Mono-synaptic reflex responses of individual motoneurons

Individual motoneuron responses to a variety of afferent inputs have been examined. At a given input some motoneurons respond to every trial, some to no trial, and some respond to a certain percentage of trials that is characteristic for the motoneuron at that input. The performance of a motoneuron is expressed by means of a firing index that relates the number of responses to the number of trials. In a representative assemblage of individual motoneurons some 20 to 30 per cent display intermediate firing indices. This number, comprising an "intermediate zone" remains fairly constant at different levels of input although the individuals within it may be entirely different at two different levels of input. Frequency distribution of individuals with respect to firing indices is U-shaped. Intermediacy of firing indices depends upon temporal fluctuation of excitability which, in the first approximation, is normal. The individual motoneurons are approximately equally frequently distributed with respect to transmitter potentiality of their monosynaptic reflex afferent connections. The distribution of motoneurons with respect to transmitter potentiality of their monosynaptic reflex connections is considered representative of a natural pool in that the sum of their individual post-tetanic response behaviors accurately reproduces the course of post-tetanic potentiation in a natural pool.     

Reduction of the muscle activity associated with self-imposed electrical stimulation of mixed nerves supplying lower limb muscles in man.

Similarly to brief hammer taps self-imposed on the limb segments, self-triggered electrical stimulation delivered to the tibial, femoral or peroneal nerves are associated with anticipatory reduction in the muscle activity (RMA) of the target leg muscles. The anticipatory RMA starts shortly before the expected perturbation and lasts until the onset of the impact. The purpose of the present work is to study to what extent the selective activation of the different homonymous and heteronymous afferents could modify the central programs and the associated time and space distribution of the anticipatory RMA pattern in the target leg muscles. Our results show that the anticipatory RMA pattern is a result mainly of a pre-programmed non-specific central command, rather than consequence of the specific composition of the afferent volleys originating from different homonymous and heteronymous nerves. The commands for the voluntary movement triggering the stimulation and the associated anticipatory RMA are closely linked but independently controlled. By their synchronisation and co-ordination the central nervous system accounts the differences in length of the particular motor pathways. It is suggested, that in contrast to the classic anticipatory postural adjustments, the anticipatory RMA is presumably an alternative mode of feed-forward control diminishing the undesired effects of the afferent inputs.     

Monosynaptic reflex response of spinal motoneurons to graded afferent stimulation

Monosynaptic reflex response of spinal motoneurons to graded afferent volleys has been studied in natural populations and in a representative sample of individual motoneurons. By analysis of input-response relations certain of the requirements for initiation of reflex discharge have been defined. Initation of motoneuron discharge by monosynaptic afferent excitatory volleys results from the development of transmitter potentiality among members of a pool. Transmitter potentiality is considered to have the following characteristics: 1. It is a function of the number of active excitatory synaptic knobs, the degree to which such knobs are aggregated on the motoneuron soma, and the intensity of action per knob. 2. It has an appreciable spatial decrement and rapid temporal decay. 3. While transmitter potentiality has considerable dependence on number of active excitatory knobs, proximity of such knobs is an important variable. Total activation of a discrete zone does not appear to be necessary for initiation of discharge. In addition to initiation of discharge, volleys in monosynaptic afferent excitatory fibers facilitate response otherwise engendered. Such facilitation depends upon the production of an increment in transmitter potentiality. Facilitator potentiality has the following characteristics: 1. It depends principally on number of active excitatory synaptic knobs and intensity of action per knob. 2. Facilitatory action may result from synchronous activity in knobs interspersed among aggregations of knobs otherwise activated, thus fulfilling spatial requirements for transmitter potentiality. Alternatively a residual facilitation may result from a generalized action. 3. Residual facilitation has a slow temporal decay in comparison with transmitter potentiality.     

