Sensing and decoding the neural drive to paralyzed muscles during attempted movements of a person with tetraplegia using a sleeve array

Motor neurons convey information about motor intent that can be extracted and interpreted to control assistive devices. However, most methods for measuring the firing activity of single neurons rely on implanted microelectrodes. Although intracortical brain-computer interfaces (BCIs) have been shown to be safe and effective, the requirement for surgery poses a barrier to widespread use that can be mitigated by instead using noninvasive interfaces. The objective of this study was to evaluate the feasibility of deriving motor control signals from a wearable sensor that can detect residual motor unit activity in paralyzed muscles after chronic cervical spinal cord injury (SCI). Despite generating no observable hand movement, volitional recruitment of motor units below the level of injury was observed across attempted movements of individual fingers and overt wrist and elbow movements. Subgroups of motor units were coactive during flexion or extension phases of the task. Single digit movement intentions were classified offline from the EMG power (RMS) or motor unit firing rates with median classification accuracies >75% in both cases. Simulated online control of a virtual hand was performed with a binary classifier to test feasibility of real-time extraction and decoding of motor units. The online decomposition algorithm extracted motor units in 1.2 ms, and the firing rates predicted the correct digit motion 88 ± 24% of the time. This study provides the first demonstration of a wearable interface for recording and decoding firing rates of motor units below the level of injury in a person with motor complete SCI.

Download Full-text

Motor Unit Firing During and After Voluntary Contractions of Human Thenar Muscles Weakened by Spinal Cord Injury

Journal of Neurophysiology ◽

10.1152/jn.00492.2002 ◽

2003 ◽

Vol 89 (4) ◽

pp. 2065-2071 ◽

Cited By ~ 49

Author(s):

Inge Zijdewind ◽

Christine K. Thomas

Keyword(s):

Spinal Cord ◽

Spinal Cord Injury ◽

Motor Unit ◽

Cervical Spinal Cord ◽

Motor Units ◽

Firing Rates ◽

Rate Modulation ◽

Motor Unit Firing ◽

Cord Injury ◽

Voluntary Contractions

Spinal cord injury may change both the distribution and the strength of the synaptic input within a motoneuron pool and therefore alter force gradation. Here, we have studied the relative contributions of motor unit recruitment and rate modulation to force gradation during voluntary contractions of thenar muscles performed by five individuals with chronic (>1 yr) cervical spinal cord injury. Mean ± SD thenar unit firing rates were low during both steady-level 25% (8.3 ± 2.2 Hz, n = 27 units) and 100% maximal voluntary contractions (MVCs, 9.2 ± 3.1 Hz, n = 23 units). Thus modest rate modulation, or a lack of it in some units, was seen despite an average fourfold increase in integrated surface electromyographic activity and force. During ramp contractions, units were recruited at 5.7 ± 2.5 Hz, but still only reached maximal firing rates of 12.8 ± 4.9 Hz. Motor units were recruited up to 85% of the maximal force achieved (14.6 ± 5.6 N). In contrast, unit recruitment in control hand muscles is largely complete by 30% MVC. Thus, during voluntary contractions of thenar muscles weakened by cervical spinal cord injury, motor unit rate modulation was limited and recruitment occurred over a wider than usual force range. Those motor units that were stopped voluntarily had significantly lower derecruitment versus recruitment thresholds. However, 8 units (24%) continued to fire long after the signal to end the voluntary contraction at a mean frequency of 5.9 ± 0.8 Hz. The forces generated by this prolonged unit activity ranged from 0.3 to 7.2% maximum. Subjects were unable to stop this involuntary unit activity even with the help of feedback. The mechanisms that underlie this prolonged motor unit firing need to be explored further.

Download Full-text

Sensing and decoding the neural drive to paralyzed muscles during attempted movements of a person with tetraplegia using a sleeve array

10.1101/2021.02.24.21250962 ◽

2021 ◽

Cited By ~ 1

Author(s):

Jordyn E. Ting ◽

Alessandro Del Vecchio ◽

Devapratim Sarma ◽

Samuel C. Colachis ◽

Nicholas V. Annetta ◽

...

