The motor neuron recruitment strategy and muscle anatomical properties determine the influence of synaptic noise on the variability of motor output
-
1
Bernstein Focus Neurotechnology Göttingen, University Medical Center Göttingen, Georg-August University, Department of Neurorehabilitation Engineering, Germany
-
2
Aalborg University, Department of Health Science and Technology, Denmark
During muscle contraction, alpha motor neurons receive synaptic input from tens of thousands of neural connections, causing continuous fluctuations of the membrane voltage (synaptic noise) and resulting in variability in the times of occurrence of action potentials (Berg et al., 2007). This inherent variability may determine unstable motor output. We hypothesized that in human muscles the influence of synaptic noise on the stability of motor output would be limited by the mechanisms of transduction into force (spatial and temporal summation of force twitches) so that the synaptic noise at motor neurons would be a limiting factor in motor output stability only for a small range of generated forces. To verify this hypothesis we described force generation analytically and we simulated it by a computational model of motor unit population and realistic descending motor commands (Dideriksen et al., 2010). The simulations varied the contraction force, the level of synaptic noise, the motor neuron population size (100-500), the recruitment range (40-70% of the maximal force, MVC), and the motor unit twitch contraction times (slowest fiber: 45-180 ms; fastest fiber: 15-60 ms).
The simulations indicated that once the generated force exceeded a certain threshold, primarily the low-frequency components of the descending drive were reflected in the force variability, whereas synaptic noise was almost completely filtered out. This was reflected in a gradual decrease in the correlation between the discharge time variability and the force variability as contraction force increased, whereas the correlation between the variability of the descending drive and force variability was not influenced by the generated force. These simulation results were explained by the analytical derivation as the combination of the low-pass filtering effects related to the convolution with the motor unit twitches (temporal summation) and the averaging filter performed by the summation of single motor unit forces (spatial summation). The force value above which synaptic noise did not influence the stability of force varied with recruitment range and muscle properties, however for typical values for these parameters it was smaller than 10% MVC.
In conclusion, the motor neuron recruitment strategy and muscle properties in typical muscles are tuned so that the influence of synaptic noise on motor output stability is limited to relatively low forces only. For greater forces, the synaptic noise is not anymore a limiting factor and force variability is determined by the low-frequency oscillations in motor neuron discharge rate which are due to the ability of the central nervous system to generate a stable neural drive to muscles when integrated with afferent input.
Acknowledgements
We acknowledge financial support by the German Ministry for Education and Research (BMBF) via the Bernstein Focus Neurotechnology (BFNT) Göttingen under Grant No. 01GQ0810.
References
Berg RW, Alaburda A, Hounsgaard J., 2007. Balanced inhibition and excitation drive spike activity in spinal half-centers. Science 315(5810).
Dideriksen JL, Farina D, Baekgaard M, Enoka RM., 2010. An integrative model of motor unit activity during sustained submaximal contractions. J Appl Physiol, 108(6).
Keywords:
force steadiness,
motor control,
motor neuron,
recruitment,
synaptic noise
Conference:
BC11 : Computational Neuroscience & Neurotechnology Bernstein Conference & Neurex Annual Meeting 2011, Freiburg, Germany, 4 Oct - 6 Oct, 2011.
Presentation Type:
Poster
Topic:
motor control (please use "motor control" as keyword)
Citation:
Negro
F,
Dideriksen
JL and
Farina
D
(2011). The motor neuron recruitment strategy and muscle anatomical properties determine the influence of synaptic noise on the variability of motor output.
Front. Comput. Neurosci.
Conference Abstract:
BC11 : Computational Neuroscience & Neurotechnology Bernstein Conference & Neurex Annual Meeting 2011.
doi: 10.3389/conf.fncom.2011.53.00196
Copyright:
The abstracts in this collection have not been subject to any Frontiers peer review or checks, and are not endorsed by Frontiers.
They are made available through the Frontiers publishing platform as a service to conference organizers and presenters.
The copyright in the individual abstracts is owned by the author of each abstract or his/her employer unless otherwise stated.
Each abstract, as well as the collection of abstracts, are published under a Creative Commons CC-BY 4.0 (attribution) licence (https://creativecommons.org/licenses/by/4.0/) and may thus be reproduced, translated, adapted and be the subject of derivative works provided the authors and Frontiers are attributed.
For Frontiers’ terms and conditions please see https://www.frontiersin.org/legal/terms-and-conditions.
Received:
19 Aug 2011;
Published Online:
04 Oct 2011.
*
Correspondence:
Prof. Dario Farina, Bernstein Focus Neurotechnology Göttingen, University Medical Center Göttingen, Georg-August University, Department of Neurorehabilitation Engineering, Göttingen, 37075, Germany, d.farina@imperial.ac.uk