Modulation of the presynaptic inhibition of spinal α-motoneurons during mechanical stimulation of different types

Using the method of assessing the presynaptic inhibition of heteronymous Ia afferents and α motoneurons of the m. soleus during a homonymous vibration effect on the tendo calcaneus in ten subjects, changes in the inhibition of spinal α motoneurons during 15 min of the aftereffect of mechanical stimulation of different types were studied. Intense mechanical stimuli and weak tactile, vibratory stimuli applied in combination intensify inhibitory processes in the afferent fibers of group Ia, their effects differing in the value of the increase in the presynaptic inhibition of spinal α motoneurons.     

Peripheral specification of Ia synaptic input to motoneurons innervating foreign target muscles

Muscle sensory neurons, called Ia afferents, make monosynaptic connections with functionally related sets of motoneurons in the spinal cord. Previous work has suggested that peripheral target muscles play a major role in determining the central connections of Ia afferents with motoneurons. Here, we ask whether motoneurons can also be influenced by their target muscles in terms of the monosynaptic input they receive from Ia afferents, by transplanting thoracic motoneurons into the lumbosacral spinal cord so that they innervate foreign muscles. Three or four segments of thoracic neural tube from stage 14-15 chicken embryos were transplanted to the lumbosacral region of stage 16-17 embryos, and electrophysiological recordings were made from transplanted motoneurons after the embryos had reached stage 38-40. Transplanted thoracic motoneurons innervated limb muscles and received monosynaptic inputs from Ia afferents. These connections were not random: Most of the connections were formed between Ia afferents and motoneurons projecting to the same muscle (homonymous connections). Few aberrant connections were found although the anatomical distribution of afferents in the transplant indicated that they had ample opportunity to contact inappropriate motoneurons. We conclude that although peripheral target cues are not sufficient to respecify an already committed motoneuron (turn a thoracic motoneuron into a lumbosacral motoneuron), they do provide sufficient information for Ia afferent input to be functionally correct.     

Transmission in fractionated monosynaptic spinal reflex systems

A study has been made of conditions that support monosynaptic reflex transmission from afferent fibers of one part of a synergic muscle mass to motoneurons of another part. Heteronymous response so called can be brought on by prior tetanization of the afferent pathway and by asphyxiation to a critical stage. The response is facilitated by cooling and may appear in the cold preparation without need for prior tetanization. By appropriate asymmetrical subdivision of a monosynaptic reflex system an afferent inflow can be obtained that is sufficiently powerful to secure heteronymous transmission without the need for prior tetanization or cooling. Each junction between a monosynaptic afferent fiber and a motoneuron possesses some degree of potentiality for transmitting. Transmitter potentiality of an afferent fiber at its several junctions with motoneurons varies widely. Reasons are advanced for supposing the variation to be graded rather than stepwise, and quantitative rather than qualitative.     

Early post-tetanic potentiation and low frequency depression of some group I reflex actions

Group I reflex functions, namely monosynaptic reflex transmission, facilitation of synergists, and direct and disynaptic inhibition, show early post-tetanic potentiation following conditioning with a brief, high frequency, tetanus. Of these reflex functions, monosynaptic transmission always shows low frequency depression. Direct inhibitory pathways, and therefore inhibitory junctions, are insensitive to low frequency depression. The fact that direct inhibition can be potentiated shows it to be sufficiently labile that a decrease in efficacy at inhibitory junctions during repetitive activity should be revealed. Disynaptic inhibition often shows low frequency depression. As it is likely that inhibitory junctions in the direct and disynaptic pathways are similar, the low frequency depression of disynaptic inhibition is probably due to the properties of the excitatory relay between afferent fibers and interneurons in that pathway. Facilitation between synergists is often more depressed when the conditioning and testing volleys are nearly simultaneous than when they are separated by 1 to 1.5 msec. This result indicates that an early and rapid phase of action, responsible for homonymous and heteronymous transmission, is more sensitive to low frequency depression than is residual facilitation. In general, reflex transmission is more sensitive than are other aspects of action by group I fibers to events concurrent with and following repetitive activation.     

