Static sensitivity of primary muscle spindle endings

Static discharges were studied in 75 primary endings of passive muscle spindles during stepwise stretching of the cat triceps surae muscle. Afferents conducting excitation with velocities of between 72 and 115 m/sec, with high dynamic sensitivity, and with static thresholds below 8 mm were chosen. The muscle was stretched by 10 mm relative to the completely relaxed state with a step of 0.8 mm. Spike discharges were recorded 40 sec after each stretching for 30 sec and the mean frequency was calculated. Comparison of static and differential static responses for different units, of the "muscle length-mean discharge frequency" dependence, and of the static thresholds showed that a linear (under 4.5 spikes/sec/mm) or steady increase in the mean discharge frequency to 40 spikes/sec took place in only 20% of primary endings with a probability of more than 0.7 for each step of muscle stretching. In most primary endings a narrow range of sensitivity to a change in the static length of the muscle was found. It is suggested that the "poor" static sensitivity was due either to high static thresholds or to the absence of increases in mean discharge frequency despite continued stretching.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 13, No. 5, pp. 540–548, September–October, 1981.     

Model study of muscle spindle primary endings subjected to dynamic fusimotor activation

An earlier proposed model of the de-efferented muscle spindle mechano-receptors has been developed further to simulate the effects of the dynamic fusimotor ( _D) activation of the group Ia afferents (primary endings).The rate sensitivity of the original second order receptor model might be increased simply by increasing the overall viscous damping of the simulated polar regions of the nuclear bag fibre. However, adequate simulation of the typical time course of the stretch response of the primary endings during _D-activation required a subdivision of the polar regions into an active and a passive part. A reasonable behaviour of the model was obtained by simulating a local contraction covering about 50–90% of the polar regions of the nuclear bag fibres.The ramp response of the model showed a quick rate response component that increased by increasing the rate of the simulated stretch. This component was not significantly influenced by the simulated _D-activation.A slow rate component appeared to increase approximately in the same proportion as the intensity of the simulated _D-activation.The behaviour of the model closely corresponds to that of the biological prototype. The study demonstrates that the electrophysiological effects of activating the dynamic fusimotor fibres are indeed compatible with peripheral mechanical events associated with contraction phenomena within the polar regions of the nuclear bag intrafusal muscle fibres.     

A mechanical model of muscle and its application to the intrafusal fibres of the mammalian muscle spindle

A three-component model of the muscle is used in which the components change their values when the muscle is stimulated. In particular the elastic components change not only their moduli of elasticity but the unstretched lengths decrease when the muscle is in the active state. When the model is extended to the intrafusal muscle fibres of the mammalian muscle spindle it can reproduce some of the observed responses to mechanical stretch and fusimotor stimulation.     

Ultrastructure of dynamic and static skeletofusimotor endings in a cat muscle spindle

Summary Endings of four skeletofusimotor axons in a spindle of the cat tenuissimus muscle were examined in semithin (1-m thick) and ultrathin transverse serial sections. Two (dynamic) axons terminated on the nuclear bag₁ intrafusal muscle fiber and on extrafusal fibers of the dark type. Two (static) axons terminated on the nuclear chain intrafusal fibers and extrafusal fibers of the intermediate type. The degree of indentation of axon terminals into the muscle surface, thickness of the sole plate and extent of folding of subjunctional membranes differed among intrafusal and extrafusal terminations of the same axon. Endings of axons on the bag₁ and chain fibers were also morphologically dissimilar. Motor axons may not determine ending morphology. Rather the form and structure of a bag₁ or chain ending may be determined by the type of intrafusal fiber on which the ending lies and the ending's distance from the primary sensory axon.     

Effect of succinylcholine on responses of neurons in the motor cortex to natural activation of muscle spindle primary endings.

In locally anesthetized cats, the effects of intravenous administration of succinylcholine (SCh) in sub-paralytic dosages on the responses of single neurons in motor cortex to small dynamic muscle stretches were studied. A large transient enhancement of these cortical responses with a time course corresponding to the peripheral action of SCh on muscle spindles was observed. This finding is discussed in terms of the hypothesis that muscle spindle primary endings may activate projections to motor cortex.     

