Preparatory activity links frontal eye field activity with small amplitude motor unit recruitment of neck muscles during gaze planning

Author(s):  
Satya Prakash Rungta ◽  
Debaleena Basu ◽  
Naveen Sendhilnathan ◽  
Aditya Murthy

A hallmark of intelligent behavior is that we can separate intention from action. To understand the mechanism that gates the flow of information between motor planning and execution, we compared the activity of frontal eye field neurons with motor unit activity from neck muscles in the presence of an intervening delay period in which spatial information regarding the target was available to plan a response. Whereas spatially-specific delay period activity was present in the activity of frontal eye field neurons, it was absent in motor unit activity. Nonetheless, motor unit activity was correlated with the time it took to initiate saccades. Interestingly, we observed a heterogeneity of responses amongst motor units, such that only units with smaller amplitudes showed a clear modulation during the delay period. These small amplitude motor units also had higher spontaneous activity compared to the units which showed modulation only during the movement epoch. Taken together, our results suggest the activity of smaller motor units convey temporal information and explains how the delay period primes muscle activity leading to faster reaction times.

2021 ◽  
Author(s):  
Satya P. Rungta ◽  
Debaleena Basu ◽  
Naveen Sendhilnathan ◽  
Aditya Murthy

AbstractA hallmark of intelligent behavior is that we can separate intention from action. To understand the mechanism that gates the flow of information between motor planning and execution, we compared the activity of frontal eye field neurons with motor unit activity from neck muscles in the presence of an intervening delay period in which spatial information regarding the target was available to plan a response. Whereas we could infer spatially-specific delayed period activity from the activity of frontal eye field neurons, neck motor unit activity during the delay period could not be used to infer the direction of an upcoming movement, Nonetheless, motor unit activity was correlated with the time it took to initiate saccades. Interestingly, we observed a heterogeneity of responses amongst motor units, such that only units with smaller amplitudes showed a clear modulation during the delay period. These small amplitude motor units also had higher spontaneous activity compared to the units which showed modulation only during the movement epoch. Taken together, our results suggest that the temporal information is visible in the periphery amongst smaller motor units during eye movement planning and explains how the delay period primes muscle activity leading to faster reaction times.Significance statementThis study shows that the temporal aspects of a motor plan in the oculomotor circuitry can be accessed by peripheral neck muscles hundreds of milliseconds prior to the instruction to initiate a saccadic eye movement. The coupling between central and peripheral processes during the delay time is mediated by the recruitment pattern of motor units with smaller amplitude in the periphery. Besides giving insight into how information processed in cortical areas is read out by the muscles, these findings could be useful to decode intentional signals from the periphery to control brain machine interface devices.


1996 ◽  
Vol 81 (6) ◽  
pp. 2428-2435 ◽  
Author(s):  
J. H. Mateika ◽  
E. Essif ◽  
R. F. Fregosi

Mateika, J. H., E. Essif, and R. F. Fregosi. Effect of hypoxia on abdominal motor unit activities in spontaneously breathing cats. J. Appl. Physiol. 81(6): 2428–2435, 1996.—These experiments were designed to examine the behavior of external oblique motor units in spontaneously breathing cats during hypoxia and to estimate the contribution of recruitment and rate coding to changes in the integrated external oblique electromyogram (iEMG). Motor unit activities in the external oblique muscle were identified while the cats expired against a positive end-expiratory pressure (PEEP) of 1–2.5 cmH2O. After localization of unit activity, PEEP was removed, and recordings were made continuously for 3–4 min during hyperoxia, normoxia, and hypoxia. A total of 35 single motor unit activities were recorded from 10 cats. At each level of fractional concentration of end-tidal O2, the motor unit activity was characterized by an abrupt increase in mean discharge frequency, at ∼30% of expiratory time, which then continued to increase gradually or remained constant before declining abruptly at the end of expiration. The transition from hyperoxia to normoxia and hypoxia was accompanied by an increase in the number of active motor units (16 of 35, 20 of 35, and 29 of 35, respectively) and by an increase in the mean discharge frequency of those units active during hyperoxia. The changes in motor unit activity recorded during hypoxia were accompanied by a significant increase in the average peak amplitude of the abdominal iEMG. Linear regression analysis revealed that motor unit rate coding was responsible for close to 60% of the increase in peak iEMG amplitude. The changes in abdominal motor unit activity and the external oblique iEMG that occurred during hypoxia were abolished if the arterial [Formula: see text] was allowed to fall. We conclude that external oblique motor units are activated during the latter two-thirds of expiration and that rate coding and recruitment contribute almost equally to the increase in expiratory muscle activity that occurs with hypoxia. In addition, the excitation of abdominal motor units during hypoxia is critically dependent on changes in CO2 and/or tidal volume.


