The role of support afferents in organisation of the tonic muscle system

Results of experimental studies are reviewed that point out to the leading role of the support afferents in control of structural-functional properties of the tonic muscle system. It is shown that the support afferents play a role of the trigger in the postural system, the trigger enhancing (when the support is present) or inhibiting (when the support is withdrawn) the activity of tonic motor units (MU's). Under the absence of support condition, recorded in extensors are: an obvious decline of the muscle stiffness and the maximal voluntary force; a significant decrease of the absolute force of the isometric contraction of single skin muscle fibers evoked by Ca++; a prominent decline of the tonic muscle fibers transversal size; and the transformation of the myosin phenotype from slow to fast one. Mechanical stimulation of the support zones of soles in the regimes of locomotion (slow and fast stepping) under the absence of support condition eliminates all the above effects.     

Contractile characteristics of the triceps surae muscle in healthy males during 120-days head-down tilt (HDT) and countermeasures

To reveal mechanisms responsible for changes in muscle contractility during microgravity, it seems expedient to perform similar studies under microgravity or conditions simulating microgravity. Among standard methods for simulating microgravity, hypokinesia modelling support unloading (or rather its redistribution), and hypodynamia are employed. Absence of weight loading, decreased muscular effort characteristic of the Earth conditions due to counteracting gravity, results in a general muscle underloading and therefore in lowered activity of the proprioceptive input. This may be one of the reasons not only for a resetting of motor coordination and control, but also for a gradual development of a persistent change in the motor control system. The basis of countermeasures against negative consequences of microgravity (hypokinesia) is the correct choice of countermeasures. In this connection of specific interest is a study of the magnitude of change in skeletal muscle contractility in humans after a variety of countermeasures when functional activity is lowered by a long-term 120-days HDT which is an adequate simulation of physiological microgravity-induced effects.     

Mechanic stimulation of the soles support zones as a countermeasure of the contractile properties decline under microgravity conditions

Decrease in muscle contractility is an inevitable consequence of exposure in microgravity. A wealth of currently accumulated facts is indicative of profound modifications in structure and function of the skeletal muscles in the absence of gravity. Investigations with humans during space flights of varying duration (L.I. Kakurin et al., 1971; I.B. Kozlovskaya et al., 1984, 1987, 1991;.), ground-based simulation studies (A.M. Genin et al., 1969; L.S. Grigorieva et al., 1983), and numerous experiments with animals (E.I. IIyina-Kakueva et al., 1979; O.M. Edgerton et al 1991; B.S. Shenkman et al., 1994) made it evident that removal of gravitational loading is fraught with significant reductions in the contractile properties of muscular fibers, especially noticeable in muscles-extensors. Results of ground-based simulation studies led to the hypothesis that changes in muscle contractility developing already after few days in microgravity conditions are consequent to reduction in support afferentation that plays an important role in initiation and maintenance of the activity of tonic motor units (A.V. Kirenskaya et al., 1986). In view of the above, an idea has been proposed to prevent losses in tonic muscles contractility by application of artificial support. Testing of this hypothesis was the theme of the present investigation.     

Common motor mechanisms support body load in serially homologous legs of cockroaches in posture and walking

We studied the mechanisms underlying support of body load in posture and walking in serially homologous legs of cockroaches. Activities of the trochanteral extensor muscle in the front or middle legs were recorded neurographically while animals were videotaped. Body load was increased via magnets attached to the thorax and varied through a coil below the substrate. In posture, tonic firing of the slow trochanteral extensor motoneuron (Ds) in each leg was strongly modulated by changing body load. Rapid load increases produced decreases in body height and sharp increments in extensor firing. The peak of extensor activity more closely approximated the maximum velocity of body displacement than the body position. In walking, extensor bursts in front and middle legs were initiated during swing and continued into the stance phase. Moderate tonic increases in body load elicited similar, specific, phase dependent changes in both legs: extensor firing was not altered in swing but was higher after foot placement in stance. These motor adjustments to load are not anticipatory but apparently depend upon sensory feedback. These data are consistent with previous findings in the hind legs and support the idea that body load is countered by common motor mechanisms in serially homologous legs.     

