scholarly journals Recruitment of rat diaphragm motor units across motor behaviors with different levels of diaphragm activation

2014 ◽  
Vol 117 (11) ◽  
pp. 1308-1316 ◽  
Author(s):  
Yasin B. Seven ◽  
Carlos B. Mantilla ◽  
Gary C. Sieck

Phrenic motor neurons are recruited across a range of motor behaviors to generate varying levels of diaphragm muscle (DIAm) force. We hypothesized that DIAm motor units are recruited in a fixed order across a range of motor behaviors of varying force levels, consistent with the Henneman Size Principle. Single motor unit action potentials and compound DIAm EMG activities were recorded in anesthetized, neurally intact rats across different motor behaviors, i.e., eupnea, hypoxia-hypercapnia (10% O2 and 5% CO2), deep breaths, sustained airway occlusion, and sneezing. Central drive [estimated by root-mean-squared (RMS) EMG value 75 ms after the onset of EMG activity (RMS75)], recruitment delay, and onset discharge frequencies were similar during eupnea and hypoxia-hypercapnia. Compared with eupnea, central drive increased (∼25%) during deep breaths, and motor units were recruited ∼12 ms earlier ( P < 0.01). During airway occlusion, central drive was ∼3 times greater, motor units were recruited ∼30 ms earlier ( P < 0.01), and motor unit onset discharge frequencies were significantly higher ( P < 0.01). Recruitment order of motor unit pairs observed during eupnea was maintained for 98%, 87%, and 84% of the same pairs recorded during hypoxia-hypercapnia, deep breaths, and airway occlusion, respectively. Reversals in motor unit recruitment order were observed primarily if motor unit pairs were recruited <20 ms apart. These results are consistent with DIAm motor unit recruitment order being determined primarily by the intrinsic size-dependent electrophysiological properties of phrenic motor neurons.

2017 ◽  
Vol 117 (2) ◽  
pp. 537-544 ◽  
Author(s):  
Vivian Hernandez-Torres ◽  
Heather M. Gransee ◽  
Carlos B. Mantilla ◽  
Yao Wang ◽  
Wen-Zhi Zhan ◽  
...  

Unilateral C2 cervical spinal cord hemisection (SH) disrupts descending excitatory drive to phrenic motor neurons, thereby paralyzing the ipsilateral diaphragm muscle (DIAm) during ventilatory behaviors. Recovery of rhythmic DIAm activity ipsilateral to injury occurs over time, consistent with neuroplasticity and strengthening of spared synaptic inputs to phrenic motor neurons. Localized intrathecal delivery of brain-derived neurotrophic factor (BDNF) to phrenic motor neurons after SH enhances recovery of eupneic DIAm activity. However, the impact of SH and BDNF treatment on the full range of DIAm motor behaviors has not been fully characterized. We hypothesized that all DIAm motor behaviors are affected by SH and that intrathecal BDNF enhances the recovery of both ventilatory and higher force, nonventilatory motor behaviors. An intrathecal catheter was placed in adult, male Sprague-Dawley rats at C4 to chronically infuse artificial cerebrospinal fluid (aCSF) or BDNF. DIAm electromyography (EMG) electrodes were implanted bilaterally to record activity across motor behaviors, i.e., eupnea, hypoxia-hypercapnia (10% O2 and 5% CO2), sighs, airway occlusion, and sneezing. After SH, ipsilateral DIAm EMG activity was evident in only 43% of aCSF-treated rats during eupnea, and activity was restored in all rats after BDNF treatment. The amplitude of DIAm EMG (root mean square, RMS) was reduced following SH during eupnea and hypoxia-hypercapnia in aCSF-treated rats, and BDNF treatment promoted recovery in both conditions. The amplitude of DIAm RMS EMG during sighs, airway occlusion, and sneezing was not affected by SH or BDNF treatment. We conclude that the effects of SH and BDNF treatment on DIAm activity depend on motor behavior. NEW & NOTEWORTHY This study demonstrates that after unilateral C2 spinal cord hemisection (SH), there are differences in the spontaneous recovery of diaphragm (DIAm) electromyographic activity during ventilatory compared with more forceful, nonventilatory motor behaviors. Furthermore, we show that intrathecal delivery of brain-derived neurotrophic factor (BDNF) at the level of the phrenic motor neuron pool enhances recovery of ipsilateral DIAm activity following SH, exerting main effects on recovery of ventilatory but not higher force, nonventilatory behaviors.


