibitory system during activity rather than at rest [5]. Notably, they were the first to demonstrate that performance enhancements associated with changes in attentional focus, particularly an external focus, are reliant on increases in intracortical inhibition and surround inhibition [6; 7]. Additionally, Mouthon & Taube [8] were the first to introduce an intervention (i.e. highly coordinative balance training) to increase intracortical inhibition (measured with TMS) and to enhance the level of GABA (measured with magnetic resonance spectroscopy; manuscript in preparation). This was a crucial step for the application of balance exercise programs in other patient-groups with decreased inhibitory activity (for details please see section “Sport as Medicine”).

Main lines of research

• Sport as medicine (with a special focus on the GABAergic system)
• Neural plasticity in response to long-term balance learning in young and old: behavioral, structural, functional and neurophysiological adaptations
• Neuro-muscular adaptations to strength training
• Neuro-muscular adaptations to stretch-shortening cycle training (jumping)
• Non-physical (mental) training (motor imagery, action observation, and the combination of motor imagery and action observation)
• Focus of attention – What changes in the brain when changing the focus of attention?
• Augmented feedback – How to improve motor learning and motor memory consolidation by providing augmented feedback!
• Research in different sport disciplines – applied research to increase performance: Soccer, Tennis, Gymnastics, Ice skating, Slacklining, Skiing, Cycling
  
  
  
  

^{1. Kuhn, Y.-A., et al., Intracortical Inhibition Within the Primary Motor Cortex Can Be Modulated by Changing the Focus of Attention. Jove-Journal of Visualized Experiments, 2017(127).}

^{2. Kuhn, Y.-A., et al., Adopting an external focus of attention alters intracortical inhibition within the primary motor cortex. Acta Physiologica, 2017. 220(2): p. 289-299.}

^{3. Kuhn, Y.A., et al., Surround inhibition can instantly be modulated by changing the attentional focus. Sci Rep, 2018. 8(1): p. 1085.}

^{4. Kuhn, Y.A., et al., Effects of an external compared to an internal focus of attention on the excitability of fast and slow(er) motor pathways. Sci Rep, 2021. 11(1): p. 17910.}

^{5. Márquez, G., et al., Surround Inhibition in the Primary Motor Cortex is Task-specifically Modulated in Non-professional Musicians but not in Healthy Controls During Real Piano Playing. Neuroscience, 2018. 373: p. 106-112.}

^{6.Lauber, B., A. Gollhofer, and W. Taube, Differences in motor cortical control of the soleus and tibialis anterior. J Exp Biol, 2018. 221(Pt 20).}

^{7. Papegaaij, S., et al., Postural challenge affects motor cortical activity in young and old adults. Exp Gerontol, 2016. 73: p. 78-85.}

^{8. Papegaaij, S., et al., Intracortical inhibition in the soleus muscle is reduced during the control of upright standing in both young and old adults. Eur J Appl Physiol, 2016. 116(5): p. 959-67.}

^{9. Papegaaij, S., et al., Postural challenge affects motor cortical activity in young and old adults. Experimental Gerontology, 2016. 73: p. 78-85.}

^{10. Mouthon, A. and W. Taube, Intracortical Inhibition Increases during Postural Task Execution in Response to Balance Training. Neuroscience, 2019. 401: p. 35-42.}

^{11. Lauber, B., A. Gollhofer, and W. Taube, What to train first: Balance or explosive strength? Impact on performance and intracortical inhibition. Scand J Med Sci Sports, 2021.}

^{12. Taube, W., A. Gollhofer, and B. Lauber, Training-, muscle- and task-specific up- and downregulation of cortical inhibitory processes. Eur J Neurosci, 2020. 51(6): p. 1428-1440.}