Effect of the tendon reflex on motoneurons of the antagonist muscle in man

The knee jerk was elicited during regular firing of relatively low-threshold motor units of the biceps femoris muscle (during weak voluntary contraction). Besides the reflex response of the rectus femoris muscle, synchronous discharges of motor units of the biceps femoris muscle and activation of new motor units also were observed. Poststimulus histograms and statistical analysis of interspike intervals of motor units of the biceps femoris muscle revealed well-marked excitatory influences synchronous with the reflex response of the rectus femoris. This result can be explained by the presence of excitatory inputs of Ia afferents on motoneurons of the antagonist muscle. In the knee jerk, excitation of motoneurons of the antagonist was followed by later inhibitory influences which evidently correspond to the "silent period" of motoneurons of the agonist muscle during the elicitation of its tendon reflex.Institute for Problems of Information Transmission, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 8, No. 6, pp. 624–632, November–December, 1976.     

Functional Anatomy of the Association Between Motor Units and Muscle Receptors

Muscle spindles and tendon organs occur in most somatic musclesof the mammal and are particularly concentrated in muscles subservingfine movements, including postural muscles and small musclesof the distal extremities. In those mixed muscles in which thedifferent fiber and motor unit types are "compartmentalized,"the spindles, and perhaps tendon organs also, are virtuallylimited to those compartments predominated by "oxidative" musclefibers. These morphological observations based on a broad arrayof muscles in many species, complement electrophysiologicalstudies which have emphasized that (1) the "oxidative" motorunits have low reflex thresholds and (2) segmental proprioceptivereflexes may be primarily concerned with the control of finelygraded contractions. Consideration of the functional anatomyof the association between motor units and muscle receptorssuggests the need for detailed structural-functional analysesof those muscles with specializations in architecture, fiber-typecomposition and distribution, and in the number and distributionof their muscle spindles and tendon organs. An electrophysiologicalanalysis of the relationship between the spinal cord and suchmuscles might also reveal certain strategies and mechanismsunderlying segmental motor control which are either absent orobscured in the analysis of that select number of "homogenously-mixed"muscles conventionally used in the study of the mammalian segmentalmotor control system.     

Activity of fusimotor neurons during reflex muscle contraction

The influence of fusimotor activity via the gamma-loop on reflex responses of motoneurons to stretch or vibration stimulation of mm. triceps surae was studied in decerebrate cats. Action potentials of single fusimotor neurons were derived from thin filaments isolated from nerves innervating this muscle group, leaving their main nerve supply intact. Most fusimotor neurons tested were found to be coactivated with motor units during reflex muscle contraction. In the initial period of development of reflex muscle contraction a weak autogenetic inhibitory effect on discharge of fusimotor neurons was found. The results suggest that reduction of the reflex motor signal, leading to a "silent period," is partly the result of a transient decrease in the fusimotor output effect on contracting muscles. A study of changes in fusimotor discharge generation during the ascending phase of reflex muscle contraction may provide data useful for identification of autogenetic reflex influences on these motoneurons and for elucidating the conditions necessary for servoassistance of muscle contractions.Medical Research Institute, Belgrade, Yugoslavia. Translated from Neirofiziologiya, Vol. 16, No. 5, pp. 630–637, September–October, 1984.     

Changes in the excitability of and synaptic effects on motoneurons during formation of the scratch motion generator in the cat

Studies on immobilized decerebrate (at intracollicular level) cats in which the scratch generator had been set up following bicuculline application to the upper cervical segments of the spinal cord, showed that the state of the segmental apparatus of the lumbosacral section of the spinal cord differs substantially from that seen in the spinal animal. Direct excitability of motoneurons of the "aiming" and "scratching" muscles rises, while recurrent and reciprocal Ia inhibition of motoneurons intensifies and the influence of Ib afferents on motoneurons declines. Afferents of the flexor reflex exert a primarily inhibitory influence on motoneurons of the "aiming" muscles. This influence becomes predominantly excitatory following spinalization, while the inhibitory effects of these afferents on motoneurons of the "scratch" muscles declines. The functional significance of the changes discovered in generation of scratch routine is discussed.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 19, No. 2, pp. 244–250, March–April, 1987.     