Physiology ◽  
2018 ◽  
Vol 33 (2) ◽  
pp. 113-126 ◽  
Author(s):  
Matthew J. Fogarty ◽  
Carlos B. Mantilla ◽  
Gary C. Sieck

Breathing occurs without thought but is controlled by a complex neural network with a final output of phrenic motor neurons activating diaphragm muscle fibers (i.e., motor units). This review considers diaphragm motor unit organization and how they are controlled during breathing as well as during expulsive behaviors.


1996 ◽  
Vol 75 (1) ◽  
pp. 26-37 ◽  
Author(s):  
K. E. Tansey ◽  
B. R. Botterman

1. The recruitment order of 64 pairs of motor units, comprising 21 type-identified units, was studied during centrally evoked muscle contractions of the cat medial gastrocnemius (MG) muscle in an unanesthetized, high decerebrate preparation. Motor units were functionally isolated within the MG nerve by intra-axonal (or intramyelin) penetration with conventional glass microelectrodes. 2. Graded stimulation of the mesencephalic locomotor region (MLR) was used to evoke smoothly graded contractions, which under favorable conditions was estimated to reach 40% of maximum tetanic tension of the MG muscle. With this method of activation, 100% of slow twitch (type S) units, 95% of fast twitch, fatigue-resistant (type FR) units, 86% of fast twitch, fatigue-intermediate (type FI) units, and 49% of fast twitch, fatigable (type FF) units studied were recruited. 3. Motoneuron size as estimated by axonal conduction velocity (CV) was correlated with muscle-unit size as estimated by maximum tetanic tension (Po). Although the correlation between these properties was significant among type S and FR units, no significant correlation was found for these properties among type FI and FF units. 4. Motor-unit recruitment was ordered by physiological type (S > F, 100% of pairs; S > FR > FI > FF, 93% of pairs). Although none of the motor-unit properties studied predicted recruitment order perfectly, motor-unit recruitment was found to proceed by increasing Po (89% of pairs), decreasing contraction time (79% of pairs), decreasing fatigue index (80% of pairs), and increasing CV (76% of pairs). These percentages were significantly different from random (i.e., 50%). Statistically, all four motor-unit properties were equivalent in predicting recruitment order. These results are similar to those reported by other investigators for motor-unit recruitment order evoked from other supraspinal centers, as well as from peripheral sites. 5. When, however, motor-unit recruitment within pairs of motor units containing two fast-twitch (type F) units was examined, Po was a significantly better predictor of recruitment order than CV (85% vs. 52% of pairs). One explanation for this observation is that the correlation between Po and CV is high among type S, type FR units, and possibly among the lower-tension type FF units, but not among the remaining higher-tension type FF units. 6. The reproducibility of recruitment order in multiple contractions was investigated in 16 motor-unit pairs. Recruitment order was found to be variable in only three motor-unit pairs, all of which contained units of similar physiological type and recruitment threshold. 7. Analysis of recruitment order by pair-wise testing confirms the general conclusion reached in human studies that the muscle force level at recruitment for a motor unit is highly correlated with its strength. As an additional confirmation, the whole-muscle force level at recruitment for 41 units was measured in a series of contractions in which the rate of rise of muscle tension was limited to rates < 1,000 g/s. For these contractions, a significant correlation was found between muscle tension at recruitment and motor-unit Po.