Neural and neuroendocrine adaptations to microgravity and ground-based models of microgravity

The functional properties of the motor system of humans and non-human primates are readily responsive to microgravity. There is a growing body of evidence that significant adaptations occur in the spinal cord and muscle in response to prolonged exposure to microgravity. Further, there is evidence that the processing of sensory information from the periphery, particularly that input associated with the function of muscle tendons and joints, is significantly altered as a result of prolonged microgravity. We present evidence that the fundamental neural mechanisms that control the relative activity of the motor pools of a slow and fast extensor muscle is changed such that a slow, postural muscle is less readily activated during locomotion following spaceflight. Another type of change observed in mammals exposed to spaceflight relates to the release of a growth factor, called bioassayable growth hormone, which is thought to be released from the pituitary. When an individual generates a series of isometric plantarflexor contractions, the plasma levels of bioassayable growth hormone increases significantly. This response is suppressed after several days of continuous bedrest or spaceflight. These results suggest a unique neuroendocrine control system and demonstrate its sensitivity to chronic patterns of proprioceptive input associated with load-bearing locomotion.     

Recruitment of the Rhesus soleus and medial gastrocnemius before, during and after spaceflight

Electromyograms were recorded from the soleus and medial gastrocnemius muscles and tendon force from the medial gastrocnemius muscle of 2 juvenile Rhesus monkeys before, during and after Cosmos flight 2229 and of ground control animals. Recording sessions were made while the Rhesus were performing a foot pedal motor task. Preflight testing indicated normal patterns of recruitment between the soleus and medial gastrocnemius, i.e. a higher level of recruitment of the soleus compared to the medial gastrocnemius during the task. Recording began two days into the spaceflight and showed that the media gastrocnemius was recruited preferentially over the soleus. This observation persisted throughout the flight and for the 2 week period of postflight testing. These data indicate a significant change in the relative recruitment of slow and fast extensor muscles under microgravity conditions. The appearance of clonic-like activity in one muscle of each Rhesus during flight further suggests a reorganization in the neuromotor system in a microgravity environment.     

New approaches in the rehabilitation of patients with central nervous system lesions based on the gravitational mechanisms

This review discusses the functioning of the motor system under normal and reduced gravity. Analysis of the experimental data led to the conclusion that all changes in the functioning of tonic muscular system are related to each other. When transiting to the state of microgravity, changes are caused by one common factor, namely a sharp decrease in the activity of support afferent input, specifically oriented to the perception and analysis of gravitational loads and firmly embedded in the mechanisms of postural synergism organization. We analyzed data obtained in studies on the activation of cortical areas of the brain during the stimulation of support afferents in order to test the hypothesis that such stimulation in both healthy subjects and patients with neurologic deficiency leads to activation of both the sensory and motor cortex involved in supraspinal control of the movement of the lower limbs, in particular when walking.     

The effect of activity during early postnatal development on motor unit size

At early stages of neuromuscular development, motor unit territory is expanded, with each muscle fibre being supplied by several axons. During postnatal development, some synapses are eliminated, motor unit size decreases, and the adult distribution of motor unit sizes emerges. This process depends on activity, since it proceeds more rapidly when the nerve is activated and is slower when activity is reduced. Here we studied whether, in addition to influencing the rate of retraction of motor unit territory, activity during the critical period of development affects the final outcome of the distribution of motor unit sizes. The sciatic nerve of 8- to 12-day-old rats was stimulated daily. One week later the tension of the extensor digitorum longus muscle and that of its individual motor units was recorded. The sizes of individual motor units were calculated and compared with those from animals that received no stimulation. The distribution of motor unit sizes from stimulated muscles was not significantly different from those from control muscles. Therefore, we conclude that although activity increases the rate at which motor units attain their adult size, it does not influence the final outcome of motor unit size distribution.     

