Monosynaptic reflex response of individual motoneurons as a function of frequency

An assemblage of individual motoneurons constituting a synthetic motoneuron pool has been studied from the standpoint of relating monosynaptic reflex responses to frequency of afferent stimulation. Intensity of low frequency depression is not a simple function of transmitter potentiality. As frequency of stimulation increases from 3 per minute to 10 per second, low frequency depression increases in magnitude. Between 10 and approximately 60 per second low frequency depression apparently diminishes and subnormality becomes a factor in causing depression. At frequencies above 60 per second temporal summation occurs, but subnormality limits the degree of response attainable by summation. At low stimulation frequencies rhythm is determined by stimulation frequency. Interruptions of rhythmic firing depend solely upon temporal fluctuation of excitability. At high frequency of stimulation rhythm is determined by subnormality rather than inherent rhythmicity, and excitability fluctuation leads to instability of response rhythm. In short, whatever the stimulation frequency, random excitability fluctuation is the factor disrupting rhythmic response. Monosynaptic reflex response latency is stable during high frequency stimulation as it is in low frequency stimulation provided a significant extrinsic source of random bombardment is not present. In the presence of powerful random bombardment discharge may become random with respect to monosynaptic afferent excitation provided the latter is feeble. When this occurs it does so equally at low frequency and high frequency. Thus temporal summation is not a necessary factor. There is, then, no remaining evidence to suggest that the agency for temporal summation in the monosynaptic system becomes a transmitting agency in its own right.     

Reflex depression in rhythmically active monosynaptic reflex pathways

A study has been made of the depression that occurs when a monosynaptic reflex pathway is subjected to repetitive stimulation. Reflex depression has a dual origin. High frequency or early depression is postsynaptic in origin and results from subnormality in the motoneurons. Low frequency, late, or enduring depression is presynaptic in origin. The conditioning volley-test volley technique and the frequency-mean monosynaptic reflex amplitude relation yield similar information concerning reflex depression. Each method has its advantages and for some purposes one or the other of the methods necessarily must be employed. The results of a variety of experiments are consistent with the proposition that reflex depression in the monosynaptic reflex pathway originates by action in the group IA afferent fibers of muscle origin that are responsible for monosynaptic reflex transmission. Depression is present at a frequency of 0.1 per second (6 per minute) and absent at a frequency of 0.05 per second (3 per minute). Thus it is impractical for most purposes to employ repetition rates that satisfy the requirement for designation as "single shock" stimulations. The temporal course of enduring depression has been determined. It is identical with that for a number of other phenomena observable in monosynaptic reflex pathways, which suggests a common origin. The mechanism of low frequency or enduring depression is discussed in the light of this suggestion.     

Post-tetanic potentiation of response in monosynaptic reflex pathways of the spinal cord

Following tetanic afferent stimulation of a monosynaptic reflex pathway, the transmission through that pathway of isolated reflex volleys is enhanced for some minutes. Post-tetanic potentiation is comparable in the monosynaptic reflex arcs of flexor and extensor muscles. The facilitator and inhibitor actions of monosynaptic reflex afferent fibers, as well as the transmitter action, are potentiated following tetanization. Little post-tetanic change attends reflex transmission through plurisynaptic reflex arcs. Various tests for excitability change made independently of the tetanized afferent fibers reveal none or a slight depression. Hence the potentiating influence of a tetanus is limited to subsequent action on the part of the recently tetanized fibers themselves. Increase in the size of the individual impulses comprising an afferent volley such as might occur during positive after-potential, would accommodate the requirement for a limited process and provide for increased synaptic action. The proposed association between post-tetanic potentiation and positive after-potential (i.e. hyperpolarization) is supported by the following lines of evidence:- 1. Changes in intensity and duration of potentiation with change in frequency and duration of tetanic stimulation are characteristic of, and parallel to, the changes of positive after-potential in similar circumstances. 2. Afferent impulses are increased following a tetanus, and in a fashion that parallels the course of monosynaptic reflex potentiation. Post-tetanic potentiation, as here described, and after-discharge, whatever may be its mechanism, are unrelated phenomena.     

