The energetic basis for smooth human arm movements
- Faculty of Kinesiology, Department of Biomedical Enginee, Canada
- University of Calgary, Canada
Abstract
The central nervous system plans human reaching movements with stereotypically smooth kinematic trajectories and fairly consistent durations. Smoothness seems to be explained by accuracy as a primary movement objective, whereas duration seems to economize energy expenditure. But the current understanding of energy expenditure does not explain smoothness, so that two aspects of the same movement are governed by seemingly incompatible objectives. Here we show that smoothness is actually economical, because humans expend more metabolic energy for jerkier motions. The proposed mechanism is an underappreciated cost proportional to the rate of muscle force production, for calcium transport to activate muscle. We experimentally tested that energy cost in humans (N=10) performing bimanual reaches cyclically. The empirical cost was then demonstrated to predict smooth, discrete reaches, previously attributed to accuracy alone. A mechanistic, physiologically measurable, energy cost may therefore explain both smoothness and duration in terms of economy, and help resolve motor redundancy in reaching movements.
Data availability
Data has been deposited to Dryad Digital Repository, accessible here: doi:10.5061/dryad.qfttdz0gn
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The energetic basis for smooth human arm movementsDryad Digital Repository, doi:10.5061/dryad.qfttdz0gn.
Article and author information
Author details
Funding
Benno Nigg Chair
- Arthur D Kuo
NSERC Discovery and Research Chairs Program
- Arthur D Kuo
Alberta Health Trust
- Arthur D Kuo
NSERC Discovery
- Tyler Cluff
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Alaa Ahmed, University of Colorado, United States
Ethics
Human subjects: Informed consent was obtained from all subjects and the Health Research Ethics Board approved of all procedures (REB18-1521).
Version history
- Preprint posted: December 29, 2020 (view preprint)
- Received: March 3, 2021
- Accepted: December 15, 2021
- Accepted Manuscript published: December 20, 2021 (version 1)
- Version of Record published: January 7, 2022 (version 2)
- Version of Record updated: January 27, 2022 (version 3)
- Version of Record updated: February 3, 2022 (version 4)
Copyright
© 2021, Wong 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.
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The energetic basis for smooth human arm movements
eLife 10:e68013.
https://doi.org/10.7554/eLife.68013
Further reading
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- Computational and Systems Biology
- Medicine
Background:
Preterm birth is the leading cause of neonatal morbidity and mortality worldwide. Most cases of preterm birth occur spontaneously and result from preterm labor with intact (spontaneous preterm labor [sPTL]) or ruptured (preterm prelabor rupture of membranes [PPROM]) membranes. The prediction of spontaneous preterm birth (sPTB) remains underpowered due to its syndromic nature and the dearth of independent analyses of the vaginal host immune response. Thus, we conducted the largest longitudinal investigation targeting vaginal immune mediators, referred to herein as the immunoproteome, in a population at high risk for sPTB.
Methods:
Vaginal swabs were collected across gestation from pregnant women who ultimately underwent term birth, sPTL, or PPROM. Cytokines, chemokines, growth factors, and antimicrobial peptides in the samples were quantified via specific and sensitive immunoassays. Predictive models were constructed from immune mediator concentrations.
Results:
Throughout uncomplicated gestation, the vaginal immunoproteome harbors a cytokine network with a homeostatic profile. Yet, the vaginal immunoproteome is skewed toward a pro-inflammatory state in pregnant women who ultimately experience sPTL and PPROM. Such an inflammatory profile includes increased monocyte chemoattractants, cytokines indicative of macrophage and T-cell activation, and reduced antimicrobial proteins/peptides. The vaginal immunoproteome has improved predictive value over maternal characteristics alone for identifying women at risk for early (<34 weeks) sPTB.
Conclusions:
The vaginal immunoproteome undergoes homeostatic changes throughout gestation and deviations from this shift are associated with sPTB. Furthermore, the vaginal immunoproteome can be leveraged as a potential biomarker for early sPTB, a subset of sPTB associated with extremely adverse neonatal outcomes.
Funding:
This research was conducted by the Perinatology Research Branch, Division of Obstetrics and Maternal-Fetal Medicine, Division of Intramural Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, U.S. Department of Health and Human Services (NICHD/NIH/DHHS) under contract HHSN275201300006C. ALT, KRT, and NGL were supported by the Wayne State University Perinatal Initiative in Maternal, Perinatal and Child Health.
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- Computational and Systems Biology
- Genetics and Genomics
Runs of homozygosity (ROH) segments, contiguous homozygous regions in a genome were traditionally linked to families and inbred populations. However, a growing literature suggests that ROHs are ubiquitous in outbred populations. Still, most existing genetic studies of ROH in populations are limited to aggregated ROH content across the genome, which does not offer the resolution for mapping causal loci. This limitation is mainly due to a lack of methods for the efficient identification of shared ROH diplotypes. Here, we present a new method, ROH-DICE, to find large ROH diplotype clusters, sufficiently long ROHs shared by a sufficient number of individuals, in large cohorts. ROH-DICE identified over 1 million ROH diplotypes that span over 100 SNPs and are shared by more than 100 UK Biobank participants. Moreover, we found significant associations of clustered ROH diplotypes across the genome with various self-reported diseases, with the strongest associations found between the extended HLA region and autoimmune disorders. We found an association between a diplotype covering the HFE gene and hemochromatosis, even though the well-known causal SNP was not directly genotyped or imputed. Using a genome-wide scan, we identified a putative association between carriers of an ROH diplotype in chromosome 4 and an increase in mortality among COVID-19 patients (P-value=1.82×10-11). In summary, our ROH-DICE method, by calling out large ROH diplotypes in a large outbred population, enables further population genetics into the demographic history of large populations. More importantly, our method enables a new genome-wide mapping approach for finding disease-causing loci with multi-marker recessive effects at a population scale.
