Contractile properties in single muscle fibres from chronically overused motor units in relation to motoneuron firing properties in prior polio patients.

The relation between motoneuron firing rate in vivo and maximum velocity of unloaded shortening (Vmax) and myosin isoform composition in single chemically skinned muscle fibres was investigated in chronically overused motor units. Ten patients with loss of a large proportion of the motoneuron pool due to a prior polio lesion and compensatory overuse of residual neurones were studied and compared with normal individuals. The tibialis anterior muscle (TA) was chosen and prior polio patients who used all residual TA motor units at high rates during the normal step cycle were selected. In prior polio patients, all motor units fired at approximately 40 Hz when maximum voluntary force was reached. A common firing rate of 30 Hz yielded 70-90% maximum force. In normal subjects, on the other hand, maximum TA force was reached when low threshold units fired at 25-30 Hz and high threshold units at 50 Hz. Myosin heavy chain (MHC) and light chain (MLC) isoforms were resolved by 6% and 12% sodium dodecyl sulphate polyacrylamide gel electrophoresis (SDS-PAGE), respectively, and quantified densitometrically. In the whole biopsy cross-sections, types I, IIA and IIB MHC proportions were 97, 3 and 0% in a typical prior polio patient and 65, 25 and 10% in an age- and sex-matched control subject. Vmax differed significantly (p < 0.001) between type I fibres from the patient (0.54 +/- 0.12 ML/s) and the control subject (0.29 +/- 0.08 ML/s). The composition and relative contents of essential and regulatory MLC isoforms differed in single type I MHC fibres from the control subject and prior polio patient. 65% of the fibres co-expressed the fast and slow isoform of the regulatory light chain (MLC2) in the patient, while this combination was only observed in one of the control type I fibres. All prior polio fibres with a Vmax higher than 0.45 ML/s, except one, co-expressed MLC2s and MLC2f and the only control fibre co-expressing the slow and fast MLC2 isoform had the highest Vmax (0.50 ML/s) among control fibres. On the other hand, a high relative content of MLC3 was not associated with a high Vmax in type I MHC fibres. It is suggested that the composition of fast and slow isoforms of MLC2 has a significant modulatory influence on Vmax within type I MHC fibres. This combination of MLCs and high Vmax in type I MHC fibres is probably induced by chronic motor unit overuse and an altered motoneuron firing pattern.

Disuse of anterior tibial muscle during locomotion and increased proportion of type II fibres in hemiplegia.

The tibialis anterior (TA) is a muscle activated mainly during walking. Its use during the step cycle was studied in 10 patients (55.8 +/- 8.8 years) with chronic hemiplegia (duration 3-18 years) and related to the muscle fibre composition, size and expression of isoforms of myosin heavy chains (MHCs). In the average step cycle the integrated surface EMG of the paralysed TA did in the majority of the hemiplegic patients not exceed 10% of that recorded during maximal contraction of the normal leg. The type I fibre percentage in the paralysed TA subject was 57.4% as compared with 79.4% in normal muscles (P less than 0.05). The range of axonal conduction velocities in the peroneal nerve did not differ in paralysed and non-paralysed leg, suggesting that there was no selective loss of one class of motoneurons. The type II fibres consisted of IIA (66%) and IIB (31%), in contrast to the normal TA muscle where less than 1% of the muscle fibres are of type IIB. The incidence of fibres in the biopsies with both slow and fast MHCs had a mean value of 3.5% (range 0.7-9%). The type I and type II muscle fibres had normal sizes with cross-sectional area 4511 +/- 962 microns 2 and 6181 +/- 1062 microns 2. No selective type II atrophy was seen. Occasional hypertrophic type I and II fibres were seen in 4 patients.(ABSTRACT TRUNCATED AT 250 WORDS)

Firing properties of single human motor units during locomotion.