Responses of motoneurons undergoing chromatolysis

The delayed and asynchronous firing of chromatolytic motoneurons in response to group I afferent volleys is shown to be evoked monosynaptically, there being an abnormally long and variable delay between onset of monosynaptic action and generation of impulse discharge. Intensity of monosynaptic excitatory action is reduced, and considerable variability in the form of successively evoked postsynaptic potentials is often observed. No evidence has been found for the development of excitatory group I polysynaptic pathways. Reduction in responsiveness of finer dendrites is indicated by the feeble "d" response evoked by an antidromic volley in a chromatolytic motor nucleus. Antidromic impulses appear to invade the cell bodies and coarse dendrites, but die out at points short of the normal extent of dendritic invasion. Vigorous firing of Renshaw cells can be elicited by antidromic volleys. Chromatolytic motoneurons appear to maintain reasonably normal resting membrane potentials, but are more susceptible to damage than are normal cells. Action potentials are large and usually overshoot the resting potential level. Post spike potentials are similar to those of normal cells except for a less prominent, or absent, early phase of depolarisation. In contrast with the reduced responsiveness of peripheral dendrites, there is a lowered threshold for antidromic and segmental reflex synaptic activation of the more central regions, probably the cell bodies and nearby coarse dendrites, of motoneurons undergoing chromatolysis.     

Response of Renshaw cells to sinusoidal stretch of hindlimb extensor muscles.

1. Renshaw cells responding disynaptically to electrically induced group I volleys in the intact gastrocnemius-soleus (GS) nerve, were submitted to small-amplitude, high-frequency vibration applied longitudinally to the deefferented GS muscle in precollicular decerebrate cats. 2. Vibration of the GS muscle at 200/sec, 180 mu peak-to-peak amplitude for 80-100 msec produced a sudden increase in the discharge rate of Renshaw cells, which gradually decreased within 25-50 msec to reach a steady level higher than that recorded in the absence of vibration. 3. Excitation of Renshaw cells appeared at a threshold amplitude of vibration (at 200-250/sec) of 5-20 mu and increased to a maximum value for amplitudes of about 70-80 mu, i.e., when all the primary endings of the spindles from the GS muscle had been driven by the stimulus. Recruitment of the secondary endings of the muscle spindles, due to large amplitude muscle vibration, did not modify the response of the Renshaw cells to the mechanically induced group Ia volleys. 4. These findings were obtained with the GS muscle pulled at 8 mm of initial extension. A threshold response of Renshaw cells to vibration appeared at 4 mm of static stretch, while maximal responses occurred at 8 mm. No further increase and actually a slight decrease in the response appeared for initial extensions of the muscle of 10-12 mm. 5. For a given vibration amplitude, the response of the Renshaw cells increased with increasing frequencies of vibration to reach the maximum at frequencies of 150-250/sec. Bursts of Renshaw cell discharges synchronous to each stroke of vibrator occurred only for low frequencies of stimulation (less than 25/sec). 6. It is concluded that vibration of the GS muscle represents a very effective method in exciting the Renshaw cells and that this response depends upon selective stimulation of homonymous motoneurons monosynaptically excited by the orthodromic volleys originating from the primary endings of the corresponding muscle spindles.     

Sex differences in rabbit masseter motoneuron firing behavior

To evaluate whether sex differences in the proportions of fibers of different phenotypes in the masseter muscle might be the result of differences in the behavior of their motoneurons, we studied the firing patterns of masseter motoneurons in adult male and female rabbits. Activity in individual motoneurons was determined from high spatial resolution EMG recordings made during cortically evoked rhythmic activation of the masticatory muscles. Although some motoneurons could be said to fire according to slow-tonic or fast-phasic patterns, most did not. In both sexes a substantial range of median firing rates and median firing durations was found. In adult males, masseter motoneurons fired more rapidly than those recorded from adult females. No significant sex differences in motoneuron firing duration were found. These results are consistent with the hypothesis that androgen-induced differences in rabbit masseter muscle fiber phenotype are a reflection of differences in motoneuron firing rate. Whether this effect of androgen is directly upon the motoneurons or is the result of a response of muscle fibers to androgen remains to be investigated.     

