Literature DB >> 27151459

The human motor neuron pools receive a dominant slow-varying common synaptic input.

Francesco Negro1, Utku Şükrü Yavuz2, Dario Farina3.   

Abstract

KEY POINTS: Motor neurons in a pool receive both common and independent synaptic inputs, although the proportion and role of their common synaptic input is debated. Classic correlation techniques between motor unit spike trains do not measure the absolute proportion of common input and have limitations as a result of the non-linearity of motor neurons. We propose a method that for the first time allows an accurate quantification of the absolute proportion of low frequency common synaptic input (<5 Hz) to motor neurons in humans. We applied the proposed method to three human muscles and determined experimentally that they receive a similar large amount (>60%) of common input, irrespective of their different functional and control properties. These results increase our knowledge about the role of common and independent input to motor neurons in force control. ABSTRACT: Motor neurons receive both common and independent synaptic inputs. This observation is classically based on the presence of a significant correlation between pairs of motor unit spike trains. The functional significance of different relative proportions of common input across muscles, individuals and conditions is still debated. One of the limitations in our understanding of correlated input to motor neurons is that it has not been possible so far to quantify the absolute proportion of common input with respect to the total synaptic input received by the motor neurons. Indeed, correlation measures of pairs of output spike trains only allow for relative comparisons. In the present study, we report for the first time an approach for measuring the proportion of common input in the low frequency bandwidth (<5 Hz) to a motor neuron pool in humans. This estimate is based on a phenomenological model and the theoretical fitting of the experimental values of coherence between the permutations of groups of motor unit spike trains. We demonstrate the validity of this theoretical estimate with several simulations. Moreover, we applied this method to three human muscles: the abductor digiti minimi, tibialis anterior and vastus medialis. Despite these muscles having different functional roles and control properties, as confirmed by the results of the present study, we estimate that their motor pools receive a similar and large (>60%) proportion of common low frequency oscillations with respect to their total synaptic input. These results suggest that the central nervous system provides a large amount of common input to motor neuron pools, in a similar way to that for muscles with different functional and control properties.
© 2016 The Authors. The Journal of Physiology © 2016 The Physiological Society.

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Year:  2016        PMID: 27151459      PMCID: PMC5043036          DOI: 10.1113/JP271748

Source DB:  PubMed          Journal:  J Physiol        ISSN: 0022-3751            Impact factor:   5.182


  52 in total

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Journal:  Trends Neurosci       Date:  1994-07       Impact factor: 13.837

2.  The optimal neural strategy for a stable motor task requires a compromise between level of muscle cocontraction and synaptic gain of afferent feedback.

Authors:  Jakob L Dideriksen; Francesco Negro; Dario Farina
Journal:  J Neurophysiol       Date:  2015-07-22       Impact factor: 2.714

3.  Fatigue of single motor units in human masseter.

Authors:  M A Nordstrom; T S Miles
Journal:  J Appl Physiol (1985)       Date:  1990-01

4.  Corticomotoneuronal synapses in the monkey: light microscopic localization upon motoneurons of intrinsic muscles of the hand.

Authors:  D G Lawrence; R Porter; S J Redman
Journal:  J Comp Neurol       Date:  1985-02-22       Impact factor: 3.215

5.  Motor units of the human abductor digiti minimi.

Authors:  H Santo Neto; V C de Carvalho; C V Penteado
Journal:  Arch Ital Anat Embriol       Date:  1985 Jan-Mar

6.  Short-term synchrony in diverse motor nuclei presumed to receive different extents of direct cortical input.

Authors:  Douglas A Keen; Li-Wei Chou; Michael A Nordstrom; Andrew J Fuglevand
Journal:  J Neurophysiol       Date:  2012-09-26       Impact factor: 2.714

7.  The synaptic connexions to intercostal motoneurones as revealed by the average common excitation potential.

Authors:  P A Kirkwood; T A Sears
Journal:  J Physiol       Date:  1978-02       Impact factor: 5.182