Keyword(s):

Spinal Cord ◽

Motor Unit ◽

Motor Neurons ◽

Motor Units ◽

Robotic Manipulators ◽

Assistive Devices ◽

Wearable Sensor ◽

Myoelectric Signals ◽

Firing Rates ◽

Motor Unit Firing

AbstractMotor neurons in the brain and spinal cord convey information about motor intent that can be extracted and interpreted to control assistive devices, such as computers, wheelchairs, and robotic manipulators. However, most methods for measuring the firing activity of single neurons rely on implanted microelectrodes. Although intracortical brain-computer interfaces (BCIs) have been shown to be safe and effective, the requirement for surgery poses a barrier to widespread use. Here, we demonstrate that a wearable sensor array can detect residual motor unit activity in paralyzed muscles after severe cervical spinal cord injury (SCI). Despite generating no observable hand movement, volitional recruitment of motor neurons below the level of injury was observed across attempted movements of individual fingers and overt wrist and elbow movements. Subgroups of motor units were coactive during flexion or extension phases of the task. Single digit movement intentions were classified offline from the EMG power (RMS) or motor unit firing rates with median classification accuracies >75% in both cases. Simulated online control of a virtual hand was performed with a binary classifier to test feasibility of real time extraction and decoding of motor units. The online decomposition algorithm extracted motor units in 1.2 ms, and the firing rates predicted the correct digit motion 88 ± 24% of the time. This study provides the first demonstration of a wearable interface for recording and decoding firing rates of motor neurons below the level of injury in a person with tetraplegia after motor complete SCI.Significance StatementA wearable electrode array and machine learning methods were used to record and decode myoelectric signals and motor unit firing in paralyzed muscles of a person with motor complete tetraplegia. Motor unit action potentials were extracted from myoelectric signals during attempted movements of the fingers and voluntary movements of the wrist and elbow. The patterns of EMG and motor unit firing rates were highly task-specific, even in the absence of visible motion in the limb, enabling accurate classification of attempted movements of single digits. These results demonstrate the potential to create a wearable sensor for determining movement intentions from spared motor neurons, which may enable people with severe tetraplegia to control assistive devices such as computers, wheelchairs, and robotic manipulators.

Download Full-text

Stroke increases ischemia-related decreases in motor unit discharge rates

Journal of Neurophysiology ◽

10.1152/jn.00923.2017 ◽

2018 ◽

Vol 120 (6) ◽

pp. 3246-3256 ◽

Cited By ~ 2

Author(s):

Spencer A. Murphy ◽

Francesco Negro ◽

Dario Farina ◽

Tanya Onushko ◽

Matthew Durand ◽

...

Keyword(s):

