Nonlinear Input-Output Functions of Motoneurons

Binder, Marc D.; Powers, Randall K.; Heckman, C. J.

doi:10.1152/physiol.00026.2019

Cited by 113 publications

(138 citation statements)

References 76 publications

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“…Thus, it is reasonable to speculate that the increased ΔFs observed at higher contraction intensities in the present study could result from greater serotonergic and/or noradrenergic drive. Therefore, we suggest that the contraction intensity-dependent increase in PIC amplitudes in soleus and gastrocnemius medialis, indicated by the increases in ΔFs, may result from a greater serotonergic and/or noradrenergic drive from brainstem nuclei as voluntary drive is increased 8,15 . Our results corroborate the gain control system theory developed in animal and computer modelling experiments 8 .…”

Section: Discussionmentioning

confidence: 89%

Persistent Inward Currents Increase With The Level Of Voluntary Drive In Plantar Flexor Low-Threshold Motor Units

Orssatto

Mackay

Shield

et al. 2020

Preprint

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This study tested the hypothesis that estimates of persistent inward currents (PICs) in the human plantar flexors would increase with the level of voluntary drive. Twenty-one participants volunteered for this study (29.2±2.6 years). High-density surface electromyograms were collected from soleus and gastrocnemius medialis during ramp-shaped isometric contractions to 10%, 20%, and 30% (torque rise of 2%/s and 30-s duration) of each participant’s maximal torque. Motor units identified in all the contraction intensities were included in the paired-motor unit analysis to calculate delta frequency (ΔF) and estimate the PICs. Increases in PICs were observed from 10% to 20% (Δ=0.6 pps; p<0.001) and 20% to 30% (Δ=0.5 pps; p<0.001) in soleus, and from 10% to 20% (Δ=1.2 pps; p<0.001) but not 20% to 30% (Δ=0.09 pps; p=0.724) in gastrocnemius medialis. Maximal discharge rate increased for soleus and gastrocnemius medialis from 10% to 20% (respectively, Δ=1.75 pps, p<0.001; and Δ=2.43 pps, p<0.001) and 20% to 30% (respectively, Δ=0.80 pps, p<0.017; and Δ=0.92 pps, p=002). The repeated-measures correlation identified associations between ΔF and increases in maximal discharge rate for both soleus (r=0.64; p<0.001) and gastrocnemius medialis (r=0.77; p<0.001). An increase in voluntary drive tends to increase PIC strength, which has key implications for the control of force but also for comparisons between muscles or between studies when relative force levels might be different. These data indicate that increases in voluntary descending drive amplify PICs in humans and provide an important spinal mechanism for motor unit firing, and thus force output modulation.

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Section: Discussionmentioning

confidence: 89%

Persistent Inward Currents Increase With The Level Of Voluntary Drive In Plantar Flexor Low-Threshold Motor Units

Orssatto

Mackay

Shield

et al. 2020

Preprint

View full text Add to dashboard Cite

show abstract

“…Therefore, this type of sporadic firing becomes irrelevant at higher synaptic input levels in our simulations, where most units are already recruited. Even at low- to mid-levels of synaptic input, hysteresis in motor unit recruitment (lower synaptic current required to de-recruit than recruit a motor unit) can prevent sporadic discharge ( S1(C) Fig and S1 Appendix ) and promote self-sustained discharge [ 202 ]. Low threshold units, which are most susceptible to sporadic discharge, are the most strongly affected by hysteresis-generating plateau potentials [ 128 , 129 ].…”