The role of reflex mechanisms in postinhibitory rebound studied by analysis of human single motor unit activity

The mechanism of onset of rebound after inhibition induced by electrical stimulation of a nerve of maximal and submaximal strength for M-response was studied in single motor units of normal human soleus, rectus femoris, and hand muscles. Poststimulus histograms and changes in the duration of interspike intervals were compared with mechanical recordings of muscle contractions. In all muscles tested, during strong isotonic contraction, the increase in motor unit activity after a silent period was partly due to synchronization of their emergence from inhibition. However, it also contained a component of true facilitation of motoneurons, which was evidently a reflex response to lengthening of the muscle in the relaxation phase after evoked contraction. The latent period of this facilitation in the soleus and rectus femoris muscles coincided in value with the latent period of the monosynaptic spinal reflex, whereas in the hand muscles, in which a monosynaptic response to electrical nerve stimulation could not be evoked, the latent period of facilitation as a result of spindle activation during muscle relaxation was significantly longer than the latent period of the monosynaptic reflex. These findings support the hypothesis of presynaptic suppression of monosynaptic connections of Ia afferents with the motoneurons of some human muscles by descending tonic influences and of the use of information coming from spindles by supraspinal levels of the CNS.     

Muscle Plasticity During Sprouting and Reinnervation

SYNOPSIS. When peripheral nerves are cut, the axotomized nervesand denervated muscles undergo atrophic changes which are reversedonly when functional connections are remade in the periphery.The restored interaction completely reverses the effects ofaxotomy and denervation and leads to rematching of the sizeof the motoneuron, muscle unit force, speed and histochemicalproperties, according to the size principle. Differences inunit force and fatigue characteristics between motor unit typesare not fully restored in reinnervated muscles but do not obscuresize relationships between the motoneurons and their muscleunits. Although intact motoneurons will supply increased numbers ofmuscle fibers after partial nerve injuries, regenerating axonsappear to be limited in their ability to enlarge their muscleunits. Increased motor unit force in reinnervated slow motorunits is accounted for primarily by an increase in fiber diameter;fast motor units do not increase their mean force output. As a result of the rematching of muscle unit properties withthe size of the motoneurons that reinnervate them, motor unitproperties are appropriate for fine control of movement aftercomplete or partial nerve injuries. However, regenerating axonsdo not reinnervate their original muscle fibers and unless thefibers are injured close to the muscles, they often fail toreinnervate their original muscles. The mismatching of motorpools with inappropriate target muscles is probably the mainfactor responsible for poor recovery of motor function aftercomplete nerve injuries.     

Motor unit recruitment patterns during reflex compensation of muscle yield investigated by computer simulations

 An important function of the stretch reflex in the soleus muscle in the decerebrate cat preparation is to compensate for the tendency of muscle suddenly to yield during ramp increases in length. As the level of background (i.e. pre-stretch) force increases, there is a systematic change in the curvature of the force trajectory during this reflex compensation, from concave to convex with respect to increasing force. The hypothesis that this change in curvature was due to background force-dependent changes in the recruitment pattern of motor units was investigated with a combined computer simulation/ experimental technique. The simulation consisted of 20 model motor units for the soleus muscle, each based on a distributed moment muscle model. The timing of recruitment of the motor units was optimized to allow the simulation outputs to fit a set of experimental data records on the reflex response to stretch initiated at five different levels of pre-stretch force. The resulting recruitment patterns showed that a tendency for recruitment to be concentrated progressively in the early portion of the stretch as pre-stretch force increased could account for the changes in reflex force curvature. These results are consistent with the skewed distribution of intrinsic electrical thresholds of motoneurons, in which low-threshold units are much more frequent than high-threshold ones. Therefore the changes in recruitment pattern and reflex force curvature may be due primarily to the intrinsic properties of motoneurons. Received: 18 September 1995/Accepted in revised form: 21 May 1996     

Electroneuromyography analysis of reduced exercise performance in patients with lumbosacral osteochondrosis

The functional activity of the segmental apparatus and skeletal muscles of the upper and lower extremities was examined using various techniques, mainly, comprehensive electroneuromyography, in patients with lumbosacral osteochondrosis. Among the findings were significant differences between the H and the M responses of the soleus muscle, increased presynaptic inhibition of spinal motoneurons, and alteration in their reflex excitability, which explains the reduction in the exercise performance of the crus muscles as a result of the damage of spinal nerve roots involved in this pathology.     