Medullary inspiratory activity: influence of intercostal tendon organs and muscle spindle endings

Studies were conducted to determine the effects of intercostal muscle spindle endings (MSEs) and tendon organs (TOs) on medullary inspiratory activity in decerebrate and allobarbital-anesthetized cats. Impeded muscle contractions, elicited by electrical stimulation of the peripheral cut end of the T6 ventral root, were used to stimulate external and internal intercostal TOs without MSEs. Impeded contractions of either the external or internal intercostal muscles reduced phrenic and medullary inspiratory neuronal activities. Vibration was used to selectively stimulate external or internal intercostal MSEs (90 and 40 micron amplitude, respectively). Selective stimulation of either external or internal intercostal MSEs did not change phrenic or medullary inspiratory neuronal activities. It is concluded that both external and internal intercostal TOs have a generalized inhibitory effect on medullary inspiratory activity and intercostal MSEs have no effect on medullary inspiratory activity.     

Medullary expiratory activity: influence of intercostal tendon organs and muscle spindle endings

Studies were conducted to determine the effects of intercostal muscle spindle endings (MSEs) and tendon organs (TOs) on medullary expiratory activity in decerebrate cats. Impeded intercostal muscle contractions, elicited by electrical stimulation of the peripheral cut end of the T6 ventral root, were used to stimulate intercostal TOs without MSEs. Impeded contractions of the intercostal muscles augmented expiratory laryngeal motoneuron activity, and either had no effect on or reduced the activity of bulbospinal expiratory neurons. Vibration was used to stimulate intercostal MSEs. Intercostal MSEs had no effect on medullary expiratory neuron activity. It is concluded that both external and internal intercostal TOs have an excitatory effect on expiratory laryngeal motoneuron activity and an inhibitory effect on a subpopulation of expiratory neurons driving intercostal and/or abdominal muscles, and intercostal MSEs have no direct influence on medullary expiratory activity.     

Comparison of motor endings of the cat's muscle spindle stained for NADH-tetrazolium reductase and cholinesterase

Summary Cat muscle spindles were examined histochemically in serial transverse sections of tenuissimus muscles stained for ATPase, NADH-TR and ChE alternating sequentially. Motor nerve terminals on nuclear bag₁, bag₂ and nuclear chain intrafusal muscle fibers were identified in periodic sections stained for ChE. Intrafusal fiber regions that carried ChE-active areas were then examined in staining for NADH-TR. The motor endings on the three types of intrafusal fiber differed in their apparent histochemical content of both ChE and NADH-TR. The observations suggest that functional differences may exist among motor nerve terminals on the various intrafusal fiber types.     

A biological model of the excitation of a second order sensory neurone

Summary Computer simulation of a relatively simple model can reproduce the main characteristics of the firing patters of some nerve cells. The abdominal stretch receptor of the crayfish has provided an analogous biological model. Synaptic input impulses were simulated by randomly distributed, short lasting transmembrane current pulses. Under these experimental conditions the stretch receptor neurone largely behaved as predicted by the computer simulations.     

Superimposing noise linearizes the responses of primary muscle spindle afferents to sinusoidal muscle stretch

Experiments were conducted in anaesthetized and spinalized cats to measure the extent to which the non-linear response of Ia afferent fibers to sinusoidal muscle stretch as expressed by the peristimulus-time-histograms, PSTHs, can be transformed into a linear one by means of the superposition of random stretch ("mechanical noise"). The gastrocnemius muscles of one hind leg were stretched and the response to sinewave muscle stretch (amplitudes between 0.01 and 4.0 mm, frequencies between 0.1 and 20 Hz) were investigated while band-limited mechanical noise was superimposed on the sinewave stretch. The random stretch upper cut-off frequency was varied between 60 and 300 Hz; the displacements were normally distributed. The noise amplitude sigma, i.e. the standard deviation of the displacement distributions, was varied systematically between 0.002 and 0.4 mm. Mechanical noise was very effective in raising the mean discharge rate. Added to the sinusoidal stretch it prevented the cessation of firing during the release phase of the stretch cycle, or at least reduced the duration of discharge pauses, i.e., a linearization occurred. In general, the larger the noise amplitude, the more the amplitude of the fundamental harmonic component was attenuated and the phase lead reduced. Apart from this rule the particular combination of superimposing small noise (sigma less than 0.02 mm) on small sinewave stretch (A less than 0.02 mm) could enhance the depth of sinusoidal modulation of cycle histograms (compared with responses to pure sinusoids). Linearizing the sinewave response by additional noise allowed the estimation of frequency response characteristics in the otherwise non-linear range of amplitudes (sinewave amplitude 0.5-1.0 mm).(ABSTRACT TRUNCATED AT 250 WORDS)     

The pause in firing of a primary muscle spindle at the transition between dynamic and static stretch: A mathematical model

A mathematical model to offer an explanation of the pause in firing of a primary muscle spindle at the transition between dynamic and static stretch is suggested. It is proposed that the firing frequency is proportional to a generator current at the site of the transduction (presumably the five terminal endings) and that the receptor potential is a version of this current filtered by the passive cable properties of the nerve between site of transduction and site of measurement.A mathematical expression is derived for the receptor potential from data in the literature. From this and an equivalent circuit of the nerve, an expression for the generator current is derived.This work was partially supported by National Institutes of Health Training Grant, Presbyterian-St. Luke's Hospital grant-in-aid and National Science Foundation. It was done in partial fulfillment of the requirements for the degree of Doctor of Philosophy (HBN) at the University of Illinois at the Medical Center.     