The discharge properties of single motor units in the short extensors of the toes were studied during normal locomotion using electromyographic recordings which permitted the identification of single motor unit potentials. The single motor units were recruited in the same order during slowly increasing speed of locomotion as they were during slowly increasing voluntary tension, i.e. motor units with low axonal conduction velocity were recruited before motor units with higher conduction velocity. Low threshold units fired five to ten times at 80-40 ms intervals in each step cycle during walking at normal speed. Motor units with moderately high thresholds fired once or only a small number of times in each cycle at shorter interspike intervals. High threshold motor units did not participate in the step cycle during walking at normal speeds but fired in short high-frequency bursts in corrective movements.

Effect of exercise on the motor unit.

The motoneuron part of this review deals with the changes in recruitment and firing rates of the motor unit types upon changes from a physically inactive life to endurance or strength training. The muscle fibers react to prolonged exercise by adaptation to a higher level of performance. A matter of discussion is the prerequisites for a transformation between the basic muscle fiber types, slow twitch and fast twitch, during voluntary (transsynaptic) activity, which is demonstrated after artificial nerve stimulation. The review includes current knowledge of muscle fiber transformation as an adaptive response to increased usage either by electrical stimulation or by transsynaptic neuronal activity. The metabolic adaptation related to increased endurance is reviewed with special reference to effects on muscle fibers. The increase in strength as a result of high resistance training is mainly the result of increased muscle cross-section. Whether this is solely the result of an increase in size of individual fibers or an increased fiber number is a controversial matter.

Recruitment order of motor units in man: significance of pre-existing state of facilitation.

It has been shown in previous investigations that the recruitment order of motor units is different in tonic and in phasic voluntary activity. The significance of the pre-existing state of facilitation in the motoneurone pool for the recruitment of units is studied, using the phasic flexion reflex in the anterior tibial muscle as test reflex. It is shown that the recruitment order of units in a series of reflexes (1) is unstable if the subject does not expect the stimulus; (2) is stable and identical with that in tonic activity if the subject subliminally facilitates the motoneurone pool before the reflex activation; (3) is stable and almost identical with that in tonic activity if the subject expects the stimulus and therefore involuntarily influences the motoneurone pool; (4) is stable and similar to that in phasic voluntary activity if the subject inhibits the motoneurone pool before the activation and the stimulus strength thus consequentially is increased; and (5) is influenced by blockade of the proprioceptive afferent impulses from the muscle. It is concluded that normal man can select in advance the recruitment order of motor units most appropriate for the work intended.

Disturbances in the voluntary recruitment order of anterior tibial motor units in bradykinesia of Parkinsonism.

The recruitment of motor units is studied with an electromyographic technique for secure identification of single motor unit potentials. It has been shown in previous studies that the recruitment order is different in tonic and in phasic activities; in tonic activity the recruitment order is stable and low frequency units are always recruited before high frequency units; in phasic activity, however, the recruitment order is unstable and units with a higher frequency range may be recruited before units with lower frequency range. In this investigation the shifts between tonic and phasic recruitment order in voluntary contraction were compared in normal subjects and in patients with severe bradykinesia of Parkinsonism. Upon initiation of a voluntary contraction in a normal subject, phasic recruitment order may be used for a few 100 msec but tonic recruitment order then takes over. In bradykinetic patients, however, this shift from phasic to tonic recruitment order is delayed. After termination of tonic voluntary contraction in a normal subject, phasic recruitment order can again be used after a few seconds. In bradykinetic patients, however, the shift back from tonic to phasic recruitment order is also delayed. In favourable experimental situations the shift from phasic to tonic recruitment order can be normalized by passive stretch of the muscle and the shift from tonic to phasic recruitment pattern by unloading the muscle. It is discussed whether the pathological recruitment in bradykinesia might be due to disturbed gamma loop function.

Flexibility of the use of residual tibial anterior motor units during walking in neuromuscular diseases.

The use of tibial anterior (TA) motor units in lower motoneurone disorders was studied during comfortable walking that was the main function of TA. The findings were compared to those in normal subjects. The loss of TA power was compensated either by increases of recruitment and firing rate of residual TA units or by a change from the normal plantigrade gait pattern to the infantile digitigrade pattern putting less strain on TA. Moderately paralysed subjects usually maintained plantigrade gait by excessive use of residual TA units but tended to change to digitigrade gait on fatigue thus economizing with remaining TA power. Severely paralysed subjects used digitigrade gait but plantigrade gait could be restored by application of a toe using string, i.e. the string might increase the strain on TA instead of decreasing it.