2010 ◽  
Vol 24 (S1) ◽  
Author(s):  
Yasin Baris Seven ◽  
Carlos B. Mantilla ◽  
Wen‐Zhi Zhan ◽  
Gary C. Sieck

2017 ◽  
Vol 117 (2) ◽  
pp. 545-555 ◽  
Author(s):  
Sabhya Rana ◽  
Gary C. Sieck ◽  
Carlos B. Mantilla

Contusion-type injuries to the spinal cord are characterized by tissue loss and disruption of spinal pathways. Midcervical spinal cord injuries impair the function of respiratory muscles and may contribute to significant respiratory complications. This study systematically assessed the impact of a 100-kDy unilateral C4 contusion injury on diaphragm muscle activity across a range of motor behaviors in rats. Chronic diaphragm electromyography (EMG) was recorded before injury and at 1 and 7 days postinjury (DPI). Histological analyses assessed the extent of perineuronal net formation, white-matter sparing, and phrenic motoneuron loss. At 7 DPI, ∼45% of phrenic motoneurons were lost ipsilaterally. Relative diaphragm root mean square (RMS) EMG activity increased bilaterally across a range of motor behaviors by 7 DPI. The increase in diaphragm RMS EMG activity was associated with an increase in neural drive (RMS value at 75 ms after the onset of diaphragm activity) and was more pronounced during higher force, nonventilatory motor behaviors. Animals in the contusion group displayed a transient decrease in respiratory rate and an increase in burst duration at 1 DPI. By 7 days, following midcervical contusion, there was significant perineuronal net formation and white-matter loss that spanned 1 mm around the injury epicenter. Taken together, these findings are consistent with increased recruitment of remaining motor units, including more fatigable, high-threshold motor units, during higher force, nonventilatory behaviors. Changes in diaphragm EMG activity following midcervical contusion injury reflect complex adaptations in neuromotor control that may increase the risk of motor-unit fatigue and compromise the ability to sustain higher force diaphragm efforts. NEW & NOTEWORTHY The present study shows that unilateral contusion injury at C4 results in substantial loss of phrenic motoneurons but increased diaphragm muscle activity across a range of ventilatory and higher force, nonventilatory behaviors. Measures of neural drive indicate increased descending input to phrenic motoneurons that was more pronounced during higher force, nonventilatory behaviors. These findings reveal novel, complex adaptations in neuromotor control following injury, suggestive of increased recruitment of more fatigable, high-threshold motor units.


2006 ◽  
Vol 95 (3) ◽  
pp. 1518-1526 ◽  
Author(s):  
C. K. Thomas ◽  
R. S. Johansson ◽  
B. Bigland-Ritchie

Few studies have analyzed activity-induced changes in EMG activity in individual human motor units. We studied the changes in human thenar motor unit EMG that accompany the potentiation of twitch force and fatigue of tetanic force. Single motor unit EMG and force were recorded in healthy subjects in response to selective stimulation of their motor axons within the median nerve just above the elbow. Twitches were recorded before and after a series of pulse trains delivered at frequencies that varied between 5 and 100 Hz. This stimulation induced significant increases in EMG amplitude, duration, and area. However, in relative terms, all of these EMG changes were substantially smaller than the potentiation of twitch force. Another 2 min of stimulation (13 pulses at 40 Hz each second) induced additional potentiation of EMG amplitude, duration, and area, but the tetanic force from every unit declined. Thus activity-induced changes in human thenar motor unit EMG do not indicate the alterations in force or vice versa. These data suggest that different processes underlie the changes in EMG and force that occur during human thenar motor unit activity.


2002 ◽  
Vol 205 (3) ◽  
pp. 359-369 ◽  
Author(s):  
James M. Wakeling ◽  
Motoshi Kaya ◽  
Genevieve K. Temple ◽  
Ian A. Johnston ◽  
Walter Herzog

SUMMARY Motor units are the functional units of muscle contraction in vertebrates. Each motor unit comprises muscle fibres of a particular fibre type and can be considered as fast or slow depending on its fibre-type composition. Motor units are typically recruited in a set order, from slow to fast, in response to the force requirements from the muscle. The anatomical separation of fast and slow muscle in fish permits direct recordings from these two fibre types. The frequency spectra from different slow and fast myotomal muscles were measured in the rainbow trout Oncorhynchus mykiss. These two muscle fibre types generated distinct low and high myoelectric frequency bands. The cat paw-shake is an activity that recruits mainly fast muscle. This study showed that the myoelectric signal from the medial gastrocnemius of the cat was concentrated in a high frequency band during paw-shake behaviour. During slow walking, the slow motor units of the medial gastrocnemius are also recruited, and this appeared as increased muscle activity within a low frequency band. Therefore, high and low frequency bands could be distinguished in the myoelectric signals from the cat medial gastrocnemius and probably corresponded, respectively, to fast and slow motor unit recruitment. Myoelectric signals are resolved into time/frequency space using wavelets to demonstrate how patterns of motor unit recruitment can be determined for a range of locomotor activities.


