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

Author(s):  
Jordyn E. Ting ◽  
Alessandro Del Vecchio ◽  
Devapratim Sarma ◽  
Samuel C. Colachis ◽  
Nicholas V. Annetta ◽  
...  

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.

Author(s):  
Jordyn E Ting ◽  
Alessandro Del Vecchio ◽  
Devapratim Sarma ◽  
Nikhil Verma ◽  
Samuel C Colachis ◽  
...  

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.


2003 ◽  
Vol 89 (4) ◽  
pp. 2065-2071 ◽  
Author(s):  
Inge Zijdewind ◽  
Christine K. Thomas

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.


2018 ◽  
Vol 120 (6) ◽  
pp. 3246-3256 ◽  
Author(s):  
Spencer A. Murphy ◽  
Francesco Negro ◽  
Dario Farina ◽  
Tanya Onushko ◽  
Matthew Durand ◽  
...  

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.


1998 ◽  
Vol 23 (1) ◽  
pp. 87-94 ◽  
Author(s):  
Christopher Rich ◽  
George L. O′Brien ◽  
Enzo Cafarelli

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


2011 ◽  
Vol 26 (1) ◽  
pp. 58-67 ◽  
Author(s):  
Inge Zijdewind ◽  
Katie Gant ◽  
Rob Bakels ◽  
Christine K. Thomas

2001 ◽  
Vol 86 (4) ◽  
pp. 1972-1982 ◽  
Author(s):  
David J. Bennett ◽  
Yunru Li ◽  
Philip J. Harvey ◽  
Monica Gorassini

Motor units of segmental tail muscles were recorded in awake rats following acute (1–2 days) and chronic (>30 days) sacral spinal cord transection to determine whether plateau potentials contributed to sustained motor-unit discharges after injury. This study was motivated by a companion in vitro study that indicated that after chronic spinal cord injury, the tail motoneurons of the sacrocaudal spinal cord exhibit persistent inward currents ( I PIC) that cause intrinsically sustained depolarizations ( plateau potentials) and firing ( self-sustained firing). Importantly, in this companion study, the plateaus were fully activated at recruitment and subsequently helped sustain the firing without causing abrupt nonlinearities in firing. That is, after recruitment and plateau activation, the firing rate was modulated relatively linearly with injected current and therefore provided a good approximation of the input to the motoneuron despite the plateau. Thus in the present study, pairs of motor units were recorded simultaneously from the same muscle, and the firing rate ( F) of the lowest-threshold unit (control unit) was used as an estimate of the synaptic input to both units. We then examined whether firing of the higher-threshold unit (test unit) was intrinsically maintained by a plateau, by determining whether more synaptic input was required to recruit the test unit than to maintain its firing. The difference in the estimated synaptic input at recruitment and de-recruitment of the test unit (i.e., change in control unit rate, Δ F) was taken as an estimate of the plateau current ( I PIC) that intrinsically sustained the firing. Slowly graded manual skin stimulation was used to recruit and then de-recruit the units. The test unit was recruited when the control unit rate was on average 17.8 and 18.9 Hz in acute and chronic spinal rats, respectively. In chronic spinal rats, the test unit was de-recruited when the control unit rate (re: estimated synaptic input) was significantly reduced, compared with at recruitment (Δ F = −5.5 Hz), and thus a plateau participated in maintaining the firing. In the lowest-threshold motor units, even a brief stimulation triggered very long-lasting firing (seconds to hours; self-sustained firing). Higher-threshold units required continuous stimulation (or a spontaneous spasm) to cause firing, but again more synaptic input was needed to recruit the unit than to maintain its firing (i.e., plateau present). In contrast, in acute spinal rats, the stimulation did not usually trigger sustained motor-unit firing that could be attributed to plateaus because Δ F was not significantly different from zero. These results indicate that plateaus play an important role in sustaining motor-unit firing in awake chronic spinal rats and thus contribute to the hyperreflexia and hypertonus associated with chronic injury.


2018 ◽  
Vol 119 (6) ◽  
pp. 2186-2193 ◽  
Author(s):  
Paola Contessa ◽  
John Letizi ◽  
Gianluca De Luca ◽  
Joshua C. Kline

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.


1997 ◽  
Vol 77 (5) ◽  
pp. 2847-2850 ◽  
Author(s):  
C. K. Thomas ◽  
B. H. Ross

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.


1996 ◽  
Vol 76 (3) ◽  
pp. 1503-1516 ◽  
Author(s):  
C. J. de Luca ◽  
P. J. Foley ◽  
Z. Erim

1. The purpose of this study was 1) to characterize the decrease observed in mean firing rates of motor units in the first 8-15 s of isometric constant-force contractions and 2) to investigate possible mechanisms that could account for the ability to maintain force output in the presence of decreasing motor unit firing rates. 2. The decrease in mean firing rates was characterized by investigating myoelectric signals detected with a specialized quadrifilar needle electrode from the first dorsal interosseus (FDI) and the tibialis anterior (TA) muscles of 19 healthy subjects during a total of 85 constant-force isometric contractions at 30, 50, or 80% of maximal effort. The firing times of motor units were obtained from the myoelectric signals with the use of computer algorithms to decompose the signal into the constituent motor unit action potentials. Time-varying mean firing rates and recruitment thresholds were also calculated. 3. Motor units detected from the TA muscle were found to have a continual decrease in their mean firing rates in 36 of 44 trials performed during isometric ankle dorsiflexion at force values ranging from 30 to 80% of maximal effort and a duration of 8-15 s. Likewise, motor units detected in the FDI muscle displayed a decrease in firing rate in 32 of 41 trials performed during constant-force isometric index finger abduction for contractions ranging from 30 to 80% of maximal effort. In 14 contractions (16% of total), firing rates were essentially constant, whereas in 3 contractions (4%), firing rates appeared to increase. 4. Motor units with the higher recruitment thresholds and lower firing rates tended to display the greater decreases in firing rate over the constant-force interval, whereas motor units with lower recruitment thresholds and higher firing rates had lesser rates of decrease. Furthermore, increasing contraction levels tended to intensify the decrease in the motor unit firing rates. 5. Three possible mechanisms were considered as factors responsible for the maintaining of force output while motor units decreased their firing rates: motor unit recruitment, agonist/antagonist interaction, and twitch potentiation. Of these, motor unit recruitment was discarded first because none was observed during the 8-15 s duration of any of the 85 contractions. Furthermore, contractions outside the physiological range of motor unit recruitment (at 80% of maximal effort) revealed the same decreasing trend in firing rates, ruling out recruitment as the means of sustaining force output. 6. The role of agonist or antagonist muscle interaction was investigated with the use of the muscles controlling the wrist joint. Myoelectric signals were recorded with quadrifilar needle electrodes from the wrist extensor muscles while myoelectric activity in the wrist flexor muscles was concurrently monitored with surface electrodes during constant-force isometric wrist extension at 50% of maximal effort. Firing rates of the motor units in the wrist extensor muscles simultaneously decreased while the flexor muscles were determined to be inactive. 7. All the findings of this study regarding the behavior of the firing rates could be well explained by the reported characteristics of twitch potentiation that have been previously documented in animals and humans. 8. The results of this study, combined with the results of other investigators, provide the following scenario to explain how a constant-force isometric contraction is sustained. As the contraction progresses, the twitch force of the muscle fibers undergoes a potentiation followed by a decrease. Simultaneously, the "late adaptation" property of the motoneuron decreases the firing rate of the motor unit. Findings of this study suggest that voluntary reduction in firing rates also cannot be ruled out as a means to augment the adaptation in motoneurons. (ABSTRACT TRUNCATED)


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