Firing rate and recruitment order of toe extensor motor units in different modes of voluntary conraction.

1. The discharge properties of individual motor units in different modes of voluntary contraction were studied with electromyographic techniques in the short toe extensor muscle of normal man. 2. The short toe extensor muscle consisted of type I and type II muscle fibres in about equal proportion. In some subjects there was type-grouping so that recordings with sufficient selectivity could easily be obtained. 3. Certain motor units could be driven continuously, attained regular firing intervals even at a firing rate of 10/sec, increased slowly in firing rate with increase in contraction strength, had maximum firing rate below 30/sec during sustained contraction but above 60/sec in twitch contraction. 4. Other motor units could not be dirven continuously, did not fire repeatedly at rates below 20/sec, increased rapidly in firing rate with increase in contraction strength and attained firing rates above 100/sec. 5. There were intermediate forms between continuously firing low frequency motor units and intermittently firing high frequency motor units. 6. In a prolonged contraction of constant strength only continuously firing motor units were active. 7. On rapid accelerations, however, both continuously and intermittently firing motor units were active and played about the same role. 8. This applied also to prolonged series of accelerations as in rhythmically alternating movements. 9. In twitch contractions selective activation of intermittently firing motor units occurred if the muscle was relaxed prior to the twitch and great effort was used to elicit the twitch and minimum duration of the twitch was intended. 10. It is suggested that continuously firing low frequency motor units have type I muscle fibres and intermittently firing high frequency units have type II muscle fibres and that the order of recruitment and the relative roles of the two motor unit types are adapted to the mode of contraction.

Disturbances in the voluntary recruitment order of anterior tibial motor units in ataxia.

The recruitment order of motor units was studied with an electromyographic technique for secure identification of single motor unit potentials. It has been shown in previous studies of normal subjects that the recruitment order in sustained voluntary contraction is predominantly stable, and that motor units which increase slowly in discharge rate with increasing contraction strength and which already attain regular discharge intervals at low frequencies are always recruited before motor units which increase more rapidly in discharge rate and which do not attain regular discharge intervals until at higher frequencies. In this study 15 patients with severe cerebellar ataxia were examined. It was shown that the recruitment order in sustained voluntary contraction in attaxia is unstable and that low- and high-frequency motor units may alternate as the unit of lowest threshold.

Disturbances in voluntary recruitment order of low and high frequency motor units on blockades of proprioceptive afferent activity.

The voluntary recruitment order of anterior tibial motor units was studied in electromyographic recordings using both low and high impedance electrodes. It was shown in previous papers, that the recruitment order in sustained voluntary contraction is normally stable and that motor units with low thresholds discharge at low, regular frequencies and that motor units with high thresholds discharge at higher and more irregular frequencies. In this paper the consequences for the discharge properties of reduced afferent inflow in sustained voluntary contraction were studied, using partial ischemic or lidocain blockades of the muscle nerve and local cooling of the muscle belly. 1. The recruitment order of certain low and certain high frequency units was reversed. 2. The muscle tension and sense of effort necessary for tonic firing were increased for certain low frequency units but decreased for certain high frequency units. 3. On severe reduction of the afferent inflow, the differences in discharge pattern between low and high frequency units were decreased. It is concluded that the recruitment of low frequency units before high frequency units in sustained voluntary contraction is partly due to proprioceptive afferent activity favouring low frequency units and disfavouring high frequency units. It is also concluded that the afferent inflow is involved in restricting certain units to low frequency discharge and others to high frequency discharge.

Differences in recruitment order of motor units in phasic and tonic flexion reflex in "spinal man".