2016 ◽  
Vol 116 (3) ◽  
pp. 1358-1365 ◽  
Author(s):  
Jeffrey R. Gould ◽  
Brice T. Cleland ◽  
Diba Mani ◽  
Ioannis G. Amiridis ◽  
Roger M. Enoka

The purpose of the study was to compare the discharge characteristics of single motor units during sustained isometric contractions that required either force or position control in left-handed individuals. The target force for the two sustained contractions (24.9 ± 10.5% maximal force) was identical for each biceps brachii motor unit ( n = 32) and set at 4.7 ± 2.0% of maximal voluntary contraction (MVC) force above its recruitment threshold (range: 0.5–41.2% MVC force). The contractions were not sustained to task failure, but the duration (range: 60–330 s) was identical for each motor unit and the decline in MVC force immediately after the sustained contractions was similar for the two tasks (force: 11.1% ± 13.7%; position: 11.6% ± 9.9%). Despite a greater increase in the rating of perceived exertion during the position task (task × time interaction, P < 0.006), the amplitude of the surface-recorded electromyogram for the agonist and antagonist muscles increased similarly during the two tasks. Nonetheless, mean discharge rate of the biceps brachii motor units declined more during the position task (task × time interaction, P < 0.01) and the variability in discharge times (coefficient of variation for interspike interval) increased only during the position task (task × time interaction, P < 0.008). When combined with the results of an identical study on right-handers (Mottram CJ, Jakobi JM, Semmler JG, Enoka RM. J Neurophysiol 93: 1381–1392, 2005), the findings indicate that handedness does not influence the adjustments in biceps brachii motor unit activity during sustained submaximal contractions requiring either force or position control.


2010 ◽  
Vol 108 (6) ◽  
pp. 1550-1562 ◽  
Author(s):  
Jakob L. Dideriksen ◽  
Dario Farina ◽  
Martin Baekgaard ◽  
Roger M. Enoka

The purpose of the study was to expand a model of motor unit recruitment and rate coding ( 30 ) to simulate the adjustments that occur during a fatiguing contraction. The major new components of the model were the introduction of time-varying parameters for motor unit twitch force, recruitment, discharge rate, and discharge variability, and a control algorithm that estimates the net excitation needed by the motoneuron pool to maintain a prescribed target force. The fatigue-induced changes in motor unit activity in the expanded model are a function of changes in the metabolite concentrations that were computed with a compartment model of the intra- and extracellular spaces. The model was validated by comparing the simulation results with data available from the literature and experimentally recorded in the present study during isometric contractions of the first dorsal interosseus muscle. The output of the model was able to replicate a number of experimental findings, including the time to task failure for a range of target forces, the changes in motor unit discharge rates, the skewness and kurtosis of the interspike interval distributions, discharge variability, and the discharge characteristics of newly recruited motor units. The model output provides an integrative perspective of the adjustments during fatiguing contractions that are difficult to measure experimentally.


2005 ◽  
Vol 94 (2) ◽  
pp. 1498-1508 ◽  
Author(s):  
Bonnie M. Lawrence ◽  
Robert L. White ◽  
Lawrence H. Snyder

In the present study, we examined the role of frontal eye field neurons in the maintenance of spatial information in a delayed-saccade paradigm. We found that visual, visuomovement, and movement neurons conveyed roughly equal amounts of spatial information during the delay period. Although there was significant delay-period activity in individual movement neurons, there was no significant delay-period activity in the averaged population of movement neurons. These contradictory results were reconciled by the finding that the population of movement neurons with memory activity consisted of two subclasses of neurons, the combination of which resulted in the cancellation of delay-period activity in the population of movement neurons. One subclass consisted of neurons with significantly greater delay activity in the preferred than in the null direction (“canonical”), whereas the other subclass consisted of neurons with significantly greater delay activity in the null direction than in the preferred direction (“paradoxical”). Preferred direction was defined by the saccade direction that evoked the greatest movement-related activity. Interestingly, the peak saccade-related activity of canonical neurons occurred before the onset of the saccade, whereas the peak saccade-related activity of paradoxical neurons occurred after the onset of the saccade. This suggests that the former, but not the latter, are directly involved in triggering saccades. We speculate that paradoxical neurons provide a mechanism by which spatial information can be maintained in a saccade-generating circuit without prematurely triggering a saccade.