Spike propagation synchronized by temporally asymmetric Hebbian learning

 Synchronously spiking neurons have been observed in the cerebral cortex and the hippocampus. In computer models, synchronous spike volleys may be propagated across appropriately connected neuron populations. However, it is unclear how the appropriate synaptic connectivity is set up during development and maintained during adult learning. We performed computer simulations to investigate the influence of temporally asymmetric Hebbian synaptic plasticity on the propagation of spike volleys. In addition to feedforward connections, recurrent connections were included between and within neuron populations and spike transmission delays varied due to axonal, synaptic and dendritic transmission. We found that repeated presentations of input volleys decreased the synaptic conductances of intragroup and feedback connections while synaptic conductances of feedforward connections with short delays became stronger than those of connections with longer delays. These adaptations led to the synchronization of spike volleys as they propagated across neuron populations. The findings suggests that temporally asymmetric Hebbian learning may enhance synchronized spiking within small populations of neurons in cortical and hippocampal areas and familiar stimuli may produce synchronized spike volleys that are rapidly propagated across neural tissue. Received: 28 May 2002 / Accepted: 3 June 2002 RID="*" ID="*" Correspondence to: R. E. Suri Intelligent Optical Systems (IOS), 2520 W 237th St, Torrance, CA 90505-5217, USA (e-mail: rsuri@intopsys.com, Tel.: +1-310-5307130 ext. 108, Fax: +1-210-5307417)     

Synaptic processes in thoracic α-motoneurons evoked by segmental afferent stimulation

Synaptic processes in various functional groups of thoracic motoneurons (Th₉-Th₁₁) evoked by stimulation of segmental nerves were investigated in anesthetized and decerebrate cats. No reciprocal relations were found between these groups of motoneurons. Only excitatory mono- and polysynaptic responses were recorded in the motoneurons of the principal intercostal nerve following stimulation of the homonymous nerve. Activation of the afferents of the external intercostal muscle and dorsal branches does not cause noticeable synaptic processes in these motoneurons; much more rarely it is accompanied by the development of low-amplitude polysynaptic EPSP's. In motoneurons of the dorsal branches, stimulation of homonymous nerves leads to the appearance of simple, short-latent EPSP's. Late responses of the IPSP or EPSP - IPSP type with a predominance of the inhibitory component were observed in most motoneurons of this type following activation of the afferent fibers of the principal intercostal nerve. In other motoneurons of the dorsal muscles, stimulation of the main intercostal nerve (and nerve of the external intercostal muscle) did not evoke apparent synpatic processes. EPSP's (mono- and polysynaptic) appeared in the motoneurons of the external intercostal muscle following stimulation of the homonymous and main intercostal nerves. Activation of the afferents of the dorsal branches was ineffective. The character of the synaptic responses of the respiratory motoneurons to segmental afferent stimulation, investigated under conditions of spontaneous respiration, was different. The characteristics of synaptic activation of thoracic motoneurons by segmental afferents under conditions of hyperventilation apnea and during spontaneous breathing of the animals are discussed.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 2, No. 3, pp. 279–288, May–June, 1970.     

Measurement and nature of firing rate adaptation in turtle spinal neurons

There is sparse literature on the profile of action potential firing rate (spike-frequency) adaptation of vertebrate spinal motoneurons, with most of the work undertaken on cells of the adult cat and young rat. Here, we provide such information on adult turtle motoneurons and spinal ventral-horn interneurons. We compared adaptation in response to intracellular injection of 30-s, constant-current stimuli into high-threshold versus low-threshold motoneurons and spontaneously firing versus non-spontaneously-firing interneurons. The latter were shown to possess some adaptive properties that differed from those of motoneurons, including a delayed initial adaptation and more predominant reversal of adaptation attributable to plateau potentials. Issues were raised concerning the interpretation of changes in the action potentials afterhyperpolarization shape parameters throughout spike-frequency adaptation. No important differences were demonstrated in the adaptation of the two motoneuron and two interneuron groups. Each of these groups, however, was modeled by its own unique combination of action potential shape parameters for the simulation of its 30-s duration of spike-frequency adaptation. Also, for a small sample of the very highest-threshold versus lowest-threshold motoneurons, the former group had significantly more adaptation than the latter. This finding was like that shown previously for cat motoneurons supplying fast- versus slow twitch motor units.     