The recruitment order of motoneurones in muscle contractions has been held to be largely constant and determined by the size of the cell. However, as shown in a previous investigation using electromyographic techniques, the order in which different motor units are activated during voluntary muscle contractions changes in normal human subjects on shifts from phasic to tonic contraction. In order to investigate these two types of activity also in cases in which the cerebral influence on the motoneurone pool is blocked, an analysis was made of the recruitment order in phasic and tonic flexion reflexes in 10 patients with total interruption of the spinal cord. The following four principles were found to apply and presumed to be generally valid for the isolated human spinal cord: (1) in the phasic exteroceptive reflex, the order of recruitment varies despite application of a standardized stimulus; (2) in the tonic reflex, the first unit to be recruited is usually the same even with widely different types of stimuli; (3) a shift from phasic to tonic reflex activation may result in considerable changes in recruitment order; (4) after facilitation by a subliminal long-lasting stimulus, the first unit to be recruited in the phasic reflex is also the first to be recruited in the tonic reflex. It is suggested that a tonic influence on the motoneurone pool is required for the presupposed constancy of the recruitment order.

The afferent influence on the voluntary firing range of individual motor units in man.

The firing ranges of 50 normal anterior tibial or short toe extensor motor units in sustained isometric voluntary contraction were studied in electromyographic recordings. The afferent inflow was decreased by compression of the sciatic nerve, thereby blocking large afferents before alpha efferents. Motor units with low minimum and low maximum rates before blockade had higher minimum and maximum rates before blockade had a lower minimum but an unchanged maximum rate on blockade. The firing range recorded for both types of motor unit on blockade was also recorded for all tonically firing motor units during early reinnervation after traumatic lesion to the muscle nerve in 14 patients. It is concluded that both facilitating and inhibiting proprioceptive afferent activity is involved in the differentiation of motor unit firing ranges in sustained isometric voluntary contraction.

Axonal conduction velocity and voluntary discharge properties of individual short toe extensor motor units in man.

1. The axonal conduction velocity and the voluntary discharge properties of 120 short toe extensor motor units were studied in man. 2. Electromyographic techniques were used which permitted the identification of individual motor unit potentials after proximal and distal electrical nerve stimulation and during maximum voluntary effort. 3. The necessary selectivity of the e.m.g. recordings was achieved in two circumstances. In some subjects, previous motor nerve lesions distal to the point of stimulation had led to collateral sprouting with larger motor unit potentials. In other subjects an accessory deep peroneal nerve was present, so that lidocaine block of the main motor nerve left a small number of innervated motor units. 4. The axonal conduction velocities of the individual motor units ranged from 30 to 54 m/sec with most motor units between 35 and 45 m/sec. 5. Motor units which voluntarily could be driven continuously at frequencies below 10/sec had axonal conduction velocities between 30 and 45 m/sec. 6. Motor units which on voluntary drive responded only in high frequency bursts had axonal conduction velocities between 40 and 54 m/sec. 7. Motor units with intermediate voluntary discharge properties had intermediate axonal conduction velocities. 8. Thus a relationship was established between voluntary discharge properties and axonal conduction velocity.

Motor neuron firing range, axonal conduction velocity, and muscle fiber histochemistry in neuromuscular diseases.

The voluntary discharge properties and axonal conduction velocity of single motor units were studied in patients with neuromuscular diseases with retained differentiation of the muscle fibers into type 1 and type 2, and in patients with late-onset hereditary distal myopathy in which muscle fibers have only intermediate histochemical properties. In the patients with muscle fiber differentiation, the findings were similar to those in normal subjects; that is, there was a continuum between motor units which fired tonically at low rates and had a low axonal conduction velocity, and motor units which fired phasically at high rates and had a high axonal conduction velocity. In the patients without muscle fiber differentiation, all motor units had intermediate firing properties and a low axonal conduction velocity. It is suggested that in chronic pathologic states, the differentiation of the muscle fiber histochemistry remains only as long as the differentiation of the motor neurons remains.

Contraction time and voluntary discharge properties of individual short toe extensor motor units in man.

