In Brain and Behavior: A multimethod investigation of motor inhibition in professional drummers

Boom Chack Boom—A multimethod investigation of motor inhibition in professional drummers. Lara Schlaffke  Sarah Friedrich  Martin Tegenthoff  Onur Güntürkün  Erhan Genç  Sebastian Ocklenburg. Brain and Behavior, December 4 2019. https://doi.org/10.1002/brb3.1490

Abstract
Introduction: Our hands are the primary means for motor interaction with the environment, and their neural organization is fundamentally asymmetric: While most individuals can perform easy motor tasks with two hands equally well, only very few individuals can perform complex fine motor tasks with both hands at a similar level of performance. The reason why this phenomenon is so rare is not well understood. Professional drummers represent a unique population to study it, as they have remarkable abilities to perform complex motor tasks with their two limbs independently.

Methods: Here, we used a multimethod neuroimaging approach to investigate the structural, functional, and biochemical correlates of fine motor behavior in professional drummers (n = 20) and nonmusical controls (n = 24).

Results: Our results show that drummers have higher microstructural diffusion properties in the corpus callosum than controls. This parameter also predicts drumming performance and GABA levels in the motor cortex. Moreover, drummers show less activation in the motor cortex when performing a finger‐tapping task than controls.

Conclusion: In conclusion, professional drumming is associated with a more efficient neuronal design of cortical motor areas as well as a stronger link between commissural structure and biochemical parameters associated with motor inhibition.

1 INTRODUCTION
Our hands are the primary means of interaction with the environment. A key aspect of hand use in humans is its asymmetrical organization. While most individuals can perform easy motor tasks with two hands at a similar level, only very few individuals can perform complex fine motor tasks with both hands equally well. Most individuals strongly prefer one hand (often called the dominant hand) over the other hand. Typically, each individual has a distinct handedness and prefers either the left or the right hand for complex fine motor tasks, for example writing (Güntürkün & Ocklenburg, 2017; Ocklenburg, Hugdahl, & Westerhausen, 2013). Handedness is thus one of the most pronounced and most widely investigated aspects of hemispheric asymmetries. A ratio of 90% right‐handed to 10% left‐handed people is constant for the past 5,000 years over all continents (Coren & Porac, 1977) and is noticeable even in utero (Hepper, Shahidullah, & White, 1990).

Each hand is controlled by the contralateral motor cortex. Neuronal correlates of handedness are mostly investigated by examining brain activity during more or less complex hand movement tasks. Such activities with the dominant hand are largely regulated by the contralateral hemisphere, whereas motor tasks with the nondominant hand are controlled more bilaterally by both hemispheres (van den Berg, Swinnen, & Wenderoth, 2011; Grabowska et al., 2012). The corpus callosum, as the major connecting pathway between hemispheres, was shown to have substantial influence on the characteristics of handedness (Hayashi et al., 2008; Westerhausen et al., 2004). Right‐handed people show a strong ipsilateral motor cortex de‐activation, when performing tasks with their dominant hand (Genç, Ocklenburg, Singer, & Güntürkün, 2015). In contrast, in left‐handed people, ipsilateral activations/de‐activation are equally pronounced, independent of the used hand. These findings demonstrate the correlation between ipsilateral activations and transcallosal inhibitions (Tzourio‐Mazoyer et al., 2015). Furthermore, patients with callosal agenesis, a hereditary condition in which the corpus callosum is absent in the brain, show a stronger tendency toward both‐handedness, for example not having a dominant hand (Ocklenburg, Ball, Wolf, Genç, & Güntürkün, 2015). Therefore, inhibitory functions of the corpus callosum represent an important aspect when understanding the neuronal correlates of handedness (Genç et al., 2015; Ocklenburg, Friedrich, Güntürkün, & Genç, 2016).

Since handedness can be partly altered through training (Perez et al., 2007), its constituent neural fundaments can change by learning. Neuroplasticity describes the adaption and cortical reorganization for example after training or learning a new skill. Functional plasticity of motor skills has been in the focus of neuroscientific research for decades. Already in the 1990s, it has been shown that playing the violin as a professional is influencing the somatosensory representations of the left (nondominant) hand (Elbert, Pantev, Wienbruch, Rockstroh, & Taub, 1995). Being able to play a music instrument on a professional level can also influence visuo‐motor (Buccino et al., 2004; Stewart et al., 2003; Vogt et al., 2007) as well as audio‐motor processes (Bangert et al., 2006; Baumann, Koeneke, Meyer, Lutz, & Jäncke, 2005; Baumann et al., 2007; Parsons, Sergent, Hodges, & Fox, 2005).

Up to now, musical training‐driven plasticity was primarily centered on changes of cortical gray matter. However, most musical instruments are played with both hands, increasing the demand for fast, precise and uncoupled movements of both hands. When playing piano, both hands are recruited in an equally demanding manner and sometimes with different rhythms, whereas playing a stringed instrument requires distinct motor activities for the same rhythm. In contrast, when drumming, both hands and even legs have to perform similar motor tasks, however with distinct rhythms. Therefore, drummers are well suited as subjects for the investigation of structural correlates of transcallosal inhibition.

While it is very difficult for an untrained person to play a ¾ beat with one hand and a 4/4 beat with the other at the same time, this is an easy task for trained drummers. Research in split‐brain patients indicates that this remarkable ability to uncouple the motor trajectories of the two hands is likely related to inhibitory functions of the corpus callosum. Franz, Eliassen, Ivry, and Gazzaniga (1996) investigated bimanual movements in split‐brain patients and healthy controls and found that the controls showed deviations in the trajectories when the two hands performed movements with different spatial demands (Franz et al., 1996). In contrast, split‐brain patients did not produce spatial deviations. This suggests that movement interference in controls is mediated by the corpus callosum and that professional drummers likely show an experience‐dependent change in callosal structure and/or function that enables them to perform two different motor trajectories with the two hands at the same time. Thus, drumming requires neuroplasticity of whiter matter pathways. This is what we set out to study.

The structural, functional, and biochemical correlates of this remarkable ability of professional drummers are still completely unclear, but unraveling them would yield important insights into the general neuronal foundations of motoric decoupling. Therefore, the present study was aimed at investigating professional drummers for structural, functional, and biochemical differences to untrained controls, linked to transcallosal inhibition. To this end, we used a state‐of‐the‐art multimethod neuroimaging approach. We assessed the microstructure of the corpus callosum using DTI to reveal possible alterations of callosal anatomy between groups (Friedrich et al., 2017; Genç, Bergmann, Singer, & Kohler, 2011a; Genç, Bergmann, Tong, et al., 2011b; Westerhausen et al., 2004). Moreover, we assessed the biochemical correlates of GABA spectroscopy to test long‐term changes of inhibitory motor control (Stagg, 2014), as GABA levels in motor regions are highly associated with BOLD activations and motor learning. Specifically, lower GABA levels are associated with an increased degree of motor learning (Ziemann, Muellbacher, Hallett, & Cohen, 2001), while individuals with higher baseline levels of M1 GABA have slower reaction times and smaller task‐related signal changes (Stagg, Bachtiar, & Johansen‐Berg, 2011). Last, we also scanned participants using a fMRI finger‐tapping task to use a well‐established quantitative framework producing different behavioral complexities (Genç et al., 2015; Haaland, Elsinger, Mayer, Durgerian, & Rao, 2004). We assumed that drummers should show differences from nonmusical controls reflecting a more efficient neural organization on the structural, functional, and biochemical modality.