Literature DB >> 28356469

PICs in motoneurons do not scale with the size of the animal: a possible mechanism for faster speed of muscle contraction in smaller species.

Seoan Huh1, Ramamurthy Siripuram2, Robert H Lee2, Vladimir V Turkin3, Derek O'Neill3, Thomas M Hamm3, Charles J Heckman1,4,5, Marin Manuel6,7.   

Abstract

The majority of studies on the electrical properties of neurons are carried out in rodents, and in particular in mice. However, the minute size of this animal compared with humans potentially limits the relevance of the resulting insights. To be able to extrapolate results obtained in a small animal such as a rodent, one needs to have proper knowledge of the rules governing how electrical properties of neurons scale with the size of the animal. Generally speaking, electrical resistances of neurons increase as cell size decreases, and thus maintenance of equal depolarization across cells of different sizes requires the underlying currents to decrease in proportion to the size decrease. Thus it would generally be expected that voltage-sensitive currents are smaller in smaller animals. In this study, we used in vivo preparations to record electrical properties of spinal motoneurons in deeply anesthetized adult mice and cats. We found that PICs do not scale with size, but instead are constant in their amplitudes across these species. This constancy, coupled with the threefold differences in electrical resistances, means that PICs contribute a threefold larger depolarization in the mouse than in the cat. As a consequence, motoneuronal firing rate sharply increases as animal size decreases. These differences in firing rates are likely essential in allowing different species to control muscles with widely different contraction speeds (smaller animals have faster muscle fibers). Thus from our results we have identified a possible new mechanism for how electrical properties are tuned to match mechanical properties within the motor output system.NEW & NOTEWORTHY The small size of the mouse warrants concern over whether the properties of their neurons are a scaled version of those in larger animals or instead have unique features. Comparison of spinal motoneurons in mice to cats showed unique features. Firing rates in the mouse were much higher, in large part due to relatively larger persistent inward currents. These differences likely reflect adaptations for controlling much faster muscle fibers in mouse than cat.
Copyright © 2017 the American Physiological Society.

Entities:  

Keywords:  adult spinal motoneurons; electrical properties; persistent inward currents; voltage clamp

Mesh:

Year:  2017        PMID: 28356469      PMCID: PMC5494365          DOI: 10.1152/jn.00045.2017

Source DB:  PubMed          Journal:  J Neurophysiol        ISSN: 0022-3077            Impact factor:   2.714


  43 in total

1.  Essential role of a fast persistent inward current in action potential initiation and control of rhythmic firing.

Authors:  R H Lee; C J Heckman
Journal:  J Neurophysiol       Date:  2001-01       Impact factor: 2.714

2.  Persistent sodium currents and repetitive firing in motoneurons of the sacrocaudal spinal cord of adult rats.

Authors:  P J Harvey; Y Li; X Li; D J Bennett
Journal:  J Neurophysiol       Date:  2005-11-09       Impact factor: 2.714

3.  Mixed mode oscillations in mouse spinal motoneurons arise from a low excitability state.

Authors:  Caroline Iglesias; Claude Meunier; Marin Manuel; Yulia Timofeeva; Nicolas Delestrée; Daniel Zytnicki
Journal:  J Neurosci       Date:  2011-04-13       Impact factor: 6.167

4.  Persistent currents and discharge patterns in rat hindlimb motoneurons.

Authors:  Thomas M Hamm; Vladimir V Turkin; Neha K Bandekar; Derek O'Neill; Ranu Jung
Journal:  J Neurophysiol       Date:  2010-06-30       Impact factor: 2.714

5.  Cell body size and succinate dehydrogenase activity of spinal motoneurons innervating the soleus muscle in mice, rats, and cats.

Authors:  A Ishihara; Y Ohira; M Tanaka; W Nishikawa; N Ishioka; A Higashibata; R Izumi; T Shimazu; Y Ibata
Journal:  Neurochem Res       Date:  2001-12       Impact factor: 3.996

Review 6.  Dynamic properties of mammalian skeletal muscles.

Authors:  R I Close
Journal:  Physiol Rev       Date:  1972-01       Impact factor: 37.312

7.  Triceps surae motoneuron morphology in the rat: a quantitative light microscopic study.

Authors:  X Y Chen; J R Wolpaw
Journal:  J Comp Neurol       Date:  1994-05-01       Impact factor: 3.215

8.  The effects of general anesthetics on excitatory and inhibitory synaptic transmission in area CA1 of the rat hippocampus in vitro.

Authors:  M Wakasugi; K Hirota; S H Roth; Y Ito
Journal:  Anesth Analg       Date:  1999-03       Impact factor: 5.108

9.  Frequency-current relationships of rat hindlimb alpha-motoneurones.

Authors:  Duane C Button; Kalan Gardiner; Tanguy Marqueste; Phillip F Gardiner
Journal:  J Physiol       Date:  2006-04-13       Impact factor: 5.182

10.  Soleus motor units in chronic spinal transected cats: physiological and morphological alterations.

Authors:  T C Cope; S C Bodine; M Fournier; V R Edgerton
Journal:  J Neurophysiol       Date:  1986-06       Impact factor: 2.714

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  7 in total

1.  Meta-analysis of biological variables' impact on spinal motoneuron electrophysiology data.

Authors:  Morgan M Highlander; John M Allen; Sherif M Elbasiouny
Journal:  J Neurophysiol       Date:  2020-02-19       Impact factor: 2.714

Review 2.  Scaling of Motor Output, From Mouse to Humans.

Authors:  Marin Manuel; Matthieu Chardon; Vicki Tysseling; C J Heckman
Journal:  Physiology (Bethesda)       Date:  2019-01-01

3.  Time Course of Alterations in Adult Spinal Motoneuron Properties in the SOD1(G93A) Mouse Model of ALS.

Authors:  Seoan Huh; Charles J Heckman; Marin Manuel
Journal:  eNeuro       Date:  2021-03-22

4.  Intrinsic motoneuron excitability is reduced in soleus and tibialis anterior of older adults.

Authors:  Lucas B R Orssatto; David N Borg; Anthony J Blazevich; Raphael L Sakugawa; Anthony J Shield; Gabriel S Trajano
Journal:  Geroscience       Date:  2021-10-30       Impact factor: 7.713

5.  Effects of reciprocal inhibition and whole-body relaxation on persistent inward currents estimated by two different methods.

Authors:  Ricardo N O Mesquita; Janet L Taylor; Gabriel S Trajano; Jakob Škarabot; Aleš Holobar; Basílio A M Gonçalves; Anthony J Blazevich
Journal:  J Physiol       Date:  2022-05-19       Impact factor: 6.228

Review 6.  Voluntary activation of muscle in humans: does serotonergic neuromodulation matter?

Authors:  Justin J Kavanagh; Janet L Taylor
Journal:  J Physiol       Date:  2022-08-01       Impact factor: 6.228

7.  Hypoexcitability precedes denervation in the large fast-contracting motor units in two unrelated mouse models of ALS.

Authors:  María de Lourdes Martínez-Silva; Rebecca D Imhoff-Manuel; Aarti Sharma; C J Heckman; Neil A Shneider; Francesco Roselli; Daniel Zytnicki; Marin Manuel
Journal:  Elife       Date:  2018-03-27       Impact factor: 8.140

  7 in total

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