A synergy-based hand control is encoded in human motor cortical areas
- University of Pisa, Italy
- Arizona State University, United States
Abstract
How the human brain controls hand movements to carry out different tasks is still debated. The concept of synergy has been proposed to indicate functional modules that may simplify the control of hand postures by simultaneously recruiting sets of muscles and joints. However, whether and to what extent synergic hand postures are encoded as such at a cortical level remains unknown. Here, we combined kinematic, electromyography, and brain activity measures obtained by functional magnetic resonance imaging while subjects performed a variety of movements towards virtual objects. Hand postural information, encoded through kinematic synergies, were represented in cortical areas devoted to hand motor control and successfully discriminated individual grasping movements, significantly outperforming alternative somatotopic or muscle-based models. Importantly, hand postural synergies were predicted by neural activation patterns within primary motor cortex. These findings support a novel cortical organization for hand movement control and open potential applications for brain-computer interfaces and neuroprostheses.
Article and author information
Author details
Reviewing Editor
- Jody C Culham, University of Western Ontario, Canada
Ethics
Human subjects: This study was approved by the Ethical Committee at the University of Pisa, Italy. Participants received a detailed explanation of all the study procedures and risks and provided a written informed consent according to the protocol approved by the University of Pisa Ethical Committee (1616/2003). All participants retained the right to withdraw from the study at any moment.
Version history
- Received: December 9, 2015
- Accepted: February 13, 2016
- Accepted Manuscript published: February 15, 2016 (version 1)
- Version of Record published: February 29, 2016 (version 2)
Copyright
© 2016, Leo 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
-
- 5,046
- views
-
- 989
- downloads
-
- 84
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
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)
A synergy-based hand control is encoded in human motor cortical areas
eLife 5:e13420.
https://doi.org/10.7554/eLife.13420
Further reading
-
- Neuroscience
This study investigates the goal/habit imbalance theory of compulsion in obsessive-compulsive disorder (OCD), which postulates enhanced habit formation, increased automaticity, and impaired goal/habit arbitration. It directly tests these hypotheses using newly developed behavioral tasks. First, OCD patients and healthy participants were trained daily for a month using a smartphone app to perform chunked action sequences. Despite similar procedural learning and attainment of habitual performance (measured by an objective automaticity criterion) by both groups, OCD patients self-reported higher subjective habitual tendencies via a recently developed questionnaire. Subsequently, in a re-evaluation task assessing choices between established automatic and novel goal-directed actions, both groups were sensitive to re-evaluation based on monetary feedback. However, OCD patients, especially those with higher compulsive symptoms and habitual tendencies, showed a clear preference for trained/habitual sequences when choices were based on physical effort, possibly due to their higher attributed intrinsic value. These patients also used the habit-training app more extensively and reported symptom relief post-study. The tendency to attribute higher intrinsic value to familiar actions may be a potential mechanism leading to compulsions and an important addition to the goal/habit imbalance hypothesis in OCD. We also highlight the potential of smartphone app training as a habit reversal therapeutic tool.
-
- Neuroscience
The fact that objects without proper support will fall to the ground is not only a natural phenomenon, but also common sense in mind. Previous studies suggest that humans may infer objects’ stability through a world model that performs mental simulations with a priori knowledge of gravity acting upon the objects. Here we measured participants’ sensitivity to gravity to investigate how the world model works. We found that the world model on gravity was not a faithful replica of the physical laws, but instead encoded gravity’s vertical direction as a Gaussian distribution. The world model with this stochastic feature fit nicely with participants’ subjective sense of objects’ stability and explained the illusion that taller objects are perceived as more likely to fall. Furthermore, a computational model with reinforcement learning revealed that the stochastic characteristic likely originated from experience-dependent comparisons between predictions formed by internal simulations and the realities observed in the external world, which illustrated the ecological advantage of stochastic representation in balancing accuracy and speed for efficient stability inference. The stochastic world model on gravity provides an example of how a priori knowledge of the physical world is implemented in mind that helps humans operate flexibly in open-ended environments.