Motor Units: Physiological/Histochemical Profiles, Neural Connectivity and Functional Specializations

This brief review considers muscles as ensembles of motor units,the viewpoint usually taken by motor systems physiologists.The morphological, histochemical and mechanical properties ofmuscle units are discussed in relation to the intrinsic propertiesof the motoneurons that innervate them, and in connection withthe organization of synaptic inputs that play a significantrole in determining functional usage. These factors, from synapticorganization to muscle fiber physiology and biochemistry, areall precisely interrelated. The overall design of the soleus(SOL) and medial gastrocnemius (MG) motor unit populations inthe cat hindlimb seems ideally suited to the functional rolesplayed by these contrasting muscles. As more information accumulatesabout these populations, and about others with different functionalroles, we should have increasingly clear ideas about the fundamentalquestion of why different muscles look and act as they do invarious animal species.     

Differences between properties of male and female motor units in the rat medial gastrocnemius muscle.

Differences between motor units in hindlimb locomotor muscles of male and female Wistar rats were studied. The contractile and action potential properties of various types of motor units as well as proportions of these units in the medial gastrocnemius muscle were analyzed. Experiments were based on functional isolation and electrical stimulation of axons of single motor units. Composition of motor units was different for male and female subjects, with higher number of the fast fatigable and lower number of slow type units in male animals. The contraction and the half-relaxation times were significantly longer in male motor units, what might be due to differences in muscle size. Slower contraction of male motor units likely corresponds to lower firing rates of their motoneurons. On the other hand, no significant differences between sexes were observed with respect to force parameters of motor units (the twitch and the maximum tetanus forces), except the fast resistant units (higher force values in male muscles). The mass of the muscle was approximately 1.5 time bigger in male rats. However, the mean ratio of motor unit tetanus force to the muscle mass was almost twice smaller in this group, what indirectly suggests that muscles of male rats are composed of higher number of motor units. Finally, female muscles appeared to have higher fatigue resistance as the effect of higher proportion of resistant units (slow and fast resistant) and higher values of the fatigue index in respective motor unit types. The motor unit action potentials in female rats had slightly lower amplitudes and shorter time parameters although this difference was significant only for fast resistant units.     

Orderly recruitment among motoneurons supplying different muscles.

Virtually all movements involve the recruitment of motor units from multiple muscles. Given the functional diversity of motor units (motoneurons and the muscle fibers they supply), the effective production of specific movements undoubtedly depends upon some principle(s) to organize the ensemble of active motor units. The principle acting to organize the recruitment of motor units within muscles is the size principle, whereby the first motor units to be recruited have the smallest values for axonal conduction velocity and contractile force, and are the slowest to contract and fatigue. Here we consider the possibility that the size principle applies in the recruitment of motor units across muscles, i.e., that regardless of their muscles of origin, active motor units are recruited in rank order, for example, from low to high conduction velocity. The benefits of orderly recruitment across muscles could be similar to the acknowledged advantages of orderly recruitment within muscles. One benefit is that the neural process involved in organizing active motor units would be simplified. In a muscle-based scheme, the size principle would organize only those motor units within individual muscles, leaving the nervous system with the additional task of coordinating the relative activities of motor units from different muscles. By contrast, in an ensemble-based scheme, orderly recruitment of all motor units according to the size principle would automatically coordinate motor units both within and across motor nuclei. Another potential benefit is the provision for movements with smooth trajectory, the result of interleaving the divergent torque contributions made by motor units from muscles that differ in their orientations about joints. Otherwise, if order were restricted within muscles, the torque trajectory of a joint would change unevenly as participating muscles begin contracting at different times and grade activity at different rates. These considerations support speculation that motor units recruited from co-contracting muscles are collectively recruited according to the size principle.     