Correlation of the neuronal impulse activity of different areas of the neocortex in rabbits in the switching of positive and inhibitory conditioned reflexes

By cross-correlation method conjugation in impulse activity of pairs of simultaneously recorded units in the visual and sensorimotor areas of the neocortex (representations of the conditioned and unconditioned stimuli) was studied during the switching of defensive positive and inhibitory reflexes in rabbits. 30-second fragments of impulse activity were analyzed in intervals before and after three presentations of positive and inhibitory conditioned stimuli (CS). The activity of single pairs of units in the process of stimuli presentation was characterized by instability. Only in 29% of 51 units' pairs the presence or absence of correlation between their discharges was stable. Analysis of activity of 75 pairs of units showed differences in impulse activity in inhibitory and positive tonic reflexes. The number of pairs of correlated units in about 30 s after inhibitory CS decreased (27%) in comparison with the interval before its action (52%). In the inhibitory tonic conditioned reflex, temporal intervals of discharges of one unit correlated with discharges of the second unit undergo changes. The obtained results testify that such parameter as the number of pairs of units with correlated activity in intersignal time interval is very important for the realization of motor reaction to conditioned stimuli.     

Properties of twitch motor units of the ankle extensor muscles in the bullfrog Rana catesbeiana

A study of the mechanical properties of the twitch motor units in the ankle extensor muscles of bullfrogs was undertaken to expand our view of the diversity of motor unit properties among vertebrates. Two muscles were chosen that represent a wide range of extensor function: the plantaris longus (PL) is a large muscle providing most of the force for ankle extension in hopping and swimming, and the tibialis posticus (TP) is relatively small and may act as an ankle stabilizer or be primarily postural in function. Both muscles have highly fatigable motor units, but also some (especially in TP) low or non-fatigable ones. Mean tetanic tensions of motor units in both muscles are relatively large as compared with those of mammals but are especially large in PL, No clear correlations were found between contraction times and either motor unit tetanic tensions or fatigability, nor did the motor units fall into clearly defined types based on any functional parameters. Overall contraction and relaxation times are slow compared with those of mammals and are somewhat slow compared to those of other frogs; unlike results from earlier studies, the large units of PL are slower than the small units of TP. This results in PL units reaching fused tetani at lower stimulus frequencies. The twitch/tetanus and force/frequency ratios in PL motor units are much larger than those of TP, giving PL units greater relative forces at lower stimulus rates. These results are discussed in the context of motor unit function. © 1994 Wiley-Liss, Inc.     

Rate-coding of spinal motoneurons with high-frequency magnetic stimulation of human motor cortex

Rate-coding in spinal motoneurons was studied using high-frequency magnetic stimulation of the human motor cortex. The subject made a weak contraction to cause rhythmic (i.e., tonic) discharge of a single motor unit in flexor (or extensor) carpi radialis or tibialis anterior, while the motor cortical representation of that muscle was stimulated with brief trains of pulses from a Pyramid stimulator (4 Magstim units connected by 3 BiStim modules). An "m@n" stimulus train consisted of m number of pulses (1-4), with an interpulse interval (IPI) of n ms (1-6). Peristimulus time histograms were constructed for each stimulus condition of a given motor unit, and related to the average rectified surface electromyography (EMG) from that muscle. Surface EMG responses showed markedly more facilitation than single-pulse stimulation, with increasing numbers of pulses in the train; responses also tended to increase in magnitude for the longer IPI values (4 and 6 ms) tested. Motor-unit response probability increased in a manner comparable to that of surface EMG. In particular, motoneurons frequently responded twice to a given stimulus train. In addition to recruitment of new motor units, the increased surface EMG responses were, in part, a direct consequence of short-term rate-coding within the tonically discharging motoneuron. Our results suggest that human corticomotoneurons are capable of reliably following high-frequency magnetic stimulation rates, and that this activity pattern is carried over to the spinal motoneuron, enabling it to discharge at extremely high rates for brief periods of time, a pattern known to be optimal for force generation at the onset of a muscle contraction.     