Potentials of spinal motoneurons in cats with experimental tetanus

Potentials of motoneurons of the lower segments of the spinal cord were recorded with the aid of intracellular microelectrodes in experiments on cats with induced tetanus produced by injection of tetanus toxin (1500–2000 mouse LD₅₀) into the extensor muscles of the left shin. Neither afferent volleys of impulses in cutaneous and muscle nerves, nor antidromic volleys in the corresponding ventral roots, produced IPSPs in motoneurons of the extremity into which toxin was injected. The form both of antidromic peak potentials and of monosynaptic EPSPs in motoneurons in which IPSPs were blocked by tetanus toxin did not differ from the form of corresponding potentials of motoneurons in normal cats. The values of threshold depolarization for peak discharges during synaptic and direct stimulation were equal in tetanus and control motoneurons. Resistance and time constant values of the membrane in "tetanus" motoneurons did not differ from the corresponding values for "control" motoneurons.N. I. Pirogov Second Medical Institute, Moscow. Translated from Neirofiziologiya, Vol. 1, No. 1, pp. 25–34, July–August, 1969.     

Spinal reflexes in the long-tailed stingray, Himantura fai

We have exploited the segregation of motor and sensory axons into peripheral nerve sub-compartments to examine spinal reflex interactions in anaesthetized stingrays. Single, supra-maximal electrical stimuli delivered to segmental sensory nerves elicited compound action potentials in the motor nerves of the stimulated segment and in rostral and caudal segmental motor nerves. Compound action potentials elicited in segmental motor nerves by single stimuli delivered to sensory nerves were increased severalfold by prior stimulation of adjacent sensory nerves. This facilitation of the segmental reflex produced by intense conditioning stimuli decreased as it was applied to more remote segments, to approximately the same degree in up to seven segments in the rostral and caudal direction. In contrast, an asymmetric response was revealed when test and conditioning stimuli were delivered to different nerves, neither of which was of the same segment as the recorded motor nerve: in this configuration, conditioning volleys generally inhibited the responses of motoneurons to stimuli delivered to more caudally located sensory nerves. This suggests that circuitry subserving trans-segmental interactions between spinal afferents is present in stingrays and that interneuronal connections attenuate the influence that subsequent activity in caudal primary afferents can have on the motor elements.     

Active zones and receptor surfaces of freeze-fractured crayfish phasic and tonic motor synapses

Deep and superficial flexor muscles in the crayfish abdomen are innervated respectively by small populations of physiologically distinct phasic and tonic motoneurons. Phasic motoneurons typically produce large EPSP's, releasing 100 to 1000 times more transmitter per synapse than their tonic counterparts, and exhibiting more rapid synaptic depression with maintained stimulation. Freeze-fracturing the abdominal flexor muscles yielded images of phasic and tonic synapse-bearing terminals. The two types of synapse are qualitatively similar in ultrastructure, displaying on the presynaptic membrane's P-face synaptic contacts recognized by relatively particle-free oval plaques which are often framed by the muscle fiber's E-face leaflet with its associated receptor particles. Situated within these presynaptic plaques are discrete clusters of large intramembrane particles, forming active zone (AZ) sites specialized for transmitter release. AZs of phasic and tonic synapses are similar: 80% had a range of 15–40 large particles distributed in either paired spherical clusters or in linear form, with a few depressions denoting sites of synaptic vesicle fusion or retrieval around their perimeters. The packing density of particles is similar for phasic and tonic AZs. The E-face of the muscle membrane displays oval-shaped receptor-containing sites made up of tightly packed intramembranous particles. Phasic and tonic receptor particles are packed at similar densities and the measured values resemble those of several other crustacean and insect neuromuscular junctions. Overall, the similarity between phasic and tonic synapses in the packing density of particles at their presynaptic AZs and postsynaptic receptor surfaces suggests similar regulatory mechanisms for channel insertion and spacing. Furthermore, the findings suggest that morphological differences in active zones or receptor surfaces cannot account for large differences in transmitter release per synapse.     