Motor Unit ◽

Time Constant ◽

Motor Units ◽

Unit Discharge ◽

Firing Rates ◽

Sensory Pathways ◽

Discharge Rates ◽

Motor Unit Firing ◽

Motor Unit Discharge ◽

Density Surface

Following stroke, hyperexcitable sensory pathways, such as the group III/IV afferents that are sensitive to ischemia, may inhibit paretic motor neurons during exercise. We quantified the effects of whole leg ischemia on paretic vastus lateralis motor unit firing rates during submaximal isometric contractions. Ten chronic stroke survivors (>1 yr poststroke) and 10 controls participated. During conditions of whole leg occlusion, the discharge timings of motor units were identified from decomposition of high-density surface electromyography signals during repeated submaximal knee extensor contractions. Quadriceps resting twitch responses and near-infrared spectroscopy measurements of oxygen saturation as an indirect measure of blood flow were made. There was a greater decrease in paretic motor unit discharge rates during the occlusion compared with the controls (average decrease for stroke and controls, 12.3 ± 10.0% and 0.1 ± 12.4%, respectively; P < 0.001). The motor unit recruitment thresholds did not change with the occlusion (stroke: without occlusion, 11.68 ± 5.83%MVC vs. with occlusion, 11.11 ± 5.26%MVC; control: 11.87 ± 5.63 vs. 11.28 ± 5.29%MVC). Resting twitch amplitudes declined similarly for both groups in response to whole leg occlusion (stroke: 29.16 ± 6.88 vs. 25.75 ± 6.78 Nm; control: 38.80 ± 13.23 vs 30.14 ± 9.64 Nm). Controls had a greater exponential decline (lower time constant) in oxygen saturation compared with the stroke group (stroke time constant, 22.90 ± 10.26 min vs. control time constant, 5.46 ± 4.09 min; P < 0.001). Ischemia of the muscle resulted in greater neural inhibition of paretic motor units compared with controls and may contribute to deficient muscle activation poststroke. NEW & NOTEWORTHY Hyperexcitable inhibitory sensory pathways sensitive to ischemia may play a role in deficient motor unit activation post stroke. Using high-density surface electromyography recordings to detect motor unit firing instances, we show that ischemia of the exercising muscle results in greater inhibition of paretic motor unit firing rates compared with controls. These findings are impactful to neurophysiologists and clinicians because they implicate a novel mechanism of force-generating impairment poststroke that likely exacerbates baseline weakness.

Download Full-text

Probabilities Associated With Counting Average Motor Unit Firing Rates in Active Human Muscle

Canadian Journal of Applied Physiology ◽

10.1139/h98-006 ◽

1998 ◽

Vol 23 (1) ◽

pp. 87-94 ◽

Cited By ~ 8

Author(s):

Christopher Rich ◽

George L. O′Brien ◽

Enzo Cafarelli

Keyword(s):

Motor Unit ◽

Vastus Lateralis ◽

Small Diameter ◽

Motor Units ◽

Voluntary Contraction ◽

Human Muscle ◽

Cell Diameter ◽

Unit Recording ◽

Firing Rates ◽

Motor Unit Firing

Motor unit firing rates in human muscle can be determined from recordings made with small-diameter microelectrodes inserted directly into the muscle during voluntary contraction. Frequently, these counts are pooled to give an average motor unit firing rate under a given set of conditions. Since the fibers of one motor unit are dispersed among the cells of several others, it is conceivable that discharge rates can be measured in more than one cell from the same unit. If this occurred frequently, the distribution of firing rates could be influenced by those from units counted more than once. Based on literature values, we made the following assumptions: vastus lateralis contains approximately 300 motor units, with an average innervation ratio of 1500. Muscle cell diameter is about 50 to 100 μm and cells are randomly distributed over a motor unit territory of 10 μm diameter. The recording range of a microelectrode is about 600 μm. Given the distribution of cells normally found in whole human muscle, the probability of recording from two or more cells of the same motor unit at 50% MVC follows a Poisson distribution with a mean of 0.44. This model suggests that although there is a low probability of some duplication in this technique, the extent to which it influences the distribution of average motor unit firing rates is minimal over the entire range of forces produced by vastus lateralis. Key words: probability, motor unit, single unit recording, human muscle, rate coding

Download Full-text

Do Additional Inputs Change Maximal Voluntary Motor Unit Firing Rates After Spinal Cord Injury?

Neurorehabilitation and Neural Repair ◽

10.1177/1545968311417449 ◽

2011 ◽

Vol 26 (1) ◽

pp. 58-67 ◽

Cited By ~ 13

Author(s):

Inge Zijdewind ◽

Katie Gant ◽

Rob Bakels ◽

Christine K. Thomas

Keyword(s):

Spinal Cord ◽

Spinal Cord Injury ◽

Motor Unit ◽

Firing Rates ◽

Voluntary Motor ◽

Motor Unit Firing ◽

Cord Injury

Download Full-text

Contribution from motor unit firing adaptations and muscle coactivation during fatigue

Journal of Neurophysiology ◽

10.1152/jn.00766.2017 ◽

2018 ◽

Vol 119 (6) ◽

pp. 2186-2193 ◽

Cited By ~ 10

Author(s):