Dynamic Neural Network Models of the Premotoneuronal Circuitry Controlling Wrist Movements in Primates

Dynamic recurrent neural networks were derived to simulate neuronal populations generating bidirectional wrist movements in the monkey. The models incorporate anatomical connections of cortical and rubral neurons, muscle afferents, segmental interneurons and motoneurons; they also incorporate the response profiles of four populations of neurons observed in behaving monkeys. The networks were derived by gradient descent algorithms to generate the eight characteristic patterns of motor unit activations observed during alternating flexion-extension wrist movements. The resulting model generated the appropriate input-output transforms and developed connection strengths resembling those in physiological pathways. We found that this network could be further trained to simulate additional tasks, such as experimentally observed reflex responses to limb perturbations that stretched or shortened the active muscles, and scaling of response amplitudes in proportion to inputs. In the final comprehensive network, motor units are driven by the combined activity of cortical, rubral, spinal and afferent units during step tracking and perturbations.The model displayed many emergent properties corresponding to physiological characteristics. The resulting neural network provides a working model of premotoneuronal circuitry and elucidates the neural mechanisms controlling motoneuron activity. It also predicts several features to be experimentally tested, for example the consequences of eliminating inhibitory connections in cortex and red nucleus. It also reveals that co-contraction can be achieved by simultaneous activation of the flexor and extensor circuits without invoking features specific to co-contraction.     

Peculiarities of structural-functional organization of the motor neuropil in the dragonfly thoracic ganglia

The study considers structural-functional relations in motor neuropil of the thoracic ganglia in dragonflies-insects capable of performing very complex and fast maneuvering in flight. The motor neuropil in dragonflies was shown to be more differentiated than in less mobile insects, while its motor nuclei are more outlined and approached to each other. There were revealed dendrites of the leg muscle motoneurons (intermediate nucleus), running to the anterior and posterior nuclei that contain dendrites of the wing muscle motoneurons. A possible role of such a dendrite approaching is discussed for close functional cooperation of wing and leg muscles essential for dragonflies to catch a large prey in flight by using their legs. Peculiarities of structural organization of the wing muscle motoneurons in dragonflies and locusts are considered to suggest the greater functional capabilities of motoneurons in the dragonfly motor apparatus.     

Transient inability of neonatal rat motoneurons to reinnervate muscle

We studied the reinnervation of internal intercostal muscles of newborn rats. The distal halves were denervated by nerve section at various ages between birth and 6 weeks. Regardless of the age at denervation, neither evoked nor spontaneous nerve-muscle transmission reappeared until the animals were at least 3 weeks old. Older rats recovered a substantial degree of function within 7 days of nerve section. Normally the motor units in this muscle are narrowly distributed, so most axotomized motoneurons lost their entire synaptic periphery. Reinnervation was by axons which had been sectioned, and regenerated motor units were of normal size and number. There was no collateral sprouting from end plates left intact. Motoneurons axotomized at birth did regenerate axons the full length of the muscle within 7 days of operation. Their failure to reinnervate the muscle was due to delay in forming functional end plates. Nerve section in animals aged 1 month or older resulted in an abnormal pattern of reinnervation; reinnervated motor units were diffusely spread through large portions of the muscle, although they still did not overlap with the region left intact. This indicates that thoracic motoneurons respond to axotomy differently in neonatal rats than they do in adults.     

Effect of the tendon reflex on the silent period of motor units in man

The behavior of motor units functioning under different conditions was investigated during the patellar reflex. The reflex was elicited during regular firing of the motor units in connection with weak sustained voluntary effort without postural change. Under these conditions the firing rate of the motor units serves as a statistical characteristic of threshold: during the maintenance of an assigned level of contraction the mean firing rate of the low-threshold motor units was higher. The greater the mean spontaneous interspike interval of the motor units, the longer the duration of their silent period after reflex muscular contraction. The duration of the silent period of single motor units in many cases exceeded the longest duration of the aggregated silent period on the electromyogram. The instant frequency (the difference between the reciprocals of the mean interspike interval and silent period) was used as a measure of inhibitory action on the motoneuron. Positive correlation was observed between the change in the instant frequency and the spontaneous firing rate of the motor units. Within the population examined, those motoneurons whose frequency was higher (low-threshold) were more inhibited. The combination of spinal factors evoking inhibition of the motoneurons after the tendon reflex and the excitatory supraspinal influences causing recruiting of the motoneurons during voluntary contraction proved more effective under the conditions investigated for the same motoneurons.     

Invited review: Mechanisms underlying motor unit plasticity in the respiratory system.