1988 ◽  
Vol 65 (1) ◽  
pp. 210-217 ◽  
Author(s):  
E. van Lunteren ◽  
N. S. Cherniack ◽  
T. E. Dick

To examine the effects of upper airway negative pressure (UAW NP) afferents on respiratory muscle activity during expiration (TE), diaphragm electromyograms (EMG) and triangularis sterni EMG and single motor unit activity were recorded from supine anesthetized tracheotomized cats while they breathed 100% O2. The period of TE during which the diaphragm was electrically active (TE-1) and the period of TE during which the diaphragm was quiescent (TE-2) were both increased with continuous UAW NP (P less than 0.001 and P less than 0.05, respectively), as was TE-1 as a percent of TE (P less than 0.001). Continuous UAW NP reduced peak triangularis sterni EMG (P less than 0.001) and delayed its expiratory onset (P less than 0.005) but did not alter its duration of firing. Changes in triangularis sterni EMG were due to a combination of complete cessation of motor unit activity (2 of 17 motor units), a reduction in mean motor unit firing frequency (P less than 0.02), and a delay in the expiratory onset of motor unit activity (P less than 0.001). Qualitatively similar results were obtained when UAW NP was applied during inspiration only. We conclude that 1) UAW NP has reciprocal stimulatory and inhibitory influences on diaphragm and triangularis sterni muscle electrical activity, respectively, during expiration, and 2) the reductions in triangularis sterni EMG are due to both motor unit derecruitment and a slowing of motor unit firing frequency.


2013 ◽  
Vol 110 (10) ◽  
pp. 2393-2401 ◽  
Author(s):  
Tanya Onushko ◽  
Harsimran S. Baweja ◽  
Evangelos A. Christou

Practice of a motor task decreases motor output variability in older adults and is associated with adaptations of discharge activity of single motor units. In this study we were interested in the practice-induced modulation of multiple motor units within 13–30 Hz because theoretically it enhances the timing of active motoneurons. Our purpose, therefore, was to determine the neural adaptation of multiple motor units and related improvements in movement control following practice. Nine healthy older adults (65–85 yr) performed 40 practice trials of a sinusoidal task (0.12 Hz) with their index finger (10° range of motion). Multi-motor unit activity was recorded intramuscularly from the first dorsal interosseus muscle. The mean spike rate (MSR), spike rate variability (CVISI), and frequency modulation (5–60 Hz) of the spike rate were calculated from the multi-motor unit activity and were correlated with movement accuracy and variability of index finger position. A decrease in movement trajectory variability was associated with an increase in MSR ( R2 = 0.58), a decrease in CVISI ( R2 = 0.58), and an increase in total power within a 13- to 30-Hz band ( R2 = 0.48). The increase in total power within a 13- to 30-Hz band was associated significantly ( P < 0.005) with an increase in MSR ( R2 = 0.75) and the decrease in CVISI ( R2 = 0.70). We demonstrate that practice-induced improvements in movement control are associated with changes in activity of multiple motor units. These findings suggest that practice-induced improvements in movement steadiness of older adults are associated with changes in the modulation of the motoneuron pool from 13 to 30 Hz.


1976 ◽  
Vol 39 (2) ◽  
pp. 370-383 ◽  
Author(s):  
R. J. Elble ◽  
J. E. Randall

Tremor of the extended third digit and bipolar surface and needle electromyograms of the extensor digitorum were recorded from six healthy volunteers for the purpose of elucidating the motor-unit activity responsible for the 8- to 12-Hz component of physiological finger tremor. Tremor was measured with a force transducer during steady voluntary contractions of approximately 200-250 g. The surface EMGs were full-wave rectified and low-pass filtered (-3 dB at 21 Hz), producing the envelope of the surface EMG (the demodulated EMG). Spectral analyses of simultaneous tremor and demodulated EMG records were performed. In four of six subjects, a pronounced 8- to 12-Hz amplitude modulation in the surface EMG was present, and coherency analysis demonstrated that this modulation was strongly correlated with the well-known 8- to 12-Hz tremor. In two subjects this amplitude modulation and tremor were barely detectable, despite the sensitive recording and analysis techniques used in this study. Spectral analysis was performed on 43 motor-unit spike trains. Twenty-two spike trains, having mean firing frequencies in the range of 10-22 spikes/s, produced statistically significant spectral peaks at 8-12 Hz, in addition to the expected spectral peaks at the mean firing frequencies. Of the 22 8- to 12-Hz-producing motor units, 12 had mean firing frequencies in the range of 17-22 spikes/s and exhibited the greatest 8- to 12-Hz activities of all motor units recorded. These motor units displayed transient sequences of double discharges in which interspike intervals (ISIS) of approximately 8-30 ms alternated with ISIS of 60-90 ms, thus producing an 8- to 12-Hz spectral peak. Adjacent ISIS of these motor units were correlated in the range of -0.5 to -0.9. Coherency analyses demonstrated that the 8- to 12-Hz activities of these motor units were correlated with the 8- to 12-Hz finger tremor and surface EMG modulation. The remaining 10 8- to 12-Hz-producing motor units had mean firing frequencies in the range of 10-17 spike/s. Although these motor units did not display the intense double-discharge firing pattern of the more rapidly firing motor units, a tendency toward action potential grouping was present and resulted in 8- to 12-Hz spectral activities which were correlated with the tremor and surface EMG modulation. .. ..