Paola Contessa ◽

John Letizi ◽

Gianluca De Luca ◽

Joshua C. Kline

Keyword(s):

Motor Unit ◽

Late Phase ◽

Motor Units ◽

Force Output ◽

Firing Behavior ◽

Firing Rates ◽

Pronator Teres ◽

Motor Unit Firing ◽

The Central Nervous System ◽

Extensor Carpi Radialis

The control of motor unit firing behavior during fatigue is still debated in the literature. Most studies agree that the central nervous system increases the excitation to the motoneuron pool to compensate for decreased force contributions of individual motor units and sustain muscle force output during fatigue. However, some studies claim that motor units may decrease their firing rates despite increased excitation, contradicting the direct relationship between firing rates and excitation that governs the voluntary control of motor units. To investigate whether the control of motor units in fact changes with fatigue, we measured motor unit firing behavior during repeated contractions of the first dorsal interosseous (FDI) muscle while concurrently monitoring the activation of surrounding muscles, including the flexor carpi radialis, extensor carpi radialis, and pronator teres. Across all subjects, we observed an overall increase in FDI activation and motor unit firing rates by the end of the fatigue task. However, in some subjects we observed increases in FDI activation and motor unit firing rates only during the initial phase of the fatigue task, followed by subsequent decreases during the late phase of the fatigue task while the coactivation of surrounding muscles increased. These findings indicate that the strategy for sustaining force output may occasionally change, leading to increases in the relative activation of surrounding muscles while the excitation to the fatiguing muscle decreases. Importantly, irrespective of changes in the strategy for sustaining force output, the control properties regulating motor unit firing behavior remain unchanged during fatigue. NEW & NOTEWORTHY This work addresses sources of debate surrounding the manner in which motor unit firing behavior is controlled during fatigue. We found that decreases in the motor unit firing rates of the fatiguing muscle may occasionally be observed when the contribution of coactive muscles increases. Despite changes in the strategy employed to sustain the force output, the underlying control properties regulating motor unit firing behavior remain unchanged during muscle fatigue.

Download Full-text

Distinct Patterns of Motor Unit Behavior During Muscle Spasms in Spinal Cord Injured Subjects

Journal of Neurophysiology ◽

10.1152/jn.1997.77.5.2847 ◽

1997 ◽

Vol 77 (5) ◽

pp. 2847-2850 ◽

Cited By ~ 31

Author(s):

C. K. Thomas ◽

B. H. Ross

Keyword(s):

Spinal Cord ◽

Spinal Cord Injury ◽

Motor Unit ◽

Motor Units ◽

Triceps Surae ◽

Firing Rates ◽

Rate Modulation ◽

Cord Injury ◽

Muscle Spasms ◽

Spinal Cord Injured

Thomas, C. K. and B. H. Ross. Distinct patterns of motor unit behavior during muscle spasms in spinal cord injured subjects. J. Neurophysiol. 77: 2847–2850, 1997. Surface electromyograms (EMG) and force were recorded during repeated involuntary spasms of paralyzed triceps surae muscles of four men with chronic cervical spinal cord injury. The firing rates of 78 medial gastrocnemius (MG) motor units also were recorded intramuscularly with tungsten microelectrodes. Spasms typically involved a relatively rapid rise, then a more gradual fall in triceps surae EMG and torque. Motor unit firing rates either increased and then decreased with the spasm intensity (54%) or were relatively constant (26%), firing mainly at 2–10 Hz. The remaining units (20%) produced trains that included one or several doublets. Mean peak spasm firing rates were 18 ± 9 Hz (mean ± SD) for rate modulated units and 11 ± 10 Hz for units with little or no rate modulation. Some motor units fired at rates comparable with those recorded previously during maximum voluntary contractions performed by intact subjects. Others fired at rates below the minimum usually seen when normal units are first recruited (<6 Hz). Doublets (interspike interval <10 ms) often repeated every 123–333 ms, or were interspersed in trains firing at low steady rates (<11 Hz). This study shows that rate coding for many motor units appears to be similar whether descending motor input is intact or whether it has been reduced severely by spinal cord injury. In contrast, rate modulation in other units appears to depend mainly on voluntary motor commands.

