Robert B. Gorman

Decline in spindle support to alpha-motoneurones during sustained voluntary contractions.

1. To address whether the muscle spindle support to alpha‐motoneurones is maintained during prolonged isometric voluntary contractions, the discharge of eighteen muscle spindle afferents, originating in the dorsiflexors of the ankle or toes, was recorded from the common peroneal nerve in eight subjects. Isometric contractions were generally sustained for 1 min, usually below 30% of the maximal voluntary dorsiflexion force. 2. Once the afferent had been identified, subjects were instructed to dorsiflex the foot slowly to recruit the spindle ending, to continue the ramp contraction until a predetermined target force was reached, and then to hold that force until requested to relax. 3. Five muscle spindle afferents maintained a constant discharge frequency during the hold phase of the isometric contraction. Following relaxation of the contraction two spindle afferents from tibialis anterior, exhibited a post‐contraction discharge despite the absence of detectable electromyographic activity (EMG). 4. The discharge frequency of most of the spindle afferents (72%) declined progressively during the isometric contraction. The mean firing rates had declined to two‐thirds of those at the onset of the contraction by 30 s, and to half after 1 min. The decline in spindle firing rate commenced during the ramp phase of the contraction and was statistically significant by 10 s, when force was held constant. The extent of the decline was greater for those units with the higher initial firing rates and for those units studied after many preceding contractions. 5. In the same contractions a progressive increase in EMG was required to maintain force and consequently the change in EMG was inversely related to the change in spindle discharge. While many mechanisms may contribute to the decline in spindle discharge during a sustained isometric contraction, it is argued that the result will be a progressive disfacilitation of alpha‐motoneurones, which may contribute to the decline in motor unit firing rates during a sustained contraction.

The firing rates of human motoneurones voluntarily activated in the absence of muscle afferent feedback.

1. To quantify the net influence of muscle afferent feedback on the firing rates of human motoneurones, the discharge frequencies of single motor axons in the common peroneal nerve were recorded during sustained voluntary efforts performed in the absence of feedback from the target muscle. These data were compared with the firing rates of single motor units in the intact tibialis anterior muscle. In five subjects, recordings were made from fifty‐two motor axons innervating tibialis anterior during acute deafferentation and paralysis of the dorsiflexor muscles produced by anaesthetic block of the nerve distal to the recording site. 2. Maximal sustainable firing rates were determined for twenty‐four motoneurons, twelve of which were classified as relatively low threshold (estimated recruitment level < or = 10% maximal) and six as high threshold. Mean firing rates of the low‐threshold motoneurones (21.7 +/‐ 2.7 Hz; +/‐ S.E.M.) were significantly higher than those of the high‐threshold motoneurones (14.0 +/‐ 4.4 Hz). The mean firing rate of the twenty‐four deafferented motoneurones during maximal efforts to contract the paralysed muscle was 18.6 +/‐ 1.9 Hz, significantly lower than the maximal firing rates of single motor units recorded from the normally innervated tibialis anterior muscle (28.2 +/‐ 0.6 Hz). 3. During half‐maximal efforts, the mean firing rate of eight deafferented motoneurones (10.8 +/‐ 1.1 Hz) was significantly lower than that of intact motor units (16.5 +/‐ 0.2 Hz). A similar finding was apparent during minimal efforts; the mean discharge frequency of seven deafferented motoneurones during weak voluntary efforts was 6.0 +/‐ 0.9 Hz, compared with 7.3 +/‐ 0.13 Hz for intact motor units. Overall, the range of motoneurone firing rates (from minimal to maximal levels of voluntary effort) was significantly affected by the acute deafferentation, but was shifted significantly to lower rates. 4. During sustained maximal voluntary efforts of at least 30 s duration the firing rate of deafferented motoneurones decreased over the first 5 s but was then maintained, i.e. there was no progressive decline as occurs with normally innervated motor units during fatiguing contractions. This observation supports a reflex origin for the normal decline in motoneurone discharge. 5. It is concluded that muscle afferents in the common peroneal nerve provide a net facilitation to the tibialis anterior motoneurone pool, reflexly increasing the motor output at all levels of voluntary drive by approximately one‐third.

Respiratory sensations, cardiovascular control, kinaesthesia and transcranial stimulation during paralysis in humans.

