A critical re-evaluation of fMRI signatures of motor sequence learning
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.
Data availability
fMRI data and analysis pipelines have been deposted to OpenNeuro, under the accession number ds002776. Analysis code is available on GitHub at https://github.com/eberlot/motor_sequence_learning.git
Article and author information
Author details
Funding
Natural Sciences and Engineering Research Council of Canada (NSERC Discovery Grant (RGPIN-2016-04890))
- Jörn Diedrichsen
Canada First Research Excellence Fund (BrainsCAN)
- Jörn Diedrichsen
Ontario Trillium Foundation (Graduate Student Scholarship (to EB))
- Jörn Diedrichsen
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Marius V Peelen, Radboud University, Netherlands
Ethics
Human subjects: Informed consent and data usage agreement was obtained from participants prior to the onset of the study. It was emphasized that participants could withdraw from the study at any timepoint. The experimental procedures were approved by the Ethics Committee at Western University (HSREB File Number: 107061).
Version history
- Received: January 17, 2020
- Accepted: April 28, 2020
- Accepted Manuscript published: May 13, 2020 (version 1)
- Version of Record published: June 2, 2020 (version 2)
Copyright
© 2020, Berlot et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 3,780
- views
-
- 497
- downloads
-
- 61
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Neuroscience
Functional magnetic resonance imaging (fMRI) studies have documented cerebellar activity across a wide array of tasks. However, the functional contribution of the cerebellum within these task domains remains unclear because cerebellar activity is often studied in isolation. This is problematic, as cerebellar fMRI activity may simply reflect the transmission of neocortical activity through fixed connections. Here, we present a new approach that addresses this problem. Rather than focus on task-dependent activity changes in the cerebellum alone, we ask if neocortical inputs to the cerebellum are gated in a task-dependent manner. We hypothesize that input is upregulated when the cerebellum functionally contributes to a task. We first validated this approach using a finger movement task, where the integrity of the cerebellum has been shown to be essential for the coordination of rapid alternating movements but not for force generation. While both neocortical and cerebellar activity increased with increasing speed and force, the speed-related changes in the cerebellum were larger than predicted by an optimized cortico-cerebellar connectivity model. We then applied the same approach in a cognitive domain, assessing how the cerebellum supports working memory. Enhanced gating was associated with the encoding of items in working memory, but not with the manipulation or retrieval of the items. Focusing on task-dependent gating of neocortical inputs to the cerebellum offers a promising approach for using fMRI to understand the specific contributions of the cerebellum to cognitive function.
-
- Neuroscience
The first neuronal wiring diagram of an insect nerve cord, which includes biological information on cell type and organisation, enables further investigation into premotor circuit function.