Motor unit firing rates during spasms in thenar muscles of spinal cord injured subjects

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.

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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.

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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.

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Effects Of Resistance Training On Maximal Motor Unit Firing Rates In Young And Older Males

Medicine & Science in Sports & Exercise ◽

10.1249/01.mss.0000536499.08903.69 ◽

2018 ◽

Vol 50 (5S) ◽

pp. 429-430

Author(s):

Phuong L. Ha ◽

Garrett M. Hester ◽

Ryan J. Colquhoun ◽

Mitchel A. Magrini ◽

Zachary K. Pope ◽

...

Keyword(s):

Resistance Training ◽

Motor Unit ◽

Firing Rates ◽

Motor Unit Firing ◽

Older Males

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Neuromuscular drive and force production are not altered during bilateral contractions

Journal of Applied Physiology ◽

10.1152/jappl.1998.84.1.200 ◽

1998 ◽

Vol 84 (1) ◽

pp. 200-206 ◽

Cited By ~ 56

Author(s):

J. M. Jakobi ◽

E. Cafarelli

Keyword(s):

Motor Unit ◽

Force Production ◽

Young Male ◽

Neuromuscular Control ◽

Force Generation ◽

Isometric Contractions ◽

Firing Rates ◽

Significant Limitation ◽

Motor Unit Firing ◽

Male Subjects

Jakobi, J. M., and E. Cafarelli. Neuromuscular drive and force production are not altered during bilateral contractions. J. Appl. Physiol. 84(1): 200–206, 1998.—Several investigators have studied the deficit in maximal voluntary force that is said to occur when bilateral muscle groups contract simultaneously. A true bilateral deficit (BLD) would suggest a significant limitation of neuromuscular control; however, some of the data from studies in the literature are equivocal. Our purpose was to determine whether there is a BLD in the knee extensors of untrained young male subjects during isometric contractions and whether this deficit is associated with a decreased activation of the quadriceps, increased activation of the antagonist muscle, or an alteration in motor unit firing rates. Twenty subjects performed unilateral (UL) and bilateral (BL) isometric knee extensions at 25, 50, 75, and 100% maximal voluntary contraction. Total UL and BL force (Δ3%) and maximal rate of force generation (Δ2.5%) were not significantly different. Total UL and BL maximal vastus lateralis electromyographic activity (EMG; 2.7 ± 0.28 vs. 2.6 ± 0.24 mV) and coactivation (0.17 ± 0.02 vs. 0.20 ± 0.02 mV) were also not different. Similarly, the ratio of force to EMG during submaximal UL and BL contractions was not different. Analysis of force production by each leg in UL and BL conditions showed no differences in force, rate of force generation, EMG, motor unit firing rates, and coactivation. Finally, assessment of quadriceps activity with the twitch interpolation technique indicated no differences in the degree of voluntary muscle activation (UL: 93.6 ± 2.51 Hz, BL: 90.1 ± 2.43 Hz). These results provide no evidence of a significant limitation in neuromuscular control between BL and UL isometric contractions of the knee extensor muscles in young male subjects.

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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.

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