1. To determine whether discomfort associated with breathing (dyspnoea) is related to the chemical drive to breath, three subjects were totally paralysed while fully conscious. Subjective responses to a rising CO2 stimulus were obtained during rebreathing, rebreathing with CO2 added, and breath holding. Dyspnoea was measured with a 10‐point Borg scale. 2. Following nasotracheal intubation and ventilation (oxygen saturation, O2,Sat, 98‐100% and end‐tidal CO2, PET,CO2, 30‐40 mmHg), total neuromuscular blockade was induced by a rapid injection of atracurium (> 2.5 mg kg‐1) and complete paralysis was maintained with an infusion (5 mg (kg h)‐1). Paralysis was confirmed by abolition of the compound muscle action potentials of both the diaphragm and abductor hallucis evoked by supramaximal electrical stimulation of the relevant nerves. Communication via finger movement was preserved for the first 20‐30 min following paralysis by inflation of a sphygmomanometer cuff on one arm. 3. Before and during complete paralysis, dyspnoea increased progressively during hypercapnia produced by rebreathing (with or without CO2 added to the circuit at 250 ml min‐1). The mean PET,CO2 eliciting severe’ dyspnoea was 46 mmHg during rebreathing, 42 mmHg during ‘breath holding’, and 52 mmHg during rebreathing with added CO2. There were no significant differences between the values obtained during paralysis and in the control study immediately before paralysis. The duration of breath holding was not prolonged by paralysis and the PET,CO2 at the ‘break point’ was not altered by paralysis. 4. Thus, dyspnoea is preserved following total neuromuscular blockade. This suggests that chemoreceptor activity, via the central neuronal activity which it evokes, can lead to discomfort in the absence of any contraction of respiratory muscles. 5. During paralysis, attempted contraction of arm, leg and trunk muscles increased heart rate and blood pressure. For attempted handgrip contractions, the increases in heart rate (range, 7‐15 beats min‐1) and mean arterial pressure (range, 20‐32 mmHg) were similar to those recorded with actual contractions in trials immediately before paralysis. In one subject, graded increases in heart rate and blood pressure occurred for attempted contractions of 45 s duration over a range of intensities (0‐100% maximal effort). 6. During complete paralysis, transcranial electromagnetic stimulation of the motor cortex produced illusory twitch‐like movements of the wrist and digits. This also occurred in separate studies during complete ischaemic paralysis and anaesthesia of the forearm and hand.(ABSTRACT TRUNCATED AT 400 WORDS)

Measurement and reproducibility of strength and voluntary activation of lower-limb muscles

Accurate measurement of muscle strength and voluntary muscle activation is important in the assessment of disorders that affect the motor pathways or muscle. We designed a multipurpose system to assess the variability and reproducibility of isometric torque measurements obtained during maximal voluntary efforts of the knee flexor, knee extensor, ankle dorsiflexor, and ankle plantarflexor muscles on each side. It used two isometric myographs mounted on an adjustable frame. Measurements of maximal voluntary torque (range, 25–188 Nm) displayed low variability within a testing session and over five testing sessions (coefficient of variation range, 5–11%). We used the same equipment to measure voluntary activation of the triceps surae muscles. Voluntary activation, measured with a sensitive twitch interpolation method, increased with increasing voluntary contraction torque (P < 0.001) and was very high during maximal efforts (mean, 97.8 ± 2.1%; median, 98.5%). Furthermore, measurements of voluntary activation during maximal efforts were reproducible across testing sessions with very little variability (coefficient of variation, <2%). The myograph system and the testing procedures should allow accurate measurement of strength and voluntary drive in longitudinal patient studies. Muscle Nerve 29: 834–842, 2004

Motoneuronal output and gradation of effort in attempts to contract acutely paralysed leg muscles in man.

1. The study was designed to determine the degree to which normal subjects can control motoneurones innervating a leg muscle when acutely deprived of muscle afferent feedback. Microneurographic recordings were made from eighteen motor fascicles in the common peroneal nerve, of which thirteen innervated tibialis anterior and five toe dorsiflexor muscles. The nerve was then blocked completely at a distal site near the fibular head with local anaesthetic. A sequence of tests was performed with each fascicle to determine the degree to which the subject could control the motoneuronal drive to the paralysed muscle. 2. During a complete distal block of the common peroneal nerve, motoneurones innervating tibialis anterior were frequently activated during weak attempted contraction of the synergist toe extensors and vice versa. 3. When subjects attempted contractions of the paralysed muscles at a constant effort, pressure applied to the dorsum of the foot caused relatively small changes in the level of neural output, producing a small increase in motoneuronal drive to tibialis anterior, but no consistent change in the drive to toe extensor fascicles. 4. Subjects were able to increase the motoneuronal drive to the paralysed tibialis anterior in five steps of effort each lasting 10 s. The level of motor output increased linearly with step number, but declined as the step was maintained, more so when auditory feedback was withdrawn. 5. There was hysteresis in the relationship between motoneuronal output and force (measured on the contralateral side) during attempts to make slowly increasing then decreasing ramps of effort on both sides over 20‐120 s. Motor drive to the paralysed muscle increased disproportionately rapidly compared with contralateral force when subjects attempted bilaterally symmetrical increasing efforts. 6. Subjects attempted to activate the paralysed muscle group maximally for 20‐30 s with auditory feedback of the neurogram and verbal encouragement. There was a small statistically significant reduction in the motoneuronal output 5‐10 s into the 30 s effort but, with further encouragement, it recovered towards the end of the effort. 7. When compared directly in the same recording sequences, attempts to make rapid brief maximal efforts (2‐3 s duration) produced the same motoneuronal output as attempts to make sustained efforts. 8. Similar results occurred when the motoneuronal output to tibialis anterior was recorded during a selective distal block of tibialis anterior sparing toe dorsiflexors.(ABSTRACT TRUNCATED AT 400 WORDS)