1982 ◽  
Vol 47 (5) ◽  
pp. 797-809 ◽  
Author(s):  
P. J. Cordo ◽  
W. Z. Rymer

1. Subdivided portions of the cut ventral root innervation of the soleus muscle were electrically stimulated in 14 anesthetized cats. The stimulus trains imposed on these nerves simulated the recruitment and rate-modulation patterns of single motor units recorded during stretch-reflex responses in decerebrate preparations. Each activation pattern was evaluated for its ability to prevent muscle yield. 2. Three basic stimulus patterns, recruitment, step increases in stimulus rate, and doublets were imposed during the course of ramp stretches applied over a wide range of velocities. The effect of each stimulus pattern on muscle force was compared to the force output recorded without stretch-related recruitment or rate modulation. 3. Motor-unit recruitment was found to be most effective in preventing yield during muscle stretch. Newly recruited motor units showed no evidence of yielding for some 250 ms following activation, at which time muscle stiffness declined slightly. This time-dependent resistance to yield was observed regardless of whether the onset of the neural stimulus closely preceded or followed stretch onset. 4. Step increases in stimulus rate arising shortly after stretch onset did not prevent the occurrence of yield at most stretch velocities, but did augment muscle stiffness later in the stretch. Doublets in the stimulus train were found to augment muscle stiffness only when they occurred in newly recruited motor units. 5. These results suggest that at low or moderate initial forces, the prevention of yield in lengthening, reflexively intact muscle results primarily from rapid motor-unit recruitment. To a lesser extent, the spring-like character of the stretch-reflex response also derives from step increases in firing rate of motor units active before stretch onset and doublets in units recruited during the course of stretch. Smooth rate increases appear to augment muscle force later in the course of the reflex response.


2005 ◽  
Vol 94 (5) ◽  
pp. 3126-3133 ◽  
Author(s):  
Benjamin Pasquet ◽  
Alain Carpentier ◽  
Jacques Duchateau

This study examines the effect of fascicle length change on motor-unit recruitment and discharge rate in the human tibialis anterior (TA) during isometric contractions of various intensities. The torque produced during dorsiflexion and the surface and intramuscular electromyograms (EMGs) from the TA were recorded in eight subjects. The behavior of the same motor unit ( n = 59) was compared at two ankle joint angles (+10 and −10° around the ankle neutral position). Muscle fascicle length of the TA was measured noninvasively using ultrasonography recordings. When the ankle angle was moved from 10° plantarflexion to 10° dorsiflexion, the torque produced during maximal voluntary contraction (MVC) was significantly reduced [35.2 ± 3.3 vs. 44.3 ± 4.2 (SD) Nm; P < 0.001] and the average surface EMG increased (0.47 ± 0.08 vs. 0.43 ± 0.06 mV; P < 0.05). At reduced ankle joint angle, muscle fascicle length declined by 12.7% ( P < 0.01) at rest and by 18.9% ( P < 0.001) during MVC. Motor units were activated at a lower recruitment threshold for short compared with long muscle fascicle length, either when expressed in absolute values (2.1 ± 2.5 vs. 3.6 ± 3.7 Nm; P < 0.001) or relative to their respective MVC (5.2 ± 6.1 vs. 8.8 ± 9.0%). Higher discharge rate and additional motor-unit recruitment were observed at a given absolute or relative torque when muscle fascicles were shortened. However, the data indicate that increased rate coding was mainly present at low torque level (<10% MVC), when the muscle-tendon complex was compliant, whereas recruitment of additional motor units played a dominant role at higher torque level and decreased compliance (10–35% MVC). Taken together, the results suggest that the central command is modulated by the afferent proprioceptive information during submaximal contractions performed at different muscle fascicle lengths.


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