Central nervous system modulates the neuromechanical delay in a broad range for the control of muscle force.

Force is generated by muscle units according to the neural activation sent by motor neurons. The motor unit is therefore the interface between the neural coding of movement and the musculotendinous system. Here we propose a method to accurately measure the latency between an estimate of the neural drive to muscle and force. Furthermore, we systematically investigate this latency, which we refer to as the neuromechanical delay (NMD), as a function of the rate of force generation. In two experimental sessions, eight men performed isometric finger abduction and ankle dorsiflexion sinusoidal contractions at three frequencies and peak-to-peak amplitudes {0.5, 1, and 1.5 Hz; 1, 5, and 10 of maximal force [%maximal voluntary contraction (MVC)]}, with a mean force of 10% MVC. The discharge timings of motor units of the first dorsal interosseous (FDI) and tibialis anterior (TA) muscle were identified by high-density surface EMG decomposition. The neural drive was estimated as the cumulative discharge timings of the identified motor units. The neural drive predicted 80 ± 0.4% of the force fluctuations and consistently anticipated force by 194.6 ± 55 ms (average across conditions and muscles). The NMD decreased nonlinearly with the rate of force generation ( R2 = 0.82 ± 0.07; exponential fitting) with a broad range of values (from 70 to 385 ms) and was 66 ± 0.01 ms shorter for the FDI than TA ( P < 0.001). In conclusion, we provided a method to estimate the delay between the neural control and force generation, and we showed that this delay is muscle-dependent and is modulated within a wide range by the central nervous system. NEW & NOTEWORTHY The motor unit is a neuromechanical interface that converts neural signals into mechanical force with a delay determined by neural and peripheral properties. Classically, this delay has been assessed from the muscle resting level or during electrically elicited contractions. In the present study, we introduce the neuromechanical delay as the latency between the neural drive to muscle and force during variable-force contractions, and we show that it is broadly modulated by the central nervous system.

[1]  Dario Farina,et al.  The effective neural drive to muscles is the common synaptic input to motor neurons , 2014, The Journal of physiology.

[2]  C. D. De Luca,et al.  Behaviour of human motor units in different muscles during linearly varying contractions , 1982, The Journal of physiology.

[3]  D Farina,et al.  Distribution of muscle fibre conduction velocity for representative samples of motor units in the full recruitment range of the tibialis anterior muscle , 2018, Acta physiologica.

[4]  S. McLean,et al.  Electromechanical delay in isometric actions initiated from nonresting levels. , 2001, Medicine and science in sports and exercise.

[5]  S. Zhou Acute effect of repeated maximal isometric contraction on electromechanical delay of knee extensor muscle. , 1996, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[6]  Sophia Erimaki,et al.  Neuromuscular mechanisms and neural strategies in the control of time-varying muscle contractions. , 2013, Journal of neurophysiology.

[7]  D. Farina,et al.  Accurate identification of motor unit discharge patterns from high-density surface EMG and validation with a novel signal-based performance metric , 2014, Journal of neural engineering.

[8]  R. Eston,et al.  Effects of acute fatigue on the volitional and magnetically-evoked electromechanical delay of the knee flexors in males and females , 2007, European Journal of Applied Physiology.

[9]  J. Duchateau,et al.  Motor unit behaviour and contractile changes during fatigue in the human first dorsal interosseus , 2001, The Journal of physiology.

[10]  Dario Farina,et al.  Associations between motor unit action potential parameters and surface EMG features. , 2017, Journal of applied physiology.

[11]  Jonathan P Folland,et al.  Neuromuscular performance of explosive power athletes versus untrained individuals. , 2010, Medicine and science in sports and exercise.

[12]  R. Burke Motor Units: Anatomy, Physiology, and Functional Organization , 1981 .

[13]  Shi Zhou,et al.  Electromechanical delay in isometric muscle contractions evoked by voluntary, reflex and electrical stimulation , 2004, European Journal of Applied Physiology and Occupational Physiology.

[14]  Dario Farina,et al.  Common Synaptic Input to Motor Neurons, Motor Unit Synchronization, and Force Control , 2015, Exercise and sport sciences reviews.

[15]  D. Farina,et al.  Fluctuations in isometric muscle force can be described by one linear projection of low‐frequency components of motor unit discharge rates , 2009, The Journal of physiology.

[16]  A. Manira,et al.  Principles governing recruitment of motoneurons during swimming in zebrafish , 2011, Nature Neuroscience.

[17]  P. Cavanagh,et al.  Electromechanical delay in human skeletal muscle under concentric and eccentric contractions , 1979, European Journal of Applied Physiology and Occupational Physiology.

[18]  G. Somjen,et al.  FUNCTIONAL SIGNIFICANCE OF CELL SIZE IN SPINAL MOTONEURONS. , 1965, Journal of neurophysiology.

[19]  D. Farina,et al.  Multi-channel intramuscular and surface EMG decomposition by convolutive blind source separation , 2016, Journal of neural engineering.

[20]  J. Duchateau,et al.  Mechanical properties and behaviour of motor units in the tibialis anterior during voluntary contractions. , 1997, Canadian journal of applied physiology = Revue canadienne de physiologie appliquee.

[21]  Tetsuro Muraoka,et al.  Influence of tendon slack on electromechanical delay in the human medial gastrocnemius in vivo. , 2004, Journal of applied physiology.

[22]  E. Godaux,et al.  Ballistic contractions in man: characteristic recruitment pattern of single motor units of the tibialis anterior muscle. , 1977, The Journal of physiology.

[23]  L D PARTRIDGE,et al.  MODIFICATIONS OF NEURAL OUTPUT SIGNALS BY MUSCLES: A FREQUENCY RESPONSE STUDY. , 1965, Journal of applied physiology.

[24]  M. Santello,et al.  The human central nervous system transmits common synaptic inputs to distinct motor neuron pools during non‐synergistic digit actions , 2019, The Journal of physiology.

[25]  Dario Farina,et al.  You are as fast as your motor neurons: speed of recruitment and maximal discharge of motor neurons determine the maximal rate of force development in humans , 2019, The Journal of physiology.

[26]  P. Cavallari,et al.  Motoneuronal pre‐compensation for the low‐pass filter characteristics of muscle. A quantitative appraisal in cat muscle units , 1998, The Journal of physiology.

[27]  Damjan Zazula,et al.  Multichannel Blind Source Separation Using Convolution Kernel Compensation , 2007, IEEE Transactions on Signal Processing.

[28]  Lawrence C. Rome,et al.  Why animals have different muscle fibre types , 1988, Nature.

[29]  Dario Farina,et al.  The increase in muscle force after 4 weeks of strength training is mediated by adaptations in motor unit recruitment and rate coding , 2019, The Journal of physiology.

[30]  Stefan Catheline,et al.  Electromechanical delay revisited using very high frame rate ultrasound. , 2009, Journal of applied physiology.

[31]  E. Henneman Relation between size of neurons and their susceptibility to discharge. , 1957, Science.

[32]  V G Macefield,et al.  Comparison of contractile properties of single motor units in human intrinsic and extrinsic finger muscles , 2000, The Journal of physiology.