Cortico-spinal synchronization reflects changes in performance when learning a complex bimanual task

Abstract

Motor performance is accompanied by neural activity in various cortical and sub-cortical areas. This intricate network has to be delicately orchestrated. We analyzed the role of beta synchronization in motor learning using magneto-encephalography combined with electromyography. Cortico-spinal synchronization in the beta band was found to be of particular importance in establishing bimanual movement patterns in the context of a 3:2 polyrhythmic (isometric) force production task. Its dynamics correlated highly with the learning of this complex bimanual motor skill. We submit that the cortical dynamics entrains the spinal motor system by which cortico-spinal beta synchrony serves higher-level motor control functions as primary means of information transfer along the neural axis.

Introduction

Oscillatory neural activity can be found at different frequency bands in various cortical and sub-cortical areas. These neural oscillations have to be accurately tuned to achieve proper macroscopic performance. When assessed by encephalography, oscillatory activity generally gives rise to synchronization within a neural ensemble or between ensembles (Salenius and Hari, 2003). Importantly, neurons synchronize their firing patterns in accordance with different behavioral states. Changes in instantaneous amplitude or power therefore reflect changes in local synchronization, e.g., within a cortical area. In contrast, changes in instantaneous relative phase or coherence reflect changes in more global, distributed synchronization, e.g., between cortical areas or between cortex and neural ensembles in the spinal cord. In fact, synchronized activity across neural networks is believed to offer an effective mechanism for information transfer, especially when discriminating between frequency- and phase-locked activity (Alegre and Artieda, 2000, Salinas and Sejnowski, 2001).

In the context of motor control, it has been suggested that synchronization at different levels along the neural axis constitutes an important vehicle for motor timing (Baker et al., 1999, Farmer, 1998, Schoffelen et al., 2005). Cortical–cortical and cortico-spinal synchronization have been observed for both rhythmical (Boonstra et al., 2007) and non-rhythmical tasks (Kristeva et al., 2007, Salenius and Hari, 2003) and may occur in several frequency bands (Cheyne et al., 2008), each of which has been linked to a specific functional role. To paraphrase MacKay: “Oscillatory signals around 10, 20, and 40 Hz in the sensorimotor cortex have been associated with constant sustained muscle contractions. The dynamic phase at the onset of an intended movement is preceded by a marked drop in power, but not all frequencies are suppressed. Fast gamma (above 30 Hz) rhythms coincide with movement onset. Oscillatory signals even at low frequencies (between 4 and 12 Hz) may be linked to dynamic episodes of movement. These appear to exert preparatory functions. The neurogenic component of physiological tremor, an 8 Hz signal, is emerging as a factor in shaping the pulsatile dynamic micro-structure of movement, possibly in coordinating diverse actions” (MacKay, 2005, page 181). Cortico-spinal synchronization in the beta band is often associated with movement initiation and may also play an active role in postural stabilization (Androulidakis et al., 2007, Baker et al., 1999, Gilbertson et al., 2005, van Wijk et al., 2009). Does this imply that beta activity is also relevant for motor learning?

To test for a significant role of beta synchrony in cortico-spinal systems in the context of motor learning, we studied synchronization while subjects learned a complex motor skill in which isometric forces had to be generated with the right and left index fingers at a fixed 3:2 polyrhythm. We previously investigated steady pre- and post-learning conditions (Houweling et al., 2008b), which revealed sustained changes in primary motor areas and in the cerebellum, even in control tasks that had not been learned. Synchronization patterns within and between oscillatory activities in these areas differentiated to distinct frequency bands. Here we report the dynamics of motor learning and delineate the characteristics of synchrony that co-vary with the observed changes in behavior, i.e., with the achievement of proper motor timing. We expected cortico-spinal synchronization to increase with motor learning.