Elsevier

Neuroscience

Volume 275, 5 September 2014, Pages 47-53
Neuroscience

Changes of motor-cortical oscillations associated with motor learning

https://doi.org/10.1016/j.neuroscience.2014.06.008Get rights and content

Highlights

  • Motor-cortical alpha power changes with motor learning.

  • Gain of reaction times is correlated with the amount of beta power suppression.

  • Beta power suppression may indicate early cortical reorganization associated with motor learning.

Abstract

Motor learning results from practice but also between practice sessions. After skill acquisition early consolidation results in less interference with other motor tasks and even improved performance of the newly learned skill. A specific significance of the primary motor cortex (M1) for early consolidation has been suggested. Since synchronized oscillatory activity is assumed to facilitate neuronal plasticity, we here investigate alterations of motor-cortical oscillations by means of event-related desynchronization (ERD) at alpha (8–12 Hz) and beta (13–30 Hz) frequencies in healthy humans. Neuromagnetic activity was recorded using a 306-channel whole-head magnetoencephalography (MEG) system. ERD was investigated in 15 subjects during training on a serial reaction time task and 10 min after initial training. The data were compared with performance during a randomly varying sequence serving as control condition. The data reveal a stepwise decline of alpha-band ERD associated with faster reaction times replicating previous findings. The amount of beta-band suppression was significantly correlated with reduction of reaction times. While changes of alpha power have been related to lower cognitive control after initial skill acquisition, the present data suggest that the amount of beta suppression represents a neurophysiological marker of early cortical reorganization associated with motor learning.

Introduction

Motor skills are acquired during practice but often even continue to develop after practice sessions during so-called offline periods (Karni et al., 1998, Walker et al., 2002, Robertson et al., 2005, Hallgato et al., 2013). There is converging evidence that such consolidation requires a critical period after initial learning which varies between 1 and 6 h (Brashers-Krug et al., 1996, Shadmehr and Brashers-Krug, 1997, Shadmehr and Holcomb, 1997, Robertson et al., 2005, Janacsek and Nemeth, 2012). Nevertheless, a few studies reveal evidence for the assumption that improvement may occur even after a brief interval of 15 min (Denny et al., 1955, Rachman and Grassi, 1965) for a review see Halsband and Lange (2006) suggesting that newly learned motor skills become rapidly stabilized being less susceptible for interference with other motor skills (Muellbacher et al., 2002, Krakauer and Shadmehr, 2006).

The pivotal role of the primary motor cortex (M1) for stabilization of newly learned skills has been evidenced in animal studies (Nudo et al., 1996, Kleim et al., 1998, Plautz et al., 2000) as well as in humans using transcranial magnetic stimulation (TMS) (Pascual-Leone et al., 1994, Classen et al., 1998, Muellbacher et al., 2002, Robertson et al., 2005) and continuous theta-burst stimulation (Krakauer and Shadmehr, 2006, Iezzi et al., 2010). These data indicate that disrupting M1 excitability within a time period up to 2 h after initial learning deteriorates consolidation and blocks offline improvement over day (Robertson et al., 2005). M1 seems to be particularly relevant for learning of repetitive movements (Muellbacher et al., 2001, Baraduc et al., 2004, Censor and Cohen, 2011). Mapping of the motor cortex by TMS during motor learning revealed that the motor cortical output maps become progressively larger during implicit learning and return to baseline, when knowledge becomes explicit (Pascual-Leone et al., 1994) supporting the significance of M1 particularly for implicit learning (for reviews see (Ashe et al., 2006, Halsband and Lange, 2006)). Functional reorganization associated with motor learning is most likely due to long-term potentiation (LTP)-like effects as shown in animals (Rioult-Pedotti et al., 1998, Rioult-Pedotti et al., 2000, Hodgson et al., 2005) and humans (Ziemann et al., 2004, Jung and Ziemann, 2009).

Motor learning is additionally associated with changes of oscillatory activity in the alpha (8–12 Hz) (Zhuang et al., 1997) and beta (13–30 Hz) frequency range (Boonstra et al., 2007, Houweling et al., 2008). Synchronized oscillatory activity represents a pivotal mechanism for neuronal communication (Buzsaki and Draguhn, 2004, Fries, 2005). By temporally linking neurons in functional assemblies synchronized oscillatory activity facilitates neuronal plasticity and therefore plays an important role for consolidation of skills and knowledge.

TMS as well as behavioral studies suggest that consolidation of a newly learned movement requires at least 1 h. The neurophysiological changes within this interval have not been addressed so far. Therefore, the present study aims at investigating changes of motor cortical oscillations during acquisition and early consolidation of a motor sequence using magnetoencephalography (MEG).

Section snippets

Subjects and paradigm

Fifteen healthy subjects (seven male) participated in this study which was approved by the local ethics committee and complies with the Declaration of Helsinki. Data from one subject were excluded from the analysis due to poor quality of the MEG data. All participants gave their written informed consent prior to data acquisition. Mean age was 28.0 ± 2.3 years (mean ± standard error of the mean, s.e.m.). Subjects were naïve regarding the exact purpose of the study. The Edinburgh Handedness Inventory (

Motor learning

Analysis of reaction times revealed a main effect of factor condition (F(2, 26) = 55.01; p < 0.01). Post hoc tests indicated significantly faster reaction times during sequential 1 as compared to random (t(13) = 4.65; p < 0.01) and during sequential 2 as compared to sequential 1 (t(13) = 7.40; p < 0.01). Reaction times are summarized in Fig. 3A.

Analysis of skill acquisition showed reduction of reaction times of 50.21 ± 10.79 ms (skill 1) and 112.72 ± 12.66 ms (skill 2) as compared to random suggesting superior

Discussion

The present study aims at elucidating changes of motor cortical oscillations associated with acquisition and early consolidation of a motor sequence. The data support the hypothesis that motor learning is associated with a stepwise decline of alpha-band ERD and suggest that improvement of reaction times linearly varies with the amount of beta power suppression.

Neuroimaging studies evidenced activation changes within the primary motor or somatosensory cortex associated with motor learning. But

Acknowledgments

Vanessa Krause is grateful for two grants from Heinrich-Heine University (9772440, 9772467). Alfons Schnitzler acknowledges support from the Deutsche Forschungsgemeinschaft (DFG; SCHN 592/3-1, EraNet: 01EW0903) and Helmholtz Association (HelMA, HA-215). Bettina Pollok is grateful for financial support by a grant from the DFG (PO806-3) and a grant from Heinrich-Heine-University (9772558).

All authors declare no conflict of interests. Funding did neither influence the study design, collection,

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