1989 ◽  
Vol 62 (6) ◽  
pp. 1344-1359 ◽  
Author(s):  
R. M. Enoka ◽  
G. A. Robinson ◽  
A. R. Kossev

1. The activity of single motor units was recorded in the first dorsal interosseus muscle of human subjects while they performed an isometric ramp-and-hold maneuver. Motor-unit activity was characterized before and after fatigue by the use of a branched bipolar electrode that was positioned subcutaneously over the test muscle. Activity was characterized in terms of the forces of recruitment and derecruitment and the discharge pattern. The purpose was to determine, before and after fatigue, whether motor-unit activity was affected by the direction in which the force was exerted. 2. Regardless of the task during prefatigue trials, interimpulse intervals were 1) more variable during increases or decreases in force than when force was held constant at the target value (4-6% above the recruitment force), and 2) more clustered around an arbitrary central value than would be expected with a normal (Gaussian) distribution. Both effects were seen during the flexion and abduction tasks. The behavior of low-threshold motor units in first dorsal interosseus is thus largely unaffected by the direction of the force exerted by the index finger. The absence of a task (i.e., a direction of force) effect suggests that the resultant force vector about the metacarpophalangeal joint of the index finger is not coded in terms of discrete populations of motor units, but, rather, it is based on the net muscle activity about the joint. 3. Motor-unit behavior during and after fatigue showed that the relatively homogeneous behavior seen before fatigue could be severely disrupted. The fatiguing protocol involved the continuous repetition, to the endurance limit, of a 15-s ramp-and-hold maneuver in which the abduction target force was 50% of maximum and was held for 10-s epochs (ramps up and down were approximately 2 s each). Motor-unit threshold was assessed by the forces of recruitment and derecruitment associated with each cycle of the fatigue test. Changes in recruitment force during the protocol were either minimal or, when present, not systematic. In contrast, the derecruitment force of all units exhibited a marked and progressive increase over the course of the test. 4. After the fatigue test, when the initial threshold tasks were repeated, the behavior of most motor units changed. These changes included the derecruitment of previously active motor units, the recruitment of additional motor units, and an increased discharge variability of units that remained recruited. The variation in recruitment order seemed to be much greater than that reported previously for nonfatiguing conditions.(ABSTRACT TRUNCATED AT 400 WORDS)


1996 ◽  
Vol 76 (3) ◽  
pp. 1982-1990 ◽  
Author(s):  
S. J. Garland ◽  
J. D. Cooke ◽  
K. J. Miller ◽  
T. Ohtsuki ◽  
T. Ivanova

1. To explore the neural control of single joint movements in humans, the activity of 47 motor units in triceps brachii muscle was recorded during elbow flexion and extension movements. Movements were performed with different but changing deceleration magnitudes, while the acceleration magnitude was kept constant, to determine the relationship between motor unit activity and the acceleration and deceleration characteristics of single joint movements. 2. The number of motor unit action potentials was found to vary with the magnitude of the movement deceleration. In addition the duration of the discharge of a motor unit was found to parallel the duration of the acceleration phase of the movement, when the acceleration duration was varied while acceleration magnitude was kept constant. 3. Approximately half of the recorded motor units in triceps brachii were active both in the initiation and in the termination of the extension movements. However, motor units were identified that participated in specific phases of the movement (i.e., either during the 1st agonist or 2nd agonist burst of muscle activity) depending on the magnitude of the acceleration or deceleration. 4. During flexion movements, when the triceps muscle served as an antagonist, approximately half of the motor units were recruited only when the magnitude of the flexion deceleration was large. Further, this deceleration magnitude was larger than that evident during the extension movements in which the motor unit discharged. 5. The findings of this study demonstrate that the nervous system activates the same motor units whether the muscle is functioning as an agonist or antagonist so as to control the characteristics of acceleration and deceleration of single joint movements.


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