Functional organization in the terminal segments of the spinal cord with a consideration of central excitatory and inhibitory latencies in monosynaptic reflex systems

Prominent monosynaptic and disynaptic reflex discharges characterize ipsilateral reflex transmission in the third sacral segment. Convergence upon the motoneurons from the two sides of the body is inhibitory, that through disynaptic paths excitatory. The relative latencies of excitation and inhibition of reflex responses, of excitatory and inhibitory synaptic potentials, and of various aspects of impulse discharge in motoneurons are considered. It is concluded: (1) that a direct (i.e. monosynaptic) action of primary afferent collaterals upon motoneurons is responsible for inhibition of monosynaptic reflex discharge of antagonist motoneurons within a myotatic unit; (2) that the inhibitory postsynaptic potential as described is not the primary agency for monosynaptic reflex inhibition of monosynaptic reflex discharge; (3) that, however, a common causal agent may be responsible for inhibition of reflex discharge and for generation of an inhibitory postsynaptic potential; and (4) that the inhibitory post-synaptic potential may be linked with, or be the agent for, inhibition of soma response.     

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.     

Electrophysiological and psychophysical quantification of temporal summation in the human nociceptive system

Animal experiments have shown that the nociceptive reflex can be used as an indicator of central temporal integration in the nociceptive system. The aim of the present study on humans was to investigate whether the nociceptive reflex, evoked by repetitive strong electrical sural nerve stimuli, increased when summation was reported by the volunteers. The reflexes were recorded from the biceps femoris and rectus femoris muscles in eight volunteers following a series of stimulations at 0.1, 1, 2, and 3 Hz. Each series consisted of five consecutive stimuli. Using 0.1- and 1-Hz stimulation, the reflex was not facilitated in the course of the five consecutive stimuli. Following 2- and 3-Hz stimulation, the reflex size (root mean square amplitude) increased significantly during the course of the fifth stimulus. This reflex facilitation was followed by a significant increase (summation) in the pain magnitude when compared with 1- and 0.1-Hz stimulation. Furthermore, the threshold for psychophysical summation could be determined. This threshold (stimulus intensity) decreased when the stimulus frequency (1–5 Hz) of the five consecutive stimuli was increased. The nociceptive reflex and the psychophysical summation threshold might be used to clarify and quantify aspects of temporal summation within the human nociceptive system.     

Temporal integration of pungency

Four experiments explored possible temporal summation in olfactionand the common chemical sense. In one experiment, participantsjudged the perceived magnitude of various concentrations anddurations (1.25–3.75 s) of the pungent odorant ammoniaand the nonpungent odorant isoamyl butyrate. The perceived magnitudeof ammonia increased during an inhalation whereas the magnitudeof isoamyl butyrate did not. Time-intensity trading relationsfor ammonia indicated nearly perfect temporal summation. Inanother experiment, modulation of the concentration of ammoniaduring an inhalation led to assessments of perceived magnitudethat confirmed the high degree of temporal summation seen inthe first experiment. That is, approximately equal time-integratedmass of inhaled ammonia led to approximately equal perceivedintensity. A third experiment indicated that temporal summationfor ammonia arose from its pungency rather than from its odor,a fourth that trigeminally-mediated reflex apnea in responseto ammonia also exhibits temporal summation. The degree of temporalsummation measured with the reflex came very close to that assessedpsychophysically. When stimulated with ammonia, the common chemicalsense behaves more like a totalmass detector than a concentrationdetector. The investigation raises the possibility that theshortterm sensory reaction to most pungent stimuli may followthis simple rule.     

Action of meprobamate on spinal monosynaptic reflexes and on inhibitory pathways

Meprobamate was administered intravenously to spinal cats, in cumulative doses of 30 to 40 mg./kg. each. Initial doses may have a variable action on monosynaptic reflexes. At times some reflexes are depressed, while others are enhanced or unaffected. When dose levels of 100 mg./kg. or higher are reached, monosynaptic reflexes, both flexor and extensor, are depressed. Monosynaptic reflexes can be strongly depressed by meprobamate, their input-output relations often remaining unchanged. In such cases there is thus no change in the spatial summation requirements of those motoneurons remaining in the excitable zone. Inhibitory pathways, both direct and disynaptic, are highly resistant to the action of meprobamate. The drug does not distinguish between the direct and disynaptic pathways. It is suggested that meprobamate acts as a general depressant of excitatory synaptic transmission.     