Human Performance in a Realistic Instrument-Control Task during Short-Term Microgravity

Previous studies have documented the detrimental effects of microgravity on human sensorimotor skills. While that work dealt with simple, laboratory-type skills, we now evaluate the effects of microgravity on a complex, realistic instrument-control skill. Twelve participants controlled a simulated power plant during the short-term microgravity intervals of parabolic flight as well as during level flight. To this end they watched multiple displays, made strategic decisions and used multiple actuators to maximize their virtual earnings from the power plant. We quantified control efficiency as the participants’ net earnings (revenue minus expenses), motor performance as hand kinematics and dynamics, and stress as cortisol level, self-assessed mood and self-assessed workload. We found that compared to normal gravity, control efficiency substantially decreased in microgravity, hand velocity slowed down, and cortisol level and perceived physical strain increased, but other stress and motor scores didn’t change. Furthermore, control efficiency was not correlated with motor and stress scores. From this we conclude that realistic instrument control was degraded in short-term microgravity. This degradation can’t be explained by the motor and/or stress indicators under study, and microgravity affected motor performance differently in our complex, realistic skill than in the simple, laboratory-type skills of earlier studies.     

The participation of the cholinergic system of the rat sensorimotor cortex in regulating different types of movements

To study the role of the cholinergic system of the sensorimotor cortex in regulation of different manipulatory movements and locomotion of Wistar rats, the effects of injections of cholinergic drugs (a cholinergic agonist carbachol and an antagonist scopolamine) into the area of forepaw representation in the sensorimotor cortex on motor activity and performance of manipulatory movements (with prolonged and short pushing) were analyzed. The drugs were injected via special cannulae stereotaxically implanted into the cortex during surgery carried out under Nembutal anesthesia. Carbachol injections (0.03-3 micrograms in 1 microliter of physiologic solution) into the cortex resulted in a significant slowing down of both types of movements as well as an increase in locomotion in the open-field test. Injections of scopolamine (0.3-3 micrograms) into the same cortical area were accompanied by an increase in the number of fast manipulatory movements without significant changes in locomotor activity. The obtained evidence suggests that the cholinergic system of the sensorimotor cortex indifferent manners regulates the innate (locomotion) and acquired movements which require different periods of maintaining the muscle tone of the forepaw (short-time periods for the usual movements necessary for food taking from the narrow horizontal tube and prolonged periods for the learned slow movements with additional tactile and tonic components).     

An Attempt to Account for the Diversity of Crustacean Muscles

Crustacean muscles are known to contain muscle fibers of variableproperties and to be innervated by phasic and/or tonic motoneuronswhich may possess synapses of diverse physiological properties.Frequently, phasic motor axons innervate short-sarcomere phasicmuscle fibers and tonic motor axons innervate long-sarcomeretonic muscle fibers, but some muscles receiving a single (tonic)motor axon contain both phasic and tonic muscle fibers. Althoughit is not known whether neural trophic influences are involvedin muscle differentiation, some neural trophic effects havebeen found in crustaceans, and it is reasonable to assume thatsuch influences may be involved in establishing the definitiveproperties of the muscle. Several other postulates must be made:(1) Phasic and tonic motor axons differ in their trophic effectiveness:(2) muscle fibers innervated relatively early in developmentby a tonic motor axon acquire the properties of tonic musclefibers, while those innervated later become intermediate orphasic muscle fibers; (3) the developmental stage of a growingor regenerating axon terminal plays a role in determinationof synaptic properties. Studies on regenerating limb buds supportthe hypothesis, which can account for the genesis of all observedtypes of crustacean neuromuscular system. Further experimentalwork is necessary to test the hypothesis.     