8.  Spike correlations - what can they tell about synchrony?

Authors:  Tatjana Tchumatchenko; Theo Geisel; Maxim Volgushev; Fred Wolf
Journal:  Front Neurosci       Date:  2011-05-11       Impact factor: 4.677

9.  Factors influencing the estimates of correlation between motor unit activities in humans.

Authors:  Francesco Negro; Dario Farina
Journal:  PLoS One       Date:  2012-09-25       Impact factor: 3.240

10.  Motor Neuron Pools of Synergistic Thigh Muscles Share Most of Their Synaptic Input.

Authors:  Christopher M Laine; Eduardo Martinez-Valdes; Deborah Falla; Frank Mayer; Dario Farina
Journal:  J Neurosci       Date:  2015-09-02       Impact factor: 6.167

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  21 in total

1.  Exogenous neuromodulation of spinal neurons induces beta-band coherence during self-sustained discharge of hind limb motor unit populations.

Authors:  Christopher K Thompson; Michael D Johnson; Francesco Negro; Laura Miller Mcpherson; Dario Farina; Charles J Heckman
Journal:  J Appl Physiol (1985)       Date:  2019-07-18

2.  Tick-tock, spinal motor neurons go with the cortical clock in young infants.

Authors:  Francesco Lacquaniti; Myrka Zago; Dario Farina
Journal:  J Physiol       Date:  2017-02-27       Impact factor: 5.182

3.  Variability in common synaptic input to motor neurons modulates both force steadiness and pegboard time in young and older adults.

Authors:  Daniel F Feeney; Diba Mani; Roger M Enoka
Journal:  J Physiol       Date:  2018-07-04       Impact factor: 5.182

4.  A latent low-dimensional common input drives a pool of motor neurons: a probabilistic latent state-space model.

Authors:  Daniel F Feeney; François G Meyer; Nicholas Noone; Roger M Enoka
Journal:  J Neurophysiol       Date:  2017-08-02       Impact factor: 2.714

5.  Anti-phase cocontraction practice attenuates in-phase low-frequency oscillations between antagonistic muscles as assessed with phase coherence.

Authors:  Nayef E Ahmar; Jun Ueda; Minoru Shinohara
Journal:  Exp Brain Res       Date:  2019-11-28       Impact factor: 1.972

6.  Estimation of self-sustained activity produced by persistent inward currents using firing rate profiles of multiple motor units in humans.

Authors:  Babak Afsharipour; Nagib Manzur; Jennifer Duchcherer; Keith F Fenrich; Christopher K Thompson; Francesco Negro; Katharina A Quinlan; David J Bennett; Monica A Gorassini
Journal:  J Neurophysiol       Date:  2020-05-27       Impact factor: 2.714

7.  Decrease in force steadiness with aging is associated with increased power of the common but not independent input to motor neurons.

Authors:  Anna Margherita Castronovo; Natalie Mrachacz-Kersting; Andrew James Thomas Stevenson; Ales Holobar; Roger Maro Enoka; Dario Farina
Journal:  J Neurophysiol       Date:  2018-07-05       Impact factor: 2.714

8.  SK channel inhibition mediates the initiation and amplitude modulation of synchronized burst firing in the spinal cord.

Authors:  Amr A Mahrous; Sherif M Elbasiouny
Journal:  J Neurophysiol       Date:  2017-03-29       Impact factor: 2.714

9.  Fatigue-related modulation of low-frequency common drive to motor units.

Authors:  Ing-Shiou Hwang; Yen-Ting Lin; Chien-Chun Huang; Yi-Ching Chen
Journal:  Eur J Appl Physiol       Date:  2020-04-15       Impact factor: 3.078

10.  Synergistic Organization of Neural Inputs from Spinal Motor Neurons to Extrinsic and Intrinsic Hand Muscles.

Authors:  Simone Tanzarella; Silvia Muceli; Marco Santello; Dario Farina
Journal:  J Neurosci       Date:  2021-07-01       Impact factor: 6.167

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