Presynaptic Frequency- and Pattern-Dependent Filtering

Dual intracellular recordings from pairs of synaptically connected neurones have demonstrated that the frequency-dependent pattern of transmitter release varies dramatically between different classes of connections. Somewhat surprisingly, these patterns are not determined by the class of neurone supplying the axon alone, but to a large degree by the class of postsynaptic neurone. A wide range of presynaptic mechanisms, some that depress the release of transmitter and others that enhance release have been identified. It is the selective expression of these different mechanisms that determines the unique frequency- and pattern-dependent properties of each class of connection. Although the molecular interactions underlying these several mechanisms have yet to be fully identified, the wealth and complexity of the protein-protein and protein-lipid interactions that have been shown to control the release of transmitter suggest many ways in which the properties of a synapse may be tuned to respond to particular patterns and frequencies.     

Mechanisms of Accommodation in Different Types of Frog Neurons

Responses of individual spinal ganglion neurons, sympathetic ganglion neurons, and motoneurons of frogs to linearly rising currents were investigated utilizing microelectrodes for intracellular stimulation and recording. Spinal ganglion neurons exhibited rapid accommodation to linearly rising currents. Minimal current gradients (MCG's) required to excite these neurons (average value, 106 rheobases/sec) were of the same order of magnitude as for some nerve fibers. Although sympathetic ganglion neurons exhibited responses to lower current gradients than spinal ganglion neurons, distinct MCG's (average value, 26 rheobases/sec) could always be established. MCG's could not be detected in most motoneurons, even with current gradients as low as 0.6 rheobase/sec. A few motoneurons exhibited distinct MCG's (average value, 11 rheobases/sec). The failure of spinal ganglion neurons to respond to anything other than rapidly rising currents appears to be due primarily to the development of severe delayed rectification. The inability of sympathetic ganglion neurons to respond to low current gradients appears to depend not only on delayed rectification but also on increases in depolarization threshold. When present in motoneurons, accommodation appears to result from the same mechanisms responsible for its appearance in sympathetic ganglion neurons.     

Choline analogues: their use in studies of acetylcholine synthesis, storage, and release

The objective of this article is to illustrate how choline analogues might provide insight into mechanisms that regulate the synthesis, storage, and release of acetylcholine (ACh). Studies with false neurotransmitters provide information about the origin of releasable transmitter. Thus, false esters that distribute like ACh to vesicle-bound stores are as releasable as is ACh, but esters that poorly localize to synaptic vesicles are poorly releasable. Studies of choline analogue uptake provide information about the structural specificity of that transport process and, also, show that choline uptake is regulated in response to activity. Thus, stimuli that normally release transmitter increase the rate of choline transport, presumably to provide more precursor for ACh synthesis. However, the relationship between precursor delivery and product formed can be dissociated, suggesting that some factor in addition to choline delivery is involved in ACh synthesis regulation. Studies with a compound (AH5183), which inhibits ACh uptake by synaptic vesicles, provide information about the relationship of ACh stores and releasable transmitter. In the presence of AH5183 some 15% of nerve terminal ACh is released in response to nerve impulses, suggesting the existence of a small population of vesicles that contain readily releasable ACh. In presence of AH5183, ACh synthesis is activated even when ACh release is depressed, showing that transmitter synthesis can be regulated by some factor other than nerve terminal ACh levels.