Section: Discussionmentioning

confidence: 99%

Force variability is mostly not motor noise: Theoretical implications for motor control

et al. 2021

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Variability in muscle force is a hallmark of healthy and pathological human behavior. Predominant theories of sensorimotor control assume ‘motor noise’ leads to force variability and its ‘signal dependence’ (variability in muscle force whose amplitude increases with intensity of neural drive). Here, we demonstrate that the two proposed mechanisms for motor noise (i.e. the stochastic nature of motor unit discharge and unfused tetanic contraction) cannot account for the majority of force variability nor for its signal dependence. We do so by considering three previously underappreciated but physiologically important features of a population of motor units: 1) fusion of motor unit twitches, 2) coupling among motoneuron discharge rate, cross-bridge dynamics, and muscle mechanics, and 3) a series-elastic element to account for the aponeurosis and tendon. These results argue strongly against the idea that force variability and the resulting kinematic variability are generated primarily by ‘motor noise.’ Rather, they underscore the importance of variability arising from properties of control strategies embodied through distributed sensorimotor systems. As such, our study provides a critical path toward developing theories and models of sensorimotor control that provide a physiologically valid and clinically useful understanding of healthy and pathologic force variability.

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“…However, coherence between motor axon stimulation and Renshaw cells does not fall below 10 Hz ( Christakos et al, 1987 ), suggesting that the non-linearity arises at the motoneuron. Motoneuron input-output properties contain substantial non-linearities ( Binder et al, 2020 ). One candidate mechanism could be the delayed inward current I h , which is activated by hyperpolarization and found in adult motoneurons ( Milligan et al, 2006 ; Howells et al, 2012 ).…”

Section: Discussionmentioning

confidence: 99%

Spatial and Temporal Arrangement of Recurrent Inhibition in the Primate Upper Limb

2020

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Renshaw cells mediate recurrent inhibition between motoneurons within the spinal cord. The function of this circuit is not clear; we previously suggested based on computational modeling that it may cancel oscillations in muscle activity around 10 Hz, thereby reducing physiological tremor. Such tremor is especially problematic for dexterous hand movements, yet knowledge of recurrent inhibitory function is sparse for the control of the primate upper limb, where no direct measurements have been made to date. In this study, we made intracellular penetrations into 89 motoneurons in the cervical enlargement of four terminally anesthetized female macaque monkeys, and recorded recurrent IPSPs in response to antidromic stimulation of motor axons. Recurrent inhibition was strongest to motoneurons innervating shoulder muscles and elbow extensors, weak to wrist and digit extensors, and almost absent to the intrinsic muscles of the hand. Recurrent inhibitory connections often spanned joints, for example from motoneurons innervating wrist and digit muscles to those controlling the shoulder and elbow. Wrist and digit flexor motoneurons sometimes inhibited the corresponding extensors, and vice versa. This complex connectivity presumably reflects the flexible usage of the primate upper limb. Using trains of stimuli to motor nerves timed as a Poisson process and coherence analysis, we also examined the temporal properties of recurrent inhibition. The recurrent feedback loop effectively carried frequencies up to 100 Hz, with a coherence peak around 20 Hz. The coherence phase validated predictions from our previous computational model, supporting the idea that recurrent inhibition may function to reduce tremor. SIGNIFICANCE STATEMENT We present the first direct measurements of recurrent inhibition in primate upper limb motoneurons, revealing that it is more flexibly organized than previous observations in cat. Recurrent inhibitory connections were relatively common between motoneurons controlling muscles that act at different joints, and between flexors and extensors. As in the cat, connections were minimal for motoneurons innervating the most distal intrinsic hand muscles. Empirical data are consistent with previous modeling: temporal properties of the recurrent inhibitory feedback loop are compatible with a role in reducing physiological tremor by suppressing oscillations around 10 Hz.

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Nonlinear Input-Output Functions of Motoneurons

Cited by 113 publications

References 76 publications

Persistent Inward Currents Increase With The Level Of Voluntary Drive In Plantar Flexor Low-Threshold Motor Units

Persistent Inward Currents Increase With The Level Of Voluntary Drive In Plantar Flexor Low-Threshold Motor Units

Force variability is mostly not motor noise: Theoretical implications for motor control

Spatial and Temporal Arrangement of Recurrent Inhibition in the Primate Upper Limb

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