Neural drive to human genioglossus in obstructive sleep apnoea

One postulated mechanism for obstructive sleep apnoea (OSA) is insufficient drive to the upper‐airway musculature during sleep, with increased (compensatory) drive during wakefulness. This generates more electromyographic activity in upper airway muscles including genioglossus. To understand drives to upper airway muscles, we recorded single motor unit activity from genioglossus in male groups of control (n= 7, 7 ± 2 events h−1) and severe OSA (n= 9, 54 ± 4 events h−1) subjects. One hundred and seventy‐eight genioglossus units were recorded using monopolar electrodes. Subjects were awake, supine and breathing through a nasal mask. The distribution of the six types of motor unit activity in genioglossus (Inspiratory Phasic, Inspiratory Tonic, Expiratory Phasic, Expiratory Tonic, Tonic and Tonic Other) was identical in both groups. Single unit action potentials in OSA were larger in area (by 34%, P < 0.05) and longer in duration (by 23%, P < 0.05). Inspiratory units were recruited earlier in OSA than control subjects. In control subjects, Inspiratory Tonic units peaked earlier than Inspiratory Phasic units, while in OSA subjects, Inspiratory Tonic and Phasic units peaked simultaneously. Onset frequencies did not differ between groups, but the peak discharge frequency for Inspiratory Phasic units was higher in OSA (22 ± 1 Hz) than control subjects (19 ± 1 Hz, P= 0.003), but conversely, the peak discharge frequency of Inspiratory Tonic units was higher in control subjects (28 ± 1 Hz versus 25 ± 1 Hz, P < 0.05). Increased motor unit action potential area indicates that neurogenic changes have occurred in OSA. In addition, the differences in the timing and firing frequency of the inspiratory classes of genioglossus motor units indicate that the output of the hypoglossal nucleus may have changed.

Passive mechanical properties of human gastrocnemius muscle-tendon units, muscle fascicles and tendons in vivo

SUMMARY This study provides the first in vivo measures of the passive length–tension properties of relaxed human muscle fascicles and their tendons. A new method was used to derive passive length–tension properties of human gastrocnemius muscle–tendon units from measures of ankle stiffness obtained at a range of knee angles. Passive length–tension curves of the muscle–tendon unit were then combined with ultrasonographic measures of muscle fascicle length and pennation to determine passive length–tension curves of the muscle fascicles and tendons. Mean slack lengths of the fascicles, tendons and whole muscle–tendon units were 3.3±0.5 cm, 39.5±1.6 cm and 42.3±1.5 cm, respectively (means ± s.d., N=6). On average, the muscle–tendon units were slack (i.e. their passive tension was zero) over the shortest 2.3±1.2 cm of their range. With combined changes of knee and ankle angles, the maximal increase in length of the gastrocnemius muscle–tendon unit above slack length was 6.7±1.9 cm, of which 52.4±11.7% was due to elongation of the tendon. Muscle fascicles and tendons underwent strains of 86.4±26.8% and 9.2±4.1%, respectively, across the physiological range of lengths. We conclude that the relaxed human gastrocnemius muscle–tendon unit falls slack over about one-quarter of its in vivo length and that muscle fascicle strains are much greater than tendon strains. Nonetheless, because the tendons are much longer than the muscle fascicles, tendons contribute more than half of the total compliance of the muscle–tendon unit.