Download Full-text

Respiration-related discharge of hyoglossus muscle motor units in the rat

Journal of Neurophysiology ◽

10.1152/jn.00670.2013 ◽

2014 ◽

Vol 111 (2) ◽

pp. 361-368 ◽

Cited By ~ 7

Author(s):

Gregory L. Powell ◽

Amber Rice ◽

Seres J. Bennett-Cross ◽

Ralph F. Fregosi

Keyword(s):

Motor Unit ◽

Muscle Force ◽

Critical Role ◽

Motor Units ◽

Respiratory Cycle ◽

Firing Rates ◽

Rate Modulation ◽

Inspiratory Phase ◽

Anesthetized Rats ◽

Motor Unit Firing

Although respiratory muscle motor units have been studied during natural breathing, simultaneous measures of muscle force have never been obtained. Tongue retractor muscles, such as the hyoglossus (HG), play an important role in swallowing, licking, chewing, breathing, and, in humans, speech. The HG is phasically recruited during the inspiratory phase of the respiratory cycle. Moreover, in urethane anesthetized rats the drive to the HG waxes and wanes spontaneously, providing a unique opportunity to study motor unit firing patterns as the muscle is driven naturally by the central pattern generator for breathing. We recorded tongue retraction force, the whole HG muscle EMG and the activity of 38 HG motor units in spontaneously breathing anesthetized rats under low-force and high-force conditions. Activity in all cases was confined to the inspiratory phase of the respiratory cycle. Changes in the EMG were correlated significantly with corresponding changes in force, with the change in EMG able to predict 53–68% of the force variation. Mean and peak motor unit firing rates were greater under high-force conditions, although the magnitude of discharge rate modulation varied widely across the population. Changes in mean and peak firing rates were significantly correlated with the corresponding changes in force, but the correlations were weak ( r2 = 0.27 and 0.25, respectively). These data indicate that, during spontaneous breathing, recruitment of HG motor units plays a critical role in the control of muscle force, with firing rate modulation playing an important but lesser role.

Download Full-text

Restoration of breathing after opioid overdose and spinal cord injury using temporal interference stimulation

Communications Biology ◽

10.1038/s42003-020-01604-x ◽

2021 ◽

Vol 4 (1) ◽

Author(s):

Michael D. Sunshine ◽

Antonino M. Cassarà ◽

Esra Neufeld ◽

Nir Grossman ◽

Thomas H. Mareci ◽

...

Keyword(s):

Spinal Cord ◽

Spinal Cord Injury ◽

Motor Neurons ◽

Drug Overdose ◽

Cervical Spinal Cord ◽

Opioid Overdose ◽

Electrode Position ◽

Spinal Motor Neurons ◽

Cord Injury ◽

Low Amplitude

AbstractRespiratory insufficiency is a leading cause of death due to drug overdose or neuromuscular disease. We hypothesized that a stimulation paradigm using temporal interference (TI) could restore breathing in such conditions. Following opioid overdose in rats, two high frequency (5000 Hz and 5001 Hz), low amplitude waveforms delivered via intramuscular wires in the neck immediately activated the diaphragm and restored ventilation in phase with waveform offset (1 Hz or 60 breaths/min). Following cervical spinal cord injury (SCI), TI stimulation via dorsally placed epidural electrodes uni- or bilaterally activated the diaphragm depending on current and electrode position. In silico modeling indicated that an interferential signal in the ventral spinal cord predicted the evoked response (left versus right diaphragm) and current-ratio-based steering. We conclude that TI stimulation can activate spinal motor neurons after SCI and prevent fatal apnea during drug overdose by restoring ventilation with minimally invasive electrodes.

Download Full-text