Connections between descending visual interneurons and metathoracic motoneurons in the locust

Summary Connections between the four DMD neurons and metathoracic motoneurons in the locustSchistocerca were examined by recording extracellularly from the interneurons in the pro-mesothoracic connectives and intracellularly from seventeen motoneurons. A DIMD or DCMD spike causes an EPSP in the fast extensor tibiae motoneuron, which can be modified by changing the membrane potential. The EPSP always follows spikes at frequencies up to 200 Hz and with a latency of 0.9 ms, suggesting that the connections are monosynaptic and chemically mediated. EPSPs from the DIMD or DCMD arrive at the same time, their axons having the same conduction velocity, and appear simultaneously in the fast extensor tibiae motoneurons on both sides of the ganglion. There is spatial and temporal summation between the inputs but on no occasion did the motoneurons spike. Three inhibitory neurons are depolarized by DMD inputs and may on occasion spike, but it is not known whether these connections are direct. Similarly the slow excitatory motoneuron to the anterior coxal adductor muscle is hyperpolarized by DMD input. Other leg, flight or ventilatory motoneurons examined received no inputs from the DMD neurons. The connections shown are consistent with the hypothesis that the DMD neurons are in some way involved with initiation of a jump, but to achieve this must act synergistically with other inputs. This work was supported in part by USPHS grant No. NS 09404-03 to C.H.F.R. Dr. Rowell wishes to thank Dr. J. Phillipson for the use of facilities in the Oxford Department of Zoology during sabbatical leave.     

Mechanisms for spatial integration in visual detection: a model based on lateral interactions

Recent studies of visual detection show a configuration dependent weak improvement of thresholds with the number of targets, which corresponds to a fourth-root power law. We find this result to be inconsistent with probability summation models, and account for it by a model of 'physiological' integration that is based on excitatory lateral interactions in the visual cortex. The model explains several phenomena which are confirmed by the experimental data, such as the absence of spatial and temporal uncertainty effects, temporal summation curves, and facilitation by a pedestal in 2AFC tasks. The summation exponents are dependent on the strength of the lateral interactions, and on the distance and orientation relationship between the elements.     

Spatial properties of goldfish ganglion cells

We systematically classified goldfish ganglion cells according to their spatial summation properties using the same techniques and criteria used in cat and monkey research. Results show that goldfish ganglion cells can be classified as X-, Y-, or W-like based on their responses to contrast-reversal gratings. Like cat X cells, goldfish X-like cells display linear spatial summation. Goldfish Y-like cells, like cat Y cells, respond with frequency doubling at all spatial positions when the contrast-reversal grating consists of high spatial frequencies. There is also a third class of neurons, which is neither X- nor Y-like; many of these cells' properties are similar to those of the "not-X" cells found in the eel retina. Spatial filtering characteristics were obtained for each cell by drifting sinusoidal gratings of various spatial frequencies and contrasts across the receptive field of the cell at a constant temporal rate. The spatial tuning curves of the cell depend on the temporal parameters of the stimulus; at high drift rates, the tuning curves lose their low spatial frequency attenuation. To explore this phenomenon, temporal contrast response functions were derived from the cells' responses to a spatially uniform field whose luminance varied sinusoidally in time. These functions were obtained for the center, the surround, and the entire receptive field. The results suggest that differences in the cells' spatial filtering across stimulus drift rate are due to changes in the interaction of the center and surround mechanisms; at low temporal frequencies, the center and surround responses are out-of-phase and mutually antagonistic, but at higher temporal rates their responses are in-phase and their interaction actually enhances the cell's responsiveness.     

Effects of dexamethasone on the electrical activity of spinal neurons in rats with the transected sciatic nerve

Effects of the glucocorticoid hormone dexamethasone on the reflex discharges in the lumbar ventral roots and background activity (BA) of single neurons in the dorsal laminae of spinal grey were studied in rats after transection of the sciatic nerve. Administration of the hormone during early post-traumatic period (up to seven days) evoked no significant changes in the amplitude of increased (due to the postdenervation hyperreflexia) monosynaptic discharges on the side of nerve transection. At the same time, the monosynaptic discharges grew by 150–170% on the intact side. During later post-transection periods (up to 35 days), when ventral root reflex discharges were suppressed, dexamethasone facilitated reflex transmission via the polysynaptic segmental pathways on both the operated and intact sides. Nonetheless, the monosynaptic component of reflex discharges on the injured side did not recover. Dexamethasone treatment resulted in an increase in the number of BA-generating interneurons within the superficial dorsal horn laminae, and in a decrease in the proportion of units generating bursting activity (possibly of pathological nature).Neirofiziologiya/Neurophysiology, Vol. 27, No. 1, pp. 26–31, January–February, 1995.     

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.     

Effect of a dominant focus created in the center of the wink reflex on the local defense reflex in the rabbit

The paper deals with conjugated inhibition of rabbit's defensive limb reflex at formation of a dominant focus in the center of the eye-lid reflex. In the initial period of dominant focus formation, when the dominant comes through the stage of summation reflex, electrocutaneous limb stimulation induced, along with successive summation, temporary inhibition of the forming dominant focus. The dominant focus formed in the eye-lid center did not induce conjugated inhibition of the limb defensive reflex. In the study of the influence of the eye-lid reflex on the motor defensive one it was found that formation of temporary connection of summation reflex type, led to circulatory interaction between the centers.     