An integrative approach to the biomechanical function and neuromuscular control of the fingers

The exquisite mechanical functionality and versatility of the human hand emerges from complex neuro-musculo-skeletal interactions that are not completely understood. I have found it useful to work within a theoretical/experimental paradigm that outlines the fundamental neuro-musculo-skeletal components and their interactions. In this integrative paradigm, the laws of mechanics, the specifications of the manipulation task, and the sensorimotor signals define the interactions among hand anatomy, the nervous system, and manipulation function. Thus, our collaborative research activities emphasize a firm grounding in the mechanics of finger function, insistence on anatomical detail, and meticulous characterization of muscle activity. This overview of our work on precision pinch (i.e., the ability to produce and control fingertip forces) presents some of our findings around three Research Themes: Mechanics-based quantification of manipulation ability; Anatomically realistic musculoskeletal finger models; and Neural control of finger muscles. I conclude that (i) driving the fingers to some limit of sensorimotor performance is instrumental to elucidating motor control strategies; (ii) that the cross-over of tendons from flexors to extensors in the extensor mechanism is needed to produce force in every direction, and (iii) the anatomical routing of multiarticular muscles makes co-contraction unavoidable for many tasks. Moreover, creating realistic and clinically useful finger models still requires developing new computational means to simulate the viscoelastic tendinous networks of the extensor mechanism, and the muscle-bone-ligament interactions in complex articulations. Building upon this neuromuscular biomechanics paradigm is of immense clinical relevance: it will be instrumental to the development of clinical treatments to preserve and restore manual ability in people suffering from neurological and orthopedic conditions. This understanding will also advance the design and control of robotic hands whose performance lags far behind that of their biological counterparts.     

Mechanical properties of locust extensor tibiae muscles

• 1.1. The prothoracic and mesothoracic extensor tibiae muscles of the locust respond to activity in the “slow” extensor tibiae motoneuron (SETi) with very slow contractions and a low fusion frequency, while their phasic contractions are more rapid than those of the metathoracic extensor tibiae muscle.
• 2.2. SETi activity can induce a memory or “catch” effect in which a high tension is maintained by a lower frequency than is needed to develop it. “Catch” tension is reduced by phasic contractions of the muscle or by activity in the inhibitory axon.
• 3.3. A bundle of tonic fibres isolated from the metathoracic extensor tibiae muscle exhibits co-ordinated rhythmic contractions similar to those recorded from intact muscles.
• 4.4. Depolarizations of the tonic fibres coincide with the contractions and are sometimes accompanied by bursts of EPSPs and IPSPs.
• 5.5. The tonic fibres are electrically-coupled.

     

Methodological aspects of SEMG recordings for force estimation – A tutorial and review

Insight into the magnitude of muscle forces is important in biomechanics research, for example because muscle forces are the main determinants of joint loading. Unfortunately muscle forces cannot be calculated directly and can only be measured using invasive procedures. Therefore, estimates of muscle force based on surface EMG measurements are frequently used. This review discusses the problems associated with surface EMG in muscle force estimation and the solutions that novel methodological developments provide to this problem. First, some basic aspects of muscle activity and EMG are reviewed and related to EMG amplitude estimation. The main methodological issues in EMG amplitude estimation are precision and representativeness. Lack of precision arises directly from the stochastic nature of the EMG signal as the summation of a series of randomly occurring polyphasic motor unit potentials and the resulting random constructive and destructive (phase cancellation) superimpositions. Representativeness is an issue due the structural and functional heterogeneity of muscles. Novel methods, i.e. multi-channel monopolar EMG and high-pass filtering or whitening of conventional bipolar EMG allow substantially less variable estimates of the EMG amplitude and yield better estimates of muscle force by (1) reducing effects of phase cancellation, and (2) adequate representation of the heterogeneous activity of motor units within a muscle. With such methods, highly accurate predictions of force, even of the minute force fluctuations that occur during an isometric and isotonic contraction have been achieved. For dynamic contractions, EMG-based force estimates are confounded by the effects of muscle length and contraction velocity on force producing capacity. These contractions require EMG amplitude estimates to be combined with modeling of muscle contraction dynamics to achieve valid force predictions.     

