High-fidelity musculoskeletal modeling reveals a motor planning contribution to the speed-accuracy tradeoff
Abstract
A long-standing challenge in motor neuroscience is to understand the relationship between movement speed and accuracy, known as the speed-accuracy tradeoff. Here, we introduce a biomechanically realistic computational model of three-dimensional upper extremity movements that reproduces well-known features of reaching movements. This model revealed that the speed-accuracy tradeoff, as described by Fitts' law, emerges even without the presence of motor noise, which is commonly believed to underlie the speed-accuracy tradeoff. Next, we analyzed motor cortical neural activity from monkeys reaching to targets of different sizes. We found that the contribution of preparatory neural activity to movement duration variability is greater for smaller targets than larger targets, and that movements to smaller targets exhibit less variability in population-level preparatory activity, but greater movement duration variability. These results propose a new theory underlying the speed-accuracy tradeoff: Fitts' law emerges from greater task demands constraining the optimization landscape in a fashion that reduces the number of 'good' control solutions (i.e., faster reaches). Thus, contrary to current beliefs, the speed-accuracy tradeoff could be a consequence of motor planning variability and not exclusively signal-dependent noise.
Data availability
The source code for the computer simulations and our data are available at https://simtk.org/projects/ue-reaching. Users must first create a free account (https://simtk.org/account/register.php) before they can download the datasets from the site.
Article and author information
Author details
Funding
National Institutes of Health (U54EB020405)
- Scott L Delp
National Institute of Neurological Disorders and Stroke (R01NS076460)
- Krishna V Shenoy
National Institute of Mental Health (R01MH09964703)
- Krishna V Shenoy
Defense Advanced Research Projects Agency (N66001-10-C-2010)
- Krishna V Shenoy
National Institutes of Health (8DP1HD075623)
- Krishna V Shenoy
Simons Foundation (325380 and 543045)
- Krishna V Shenoy
National Institutes of Health (5F31NS103409-02)
- Saurabh Vyas
National Science Foundation (Graduate Fellowship)
- Saurabh Vyas
Stanford University (Ric Weiland Stanford Graduate Fellowship)
- Saurabh Vyas
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: All surgical and animal care procedures were performed in accordance with NationalInstitutes of Health guidelines and were approved by the Stanford University InstitutionalAnimal Care and Use Committee (8856).
Human subjects: Subjects gave written informed consent, and consent to publish, approved by the Stanford University Institutional Review Board (42787). The guidelines followed are specified in the Human Research Protection Program (HRPP Stanford University).
Copyright
© 2020, Al Borno 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
-
- 1,931
- views
-
- 248
- downloads
-
- 10
- 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
The specific role that prolactin plays in lactational infertility, as distinct from other suckling or metabolic cues, remains unresolved. Here, deletion of the prolactin receptor (Prlr) from forebrain neurons or arcuate kisspeptin neurons resulted in failure to maintain normal lactation-induced suppression of estrous cycles. Kisspeptin immunoreactivity and pulsatile LH secretion were increased in these mice, even in the presence of ongoing suckling stimulation and lactation. GCaMP fibre photometry of arcuate kisspeptin neurons revealed that the normal episodic activity of these neurons is rapidly suppressed in pregnancy and this was maintained throughout early lactation. Deletion of Prlr from arcuate kisspeptin neurons resulted in early reactivation of episodic activity of kisspeptin neurons prior to a premature return of reproductive cycles in early lactation. These observations show dynamic variation in arcuate kisspeptin neuronal activity associated with the hormonal changes of pregnancy and lactation, and provide direct evidence that prolactin action on arcuate kisspeptin neurons is necessary for suppressing fertility during lactation in mice.
-
- Neuroscience
The role of cerebellum in controlling eye movements is well established, but its contribution to more complex forms of visual behavior has remained elusive. To study cerebellar activity during visual attention we recorded extracellular activity of dentate nucleus (DN) neurons in two non-human primates (NHPs). NHPs were trained to read the direction indicated by a peripheral visual stimulus while maintaining fixation at the center, and report the direction of the cue by performing a saccadic eye movement into the same direction following a delay. We found that single-unit DN neurons modulated spiking activity over the entire time course of the task, and that their activity often bridged temporally separated intra-trial events, yet in a heterogeneous manner. To better understand the heterogeneous relationship between task structure, behavioral performance, and neural dynamics, we constructed a behavioral, an encoding, and a decoding model. Both NHPs showed different behavioral strategies, which influenced the performance. Activity of the DN neurons reflected the unique strategies, with the direction of the visual stimulus frequently being encoded long before an upcoming saccade. Moreover, the latency of the ramping activity of DN neurons following presentation of the visual stimulus was shorter in the better performing NHP. Labeling with the retrograde tracer Cholera Toxin B in the recording location in the DN indicated that these neurons predominantly receive inputs from Purkinje cells in the D1 and D2 zones of the lateral cerebellum as well as neurons of the principal olive and medial pons, all regions known to connect with neurons in the prefrontal cortex contributing to planning of saccades. Together, our results highlight that DN neurons can dynamically modulate their activity during a visual attention task, comprising not only sensorimotor but also cognitive attentional components.