1. The contraction time and the voluntary discharge properties of forty-five short toe extensor motor units were studied in man. 2. The contraction time of the individual motor unit was studied by using selective electrical nerve stimulation or by averaging the increase in force related to its electromyographic potential in tonic voluntary contraction. 3. Both methods showed a range of contraction times from 40 to 90 ms. 4. The discharge properties of the individual motor unit were studied with e.m.g. techniques, permitting the identification of its potentials during maximum voluntary effort. 5. A motor unit which could be driven continously and had a minimum rate of about 10/s and a maximum rate of about 30/s had a contraction time between 60 and 90 ms. 6. A motor unit which could not be driven continously and had a minimum rate of about 20/s and a maximum rate above 40/s had a contraction time between 40 and 55 ms. 7. A motor unit with intermediate voluntary discharge properties had an intermediate contraction time. 8. It is concluded that each motor unit fires at its fusion frequency in voluntary contraction and that the voluntary discharge frequency range of a motor unit can be used as an indication of its contraction time.

Disturbances in the voluntary recruitment order of anterior tibial motor units in spastic paraparesis upon fatigue.

The recruitment order of motor units in the tibialis anterior muscle upon fatigue of tonic voluntary contraction was studied in 20 patients with severe spastic paraparesis. An electromyographic technique for secure identification of single motor units was used. Before fatigue the recruitment order is stable and low-frequency units are recruited before high-frequency units; this recruitment pattern agrees with that in normal voluntary activity. When fatigue appears, however, the recruitment order becomes indefinite and high-frequency units can be recruited before low-frequency units; this recruitment pattern agrees with that in normal phasic voluntary activity. Finally, all voluntary activation power disappears, even in the case of units which have never been active. Contraction ability and original recruitment order are restored upon rest but also upon tonic reflex support of the voluntary drive. Whether the fatigue reaction may be due to insufficient gamma motoneurone innervation and whether it is related to spasticity are discussed. The practical physiotherapeutic implications are reviewed.

Motoneuron activity and muscle fibre type composition in hemiparesis.

The firing of single motor units (MUs) in musculus tibialis anterior (TA) was studied during maximal voluntary effort and maximal speed of walking in 10 patients with severe chronic hemiparesis and the findings compared to normal data. As shown in a previous study, the paralysed TA exhibited an increase in proportion of type 2 fibres as compared with normal muscle. Thus, 57% of the muscle fibres were type 1 and 43% type 2, while the normal percentages were 80% and 20% respectively. The present findings indicate that in the paralysed muscles a little less than half of the fibres, i.e. roughly the equivalent of the type 2 population, was not tonically active either during sustained voluntary contraction or during locomotion. Normally high threshold MUs reached high rates during both modes of activation. The findings paralysed muscles also indicate that a little more than half of the fibres, i.e. roughly the equivalent of the type 1 population, could be brought into tonic firing during voluntary contraction as well as during walking. Their maximal firing rate was, however, no more than two thirds of that of normal low threshold MUs.

Pathophysiology of fasciculations in ALS as studied by electromyography of single motor units.

Electromyographic potentials of fasciculations were studied in ten patients with amyotrophic lateral sclerosis (ALS). The EMG recordings were made from the extensor digitorum brevis muscle. The EMG recording was so selective that only one motor unit potential appeared on maximal voluntary effort and on supramaximal electrical stimulation of the peroneal nerve. In a series of fasciculations, the shapes of the EMG potentials varied, while in a series of voluntary twitch activations of electrical nerve stimulations the EMG potentials were mainly constant. Fasciculations were followed by antidromic impulses in the test unit axon as judged from collision tests, and they persisted after lidocaine blockades of the nerve to the muscle. The findings are compatible with a conclusion of distal multifocal triggering of fasciculation. Fasciculating motor units had voluntary firing properties close to those of normal low-threshold motor units. Widespread fasciculations were abolished by a nonparalytic dose of a synthetic curare derivative (Pavulon) and augmented by administration of neostigmine in two cases. The fasciculations in ALS thus have the same characteristics as experimental fasciculations evoked by cholinesterase inhibitors, and there is reason to believe that the underlying pathophysiological mechanism is similar in the two cases.