Skill learning strengthens cortical representations of motor sequences

Tobias Wiestler,Jörn Diedrichsen

doi:10.7554/elife.00801

Abstract

Motor-skill learning can be accompanied by both increases and decreases in brain activity. Increases may indicate neural recruitment, while decreases may imply that a region became unimportant or developed a more efficient representation of the skill. These overlapping mechanisms make interpreting learning-related changes of spatially averaged activity difficult. Here we show that motor-skill acquisition is associated with the emergence of highly distinguishable activity patterns for trained movement sequences, in the absence of average activity increases. During functional magnetic resonance imaging, participants produced either four trained or four untrained finger sequences. Using multivariate pattern analysis, both untrained and trained sequences could be discriminated in primary and secondary motor areas. However, trained sequences were classified more reliably, especially in the supplementary motor area. Our results indicate skill learning leads to the development of specialized neuronal circuits, which allow the execution of fast and accurate sequential movements without average increases in brain activity. DOI:http://dx.doi.org/10.7554/eLife.00801.001.

Highlights

The human brain has a remarkable ability to learn complex motor skills
Functional magnetic resonance imaging studies have shown that learning can lead to both activity increases and decreases in primary and secondary motor areas, these average activity changes remain hard to interpret
Motor skill acquisition may lead to increased neural recruitment for trained behaviors, thereby increasing average activation (Grafton et al, 1995; Karni et al, 1995; Hazeltine et al, 1997; Floyer-Lea and Matthews, 2005; Lehericy et al, 2005; Penhune and Doyon, 2002; Penhune and Doyon, 2005)

Summary

Introduction

The human brain has a remarkable ability to learn complex motor skills. the neural changes that underlie this ability remain largely unknown. Functional magnetic resonance imaging (fMRI) studies have shown that learning can lead to both activity increases and decreases in primary and secondary motor areas (for reviews, see Dayan and Cohen, 2011; Penhune and Steele, 2012; Hardwick et al, 2013), these average activity changes remain hard to interpret. Motor skill acquisition may lead to increased neural recruitment for trained behaviors, thereby increasing average activation (Grafton et al, 1995; Karni et al, 1995; Hazeltine et al, 1997; Floyer-Lea and Matthews, 2005; Lehericy et al, 2005; Penhune and Doyon, 2002; Penhune and Doyon, 2005). Motor practice may induce simultaneous signal increases (due to increased neural recruitment) and signal decreases (due to more efficient encoding), making motor learning difficult to detect using traditional fMRI paradigms (Steele and Penhune, 2010)

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