Neuromotor control of skeletal muscles, including respiratory muscles, is ultimately dependent on the function of the motor unit (comprising an individual motoneuron and the muscle fibers it innervates). Considerable diversity exists across diaphragm motor units, yet remarkable homogeneity is present (and maintained) within motor units. In recent years, the mechanisms underlying the development and adaptability of respiratory motor units have received great attention, leading to significant advances in our understanding of diaphragm motor unit plasticity. For example, following imposed inactivity of the diaphragm muscle, there are changes at phrenic motoneurons, neuromuscular junctions, and muscle fibers that tend to restore the ability of the diaphragm to sustain ventilation. The role of activity, neurotrophins, and other growth factors in modulating this adaptability is discussed.     

Functional properties of interneurons of the masticatory reflex

Interneurons of the supratrigeminal nucleus, transmitting effects from the sensory and motor branches of the trigeminal nerve to motoneurons of the muscles of mastication were investigated. Two groups of interneurons with different functional connections were found. The first group (A) contains neurons excited during stimulation of the sensory branches and the motor nerve to the digastric muscle (A₁), neurons excited during stimulation of sensory branches and high-threshold afferents of the motor nerve to the masseter muscle (A₂), and neurons excited only by low-threshold afferents of the motor nerve to the masseter muscle (A₃). Neurons of the second group (B) were activated only by sensory fibers of the trigeminal nerve. It is postulated that interneurons of group A transmit inhibitory effects to motoneurons of antagonist muscles of the lower jaw. Group B interneurons participate in the transmission of excitatory influences to motoneurons of the digastric muscle.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 4, No. 2, pp. 150–157, March–April, 1972.     

Cortico-pyramidal and cortico-extrapyramidal synaptic influences on lumbar motoneurons in monkeys

Postsynaptic potentials evoked by stimulation of the motor cortex or pyramids before and after acute pyramidotomy were investigated in the lumbar motoneurons of monkeys. In response to activation of fibers of the pyramidal tract monosynaptic EPSPs predominated in motoneurons innervating the distal muscles of the hind limbs. Monosynaptic EPSPs in the motoneurons of the distal muscles had a significantly higher amplitude and could be evoked by weaker stimuli than EPSPs in the motoneurons of the proximal muscles. Cortico-motoneuronal EPSPs in the motoneurons of the distal muscles had a less marked frequency potentiation than EPSPs with monosynaptic segmental delay in the motoneurons of the proximal muscles. Cortico-extrapyramidal synaptic responses appeared in the pyramidotomized monkeys during intensive repetitive stimulation of the motor cortex in motoneurons of both distal and proximal muscles. These effects, transmitted by descending projections of the brain stem, may be responsible for the partial preservation of cortical motor control after pyramidotomy.I. M. Sechenov Institute of Evolutionary Physiology and Biochemistry, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 4, No. 6, pp. 587–596, November–December, 1972.     

Independent development of sensory and motor innervation patterns in embryonic chick hindlimbs

Previous studies suggest that sensory axon outgrowth is guided by motoneurons, which are specified to innervate particular target muscles. Here we present evidence that questions this conclusion. We have used a new approach to assess the pathfinding abilities of bona fide sensory neurons, first by eliminating motoneurons after neural crest cells have coalesced into dorsal root ganglia (DRG) and second by challenging sensory neurons to innervate muscles in a novel environment created by shifting a limb bud rostrally. The resulting sensory innervation patterns mapped with the lipophilic dyes DiI and DiA showed that sensory axons projected robustly to muscles in the absence of motoneurons, if motoneurons were eliminated after DRG formation. Moreover, sensory neurons projected appropriately to their usual target muscles under these conditions. In contrast, following limb shifts, muscle sensory innervation was often derived from inappropriate segments. In this novel environment, sensory neurons tended to make more "mistakes" than motoneurons. Whereas motoneurons tended to innervate their embryologically correct muscles, sensory innervation was more widespread and was generally from more rostral segments than normal. Similar results were obtained when motoneurons were eliminated in embryos with limb shifts. These findings show that sensory neurons are capable of navigating through their usual terrain without guidance from motor axons. However, unlike motor axons, sensory axons do not appear to actively seek out appropriate target muscles when confronted with a novel terrain. These findings suggest that sensory neuron identity with regard to pathway and target choice may be unspecified or quite plastic at the time of initial axon outgrowth.