A critical re-evaluation of fMRI signatures of motor sequence learning

Elife. 2020 May 13:9:e55241. doi: 10.7554/eLife.55241.

Abstract

Despite numerous studies, there is little agreement about what brain changes accompany motor sequence learning, partly because of a general publication bias that favors novel results. We therefore decided to systematically reinvestigate proposed functional magnetic resonance imaging correlates of motor learning in a preregistered longitudinal study with four scanning sessions over 5 weeks of training. Activation decreased more for trained than untrained sequences in premotor and parietal areas, without any evidence of learning-related activation increases. Premotor and parietal regions also exhibited changes in the fine-grained, sequence-specific activation patterns early in learning, which stabilized later. No changes were observed in the primary motor cortex (M1). Overall, our study provides evidence that human motor sequence learning occurs outside of M1. Furthermore, it shows that we cannot expect to find activity increases as an indicator for learning, making subtle changes in activity patterns across weeks the most promising fMRI correlate of training-induced plasticity.

Keywords: human; motor learning; neuroimaging; neuroscience; plasticity; representational fmri analysis.

Plain language summary

It has famously been claimed that it takes 10,000 hours to become an expert at something. But while most of us will never become concert pianists, we can all learn new motor skills and improve existing ones – from touch-typing to tennis – by practicing. What happens in the brain to produce these improvements in performance? Researchers have tried to answer this question by scanning the brains of people as they practice motor skills, but the results have proved inconsistent. Some studies find that specific brain areas become more active as people practice. This could indicate that these areas are ‘storing’ new skills. But others report that brain activity decreases with practice. This might indicate that practice instead makes certain brain areas work more efficiently. It is also unclear where in the brain these learning-related changes occur. Some studies suggest that most occur in the primary motor cortex, or M1 – the area that sends commands to muscles. Others suggest that most changes take place outside of M1, in areas that plan movements. Berlot et al. set out to resolve these inconsistencies by scanning the brains of healthy volunteers as they learned to play six 9-digit sequences on a keyboard. Each volunteer completed about 4,000 training trials over 5 weeks, and had their brain scanned four times. As the weeks passed, the volunteers became faster and more accurate at playing the sequences. However, the activity of their primary motor cortex did not change. By contrast, the activity of areas involved in planning movements decreased throughout training. The patterns of activity for each individual sequence reorganized throughout learning in the areas outside of the M1. This happened most quickly during the early stages of training when the volunteers showed the fastest improvements in performance. Overall, these findings suggest that when we learn a new skill, activity in the brain areas supporting that skill decrease as the brain becomes more efficient. Increases in brain activity are thus unlikely to reflect the acquired skill. Instead, more subtle changes, in which the brain uses more specific patterns of activity to encode the skill, may underlie improved performance. This may also be true for other types of learning, such as acquiring a new language.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Brain Mapping*
  • Brain Waves*
  • Female
  • Humans
  • Learning*
  • Longitudinal Studies
  • Magnetic Resonance Imaging*
  • Male
  • Motor Cortex / diagnostic imaging*
  • Motor Cortex / physiology
  • Motor Skills*
  • Parietal Lobe / diagnostic imaging*
  • Parietal Lobe / physiology
  • Predictive Value of Tests
  • Time Factors
  • Young Adult