Specification of synaptic connections between sensory and motor neurons in the developing spinal cord

Experimental studies of mechanisms underlying the specification of synaptic connections in the monosynaptic stretch reflex of frogs and chicks are described. Sensory neurons innervating the triceps brachii muscles of bullfrogs are born throughout the period of sensory neurogenesis and do not appear to be related clonally. Instead, the peripheral targets of these sensory neurons play a major role in determining their central connections with motoneurons. Developing thoracic sensory neurons made to project to novel targets in the forelimb project into the brachial spinal cord, which they normally never do. Moreover, these foreign sensory neurons make monosynaptic excitatory connections with the now functionally appropriate brachial motoneurons. Normal patterns of neuronal activity are not necessary for the formation of specific central connections. Neuromuscular blockade of developing chick embryos with curare during the period of synaptogenesis still results in the formation of correct sensory-motor connections. Competitive interactions among the afferent fibers also do not seem to be important in this process. When the number of sensory neurons projecting to the forelimb is drastically reduced during development, each afferent still makes central connections of the same strength and specificity as normal. These results are discussed with reference to the development of retinal ganglion cells and their projections to the brain. Although many aspects of the two systems are similar, patterned neural activity appears to play a much more important role in the development of the visual pathway than in the spinal reflex pathway described here.     

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.     

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.     

A four-channel analysis of the tactile sensitivity of the fingertip: frequency selectivity,spatial summation,and temporal summation

Thresholds were measured for the detection of vibratory stimuli of variable frequency and duration applied to the index fingertip and thenar eminence through contactors of different sizes. The effects of stimulus frequency could be accounted for by the frequency characteristics of the Pacinian (P), non-Pacinian (NP) I, and NP III channels previously determined for the thenar eminence (Bolanowski et al., J Acoust Soc Am 84 : 1680-1694, 1988; Gescheider et al., Somatosens Mot Res 18: 191- 201, 2001). The effect of changing stimulus duration was also essentially identical for both sites, demonstrating the same amount of temporal summation in the P channel. Although the effect of changing stimulus frequency and changing stimulus duration did not differ for the two sites, the effect of varying the size of the stimulus was significantly greater for the thenar eminence than for the fingertip. The attenuated amount of spatial summation on the fingertip was interpreted as an indication that the mechanism of spatial summation consists of the operations of both neural integration and probability summation.     

A four-channel analysis of the tactile sensitivity of the fingertip: frequency selectivity,spatial summation,and temporal summation

Thresholds were measured for the detection of vibratory stimuli of variable frequency and duration applied to the index fingertip and thenar eminence through contactors of different sizes. The effects of stimulus frequency could be accounted for by the frequency characteristics of the Pacinian (P), non-Pacinian (NP) I, and NP III channels previously determined for the thenar eminence (Bolanowski et al., J Acoust Soc Am 84: 1680-1694, 1988; Gescheider et al., Somatosens Mot Res 18: 191-201, 2001). The effect of changing stimulus duration was also essentially identical for both sites, demonstrating the same amount of temporal summation in the P channel. Although the effect of changing stimulus frequency and changing stimulus duration did not differ for the two sites, the effect of varying the size of the stimulus was significantly greater for the thenar eminence than for the fingertip. The attenuated amount of spatial summation on the fingertip was interpreted as an indication that the mechanism of spatial summation consists of the operations of both neural integration and probability summation.     

Significance of the relative position in space of associated stimuli for formation and performance of motor conditioned reflexes

In experiments on cats the rate of formation of conditioned reflexes to sound (running to the feeding trough) depended on the spatial interrelations of the paired stimuli: the closer the source of the conditioned signal to the feeding trough, the sooner the formation of the conditioned reflex. It has been assumed that during formation of a conditioned reflex the closing of connection between conditioned and unconditioned stimuli is also attended with the closing of connection between the spatial parameters of the paired stimuli. Experiments with inactivation through cold of the temporal area (cortical representation of the vestibular system) of one hemisphere have shown that such a connection is formed in central parts of the vestibular analyser. When the conditioned reflex is elaborated to one feeding trough, the connection is duplicated by both hemispheres; in reflexes to two feeding troughs (i.e. spatial choice) such connections are lateralized in each hemisphere.