Distribution of inspiratory drive to the external intercostal muscles in humans

The external intercostal muscles in humans show marked regional differences in respiratory effect, and this implies that their action on the lung during breathing is primarily determined by the spatial distribution of neural drive among them. To assess this distribution, monopolar electrodes were implanted under ultrasound guidance in different muscle areas in six healthy individuals and electromyographic recordings were made during resting breathing. The muscles in the dorsal portion of the third and fifth interspace showed phasic inspiratory activity with each breath in every subject. However, the muscle in the ventral portion of the third interspace showed inspiratory activity in only three subjects, and the muscle in the dorsal portion of the seventh interspace was almost invariably silent. Also, activity in the ventral portion of the third interspace, when present, and activity in the dorsal portion of the fifth interspace were delayed relative to the onset of activity in the dorsal portion of the third interspace. In addition, the discharge frequency of the motor units identified in the dorsal portion of the third interspace averaged (mean ±s.e.m.) 11.9 ± 0.3 Hz and was significantly greater than the discharge frequency of the motor units in both the ventral portion of the third interspace (6.0 ± 0.5 Hz) and the dorsal portion of the fifth interspace (6.7 ± 0.4 Hz). The muscle in the dorsal portion of the third interspace started firing simultaneously with the parasternal intercostal in the same interspace, and the discharge frequency of its motor units was even significantly greater (11.4 ± 0.3 vs. 8.9 ± 0.2 Hz). These observations indicate that the distribution of neural inspiratory drive to the external intercostals in humans takes place along dorsoventral and rostrocaudal gradients and mirrors the spatial distribution of inspiratory mechanical advantage.

Distribution of the forces produced by motor unit activity in the human flexor digitorum profundus

In humans, the flexor digitorum profundus (FDP), which is a multi‐tendoned muscle, produces forces that flex the four distal interphalangeal joints of the fingers. We determined whether the force associated with activity in a single motor unit in the FDP was confined to a single finger or distributed to more than one finger during a natural grasp. The discharge of single low‐threshold motor units (n= 69) was recorded at sites across the muscle during weak voluntary grasping involving all fingers and spike‐triggered averaging of the forces under each of the finger pads was used to assess the distribution pattern. Spike‐triggered averaging revealed that time‐locked changes in force occurred under the ‘test’ finger (that finger on which the unit principally acted) as well as under the ‘non‐test’ fingers. However, for the index‐, middle‐ and ring‐finger units, the changes in force under non‐test fingers were typically small (< 20 % of those under the test finger). For little‐finger units, the mean changes in force under the adjacent ring finger were large (>50 % of those under the test finger). The distribution of forces by little‐finger units differed significantly from that for each of the other three fingers. Apart from increases in force under non‐test fingers, there was occasional unloading of adjacent fingers (22/267 combinations), usually affecting the index finger. The increases in force under the test finger correlated significantly with the background force for units acting on the middle, ring and little fingers. During a functional grasp, the activity of single units in the FDP allows for a relatively selective control of forces at the tips of the index, middle and ring fingers, but this is limited for little‐finger units.

Spatial distribution of inspiratory drive to the parasternal intercostal muscles in humans

The human parasternal intercostal muscles are obligatory inspiratory muscles with a diminishing mechanical advantage from cranial to caudal interspaces. This study determined whether inspiratory neural drive to these muscles is graded, and whether this distribution matches regional differences in inspiratory mechanical advantage. To determine the neural drive, intramuscular EMG was recorded from the first to the fifth parasternal intercostals during resting breathing in six subjects. All interspaces showed phasic inspiratory activity but the onset of activity relative to inspiratory flow in the fourth and fifth spaces was delayed compared with that in cranial interspaces. Activity in the first, second and third interspaces commenced, on average, within the first 10% of inspiratory time, and sometimes preceded inspiratory airflow. In contrast, activity in the fourth and fifth interspaces began after an average 33% of inspiratory time. The peak inspiratory discharge frequency of motor units in the first interspace averaged 13.4 ± 1.0 Hz (mean ±s.e.m.) and was significantly greater than in all other interspaces, in particular in the fifth space (8.0 ± 1.0 Hz). Phasic inspiratory activity was sometimes superimposed on tonic activity. In the first interspace, only 3% of units had tonic firing, but this proportion increased to 34% in the fifth space. In five subjects, recordings were also made from the medial and lateral extent of the second parasternal intercostal. Both portions showed phasic inspiratory activity which began within the first 6% of inspiratory time. Motor units from the lateral and medial portions fired at the same peak discharge rate (10.4 ± 0.7 versus 10.7 ± 0.6 Hz). These observations indicate that the distribution of neural drive to the parasternal intercostals in humans has a rostrocaudal gradient, but that the drive is uniform along the mediolateral extent of the second interspace. The distribution of inspiratory neural drive to the parasternal intercostals parallels the spatial distribution of inspiratory mechanical advantage, while tonic activity was higher where mechanical advantage was lower.