Patterns of activity in the antennular motoneurones of the hermit crab Pagurus alaskensis (Benedict).

1. Using electromyogram recordings from the antennular muscles of intact animals and recordings from the antennular nerves of partially dissected preparations, the patterns of activity in specific antennular motoneurones have been described during antennular flicking and antennular withdrawal. 2. The slow extensor motoneurone A30S is active during flicking in addition to the phasic component of the antennular motor system (A30F, A31F and A32F). 3. The flexion phase of a flick is the result of a burst of variable duration and number of spikes within flexor motoneurones A31F and A32F. 4. The extension phase of a flick is the result of a burst of variable duration and number of spikes in extensor motoneurones A30F and A30S. 5. Extension-withdrawal and slow flexion-withdrawal reflexes, tonic flexion withdrawal and maintained flexion at the MS-DS joint usually result from activity in part of the tonic component of the antennular motor system:moto-neurones A30S, A31S and A32S. 6. Fast flexion-withdrawal reflexes result from a burst of spikes in motoneurone A31F-S which constitutes the phaso-tonic component of the antennular motor system. 7. During high-frequency activity (15-60/sec), reciprocity exists between the slow flexor motoneurones A31S and A32S and slow extensor motoneurone A30S.     

The cord stretch receptors in the abdominal nerve cord of the crayfish Cherax destructor: physiology and relationships

The physiology and relationships of tonic cord stretch receptor neurons in the crayfish Cherax destructor were examined with intracellular and extracellular recording. Cord stretch evoked slow depolarisations leading to action potentials in tonic cord stretch receptor neurons. Intermittent post-synaptic potentials were also seen in cord stretch receptor neurons but were not the primary cause of the action potentials. Cord stretch still evoked action potentials in cord stretch receptor neurons when all synaptic activity, monitored at another known chemical synapse, was blocked using high [Mg(2+)] and low [Ca(2+)] in the bath. One source of facilitating excitatory post-synaptic potentials in the cord stretch receptor neurons was from mechanosensory hairs on the dorsal abdominal surface. Tonic cord stretch receptor neuron activity was associated with an increase in the activity of the abdominal slow extensor inhibitor motor neuron and at least one abdominal flexor excitor motor neuron in its segment, and reduced activity in the abdominal slow flexor inhibitor motor neuron. Activation of individual cord stretch receptor neurons produced a local resistance reflex. Cord stretch, activating many receptors, produced several other outcomes. One was the "extensor state" described in earlier literature. The tonic cord stretch receptor neurons of Cherax destructor appear to be stretch-sensitive interneurons that receive inputs from other elements of the abdominal control system and mediate polysynaptic reflex activity in postural motor neurons.     

Motor function in microgravity: movement in weightlessness

Microgravity provides unique, though experimentally challenging, opportunities to study motor control. A traditional research focus has been the effects of linear acceleration on vestibular responses to angular acceleration. Evidence is accumulating that the high-frequency vestibulo-ocular reflex (VOR) is not affected by transitions from a 1 g linear force field to microgravity (<1 g); however, it appears that the three-dimensional organization of the VOR is dependent on gravitoinertial force levels. Some of the observed effects of microgravity on head and arm movement control appear to depend on the previously undetected inputs of cervical and brachial proprioception, which change almost immediately in response to alterations in background force levels. Recent studies of post-flight disturbances of posture and locomotion are revealing sensorimotor mechanisms that adjust over periods ranging from hours to weeks.