[ARTICLE] Neural Network Underlying Intermanual Skill Transfer in Humans- Full Text

 

Highlights

 

Unimanual training also enhances performance in the untrained hand (cross-education)

Real-time manipulation of visual feedback enhances magnitude of cross-education
Yoking movement of untrained to trained hand further increases cross-education
Functional connectivity with SPL during training predicts cross-education

Summary

Physical practice with one hand results in performance gains of the other (un-practiced) hand, yet the role of sensory feedback and underlying neurophysiology is unclear. Healthy subjects learned sequences of finger movements by physical training with their right hand while receiving real-time movement-based visual feedback via 3D virtual reality devices as if their immobile left hand was training. This manipulation resulted in significantly enhanced performance gain with the immobile hand, which was further increased when left-hand fingers were yoked to passively follow right-hand voluntary movements. Neuroimaging data show that, during training with manipulated visual feedback, activity in the left and right superior parietal lobule and their degree of coupling with motor and visual cortex, respectively, correlate with subsequent left-hand performance gain. These results point to a neural network subserving short-term motor skill learning and may have implications for developing new approaches for learning and rehabilitation in patients with unilateral motor deficits.

Introduction

It is common wisdom that “practice makes perfect”; however, what constitutes an optimal practice regime when learning a new skill is not clear. In the domain of motor skills, for example, when learning to dribble a basketball, physical training with the relevant effector obviously plays a crucial role. Nonetheless, research over the past decades has recognized that sensory feedback and mental imagery play a significant role in the learning process (Nyberg et al., 2006, Sigrist et al., 2013, Wolpert et al., 2011). In the case of vision, it has been shown that even in the absence of physical training, mere observation of someone else performing a motor task is sufficient to introduce significant gains in subsequent performance of the observer (Bird et al., 2005, Cross et al., 2009, Kelly et al., 2003, Mattar and Gribble, 2005, Nojima et al., 2015, Vogt and Thomaschke, 2007, Ossmy and Mukamel, 2016). Furthermore, passive limb movement has also been shown to facilitate learning (Beets et al., 2012, Darainy et al., 2013, Vahdat et al., 2014, Wong et al., 2012). Finally, physical training with one hand is known to result in significant performance gains in the opposite (untrained) hand—a phenomenon termed intermanual transfer or cross-education (Ruddy and Carson, 2013). Intermanual transfer has been reported as early as 1894, showing that unilateral strength training of a single limb increases the strength of the contralateral (untrained) homologous muscle group (Scripture et al., 1894). Since then, this effect has been demonstrated across multiple motor tasks (Anguera et al., 2007, Brass et al., 2001, Camus et al., 2009, Carroll et al., 2006, Criscimagna-Hemminger et al., 2003, Farthing et al., 2007, Lee et al., 2010, Malfait and Ostry, 2004, Perez and Cohen, 2008, Perez et al., 2007, Sainburg and Wang, 2002) and is suggested to occur through plastic changes in the brain that are not confined to the specific neural networks controlling the physically trained effector (e.g., plastic changes also in motor cortex ipsilateral to the active hand [Duque et al., 2008, Hortobágyi et al., 2003, Muellbacher et al., 2000, Obayashi, 2004]). Enhancing the behavioral effect of intermanual transfer and elucidating its underlying neural mechanism has important implications for rehabilitation of patients with unimanual deficits (Hendy et al., 2012, Ramachandran and Altschuler, 2009) in which direct training of the affected hand is difficult.

Given that visual input, physical training, and passive movement play a significant role in performance and intermanual transfer of motor skills, research in recent years examined the behavioral and neural consequences of training with manipulated visual feedback (Halsband and Lange, 2006). In particular, unimanual training with mirrored visual feedback (as if the opposite, passive hand, is training) has been shown to enhance transfer to the opposite hand and increase excitability of primary motor cortex (M1) ipsilateral to the physically trained hand (Garry et al., 2005, Hamzei et al., 2012, Nojima et al., 2012). Nonetheless, much less is known at the whole-brain network level and how inter-regional coupling during such training correlates with subsequent behavioral changes in performance. Additionally, at the behavioral level, the interaction between manipulated visual feedback and passive movement during training is unknown.

In the present study, we examined intermanual transfer using a novel setup employing 3D virtual reality (VR) devices to control visual feedback of finger movements during unimanual training of healthy adults (experiment 1). By using a novel device, we also examined whether the addition of passive finger movement of the non-physically training hand further enhances the intermanual transfer effect (experiment 2). Finally, we used whole-brain functional magnetic resonance imaging (fMRI) to probe the relevant brain regions engaged during such training and examined their degree of inter-regional coupling with respect to subsequent behavioral changes in performance of individual subjects (experiment 3).

Continue —>  Neural Network Underlying Intermanual Skill Transfer in Humans: Cell Reports

(A) Schematic illustration of one experimental condition. A unique sequence of five digits was presented together with a sketch of the mapped fingers (instructions). Subjects performed the sequence as accurately and rapidly as possible using their right hand (RH) and their left hand (LH) separately for initial evaluation of performance. Next, subjects were trained under a specific training type and finally repeated the evaluation test again. (B) Subjects wore a headset and motion sensitive gloves and received visual feedback of virtual hands. The VR devices allowed visual manipulation of online visual feedback. A camera mounted on the headset allowed embedding the virtual hands and subject’s view inside a natural environment. (C) Experiment 1 results. Physical training with the right hand while receiving online visual feedback as if the left hand is moving (RH-LH) resulted in highest left-hand performance gains relative to all other training conditions. Error bars indicate SEM across subjects. For condition acronyms, see Table 1.

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