Ionic basis of the receptor potential in primary endings of mammalian muscle spindles

The effect of changing the ionic composition of bathing fluid on the receptor potential of primary endings has been examined in isolated mammalian spindles whose capsule was removed in the sensory region. After impulse activity is blocked by tetrodotoxin, ramp-and-hold stretch evokes a characteristic pattern of potential change consisting of a greater dynamic depolarization during the ramp phase and a smaller static depolarization during the hold phase. After a high-velocity ramp there is a transient post-dynamic undershoot to below the static level. On release from hold stretch, the potential shows a postrelease undershoot relative to base line. The depolarization produced by stretch is rapidly decreased by the removal of Na+ and Ca2+. Addition of normal Ca2+ partly restores the response. Stretch appears to increase the conductance to Na+ and Ca2+ in the sensory terminals. The postdynamic undershoot is diminished by raising external K+ and blocked by tetraethylammonium (TEA). It apparently results from a voltage-dependent potassium conductance. The postrelease undershoot is decreased by raising external K+, but is not blocked by TEA. It is presumably caused by a relative increase in potassium conductance on release. Substitution of isethionate for Cl- or the addition of ouabain does not alter the postdynamic and postrelease undershoots.     

Somatotopic organization of second order neurons of the eye muscle proprioception

Unit activity was recorded extracellularly from lamb's nucleus principalis and pars oralis of trigeminal nuclear complex following moderate manual stretching of individual extraocular muscles. The oral portion of the spinal trigeminal nucleus and the main sensory nucleus have been investigated by systematic exploration of the second-order neurons of the eye muscle proprioception. Such responses were somatotopically organized. In particular, each single extraocular muscle was represented along the main dorso-ventral axis in this manner: superior oblique and superior rectus in a dorsal layer; inferior rectus and inferior oblique in an intermediate layer, while the medial rectus and the lateral rectus were represented more ventrally. In a few experiments this representation was not observed, due to intermingling of the units. The topographic organization of eye muscle proprioception in the trigeminal nuclear complex described above closely corresponds to that reported by previous authors in the Gasser ganglion.     

Third-order reverse correlation analysis of muscle spindle primary afferent fiber responses to random muscle stretch

The response of primary muscle spindle afferent fibers to muscle stretch is nonlinear. Now spindle responses (trains of action potentials) to band-limited Gaussian white noise length perturbations of the gastrocnemius muscles (input signal) are described in cats. The input noise upper cutoff frequency was clearly above the frequency range of physiological length changes in cat hindleg muscles. The input-output relation was analyzed by means of peri-spike averages (PSAs), which could be shown to correspond to the kernels of Wiener's white noise approach to systems identification. The present approach (the reverse correlation analysis) was applied up to the third order. An experiment consisted of two recordings: one (the source recording) to determine PSAs and the other (the test recording) to provide an input signal for predicting responses. The predictions of different orders were compared with the actual neuronal response (the observation) of the test recording. Four different approximation procedures were developed to adapt prediction and observation and to determine weighting factors for the predictions of different orders. The approximations also yielded the value of the power density P of the input noise signal: at a variety of stimulus parameters, P from approximations had the same magnitude as P determined directly from the input signal amplitude spectrum. The prediction of a sequence of action potentials improved the higher the order of components. 37 of 42 action potentials of a test recording (the observation) could be confidently predicted from PSAs or kernels. Compared with the size of the linear first-order prediction curve, the relative sizes of the second and third-order prediction curves were: 1.0∶0.47∶0.26.     

Third-order reverse correlation analysis of muscle spindle primary afferent fiber responses to random muscle stretch

 The response of primary muscle spindle afferent fibers to muscle stretch is nonlinear. Now spindle responses (trains of action potentials) to band-limited Gaussian white noise length perturbations of the gastrocnemius muscles (input signal) are described in cats. The input noise upper cutoff frequency was clearly above the frequency range of physiological length changes in cat hindleg muscles. The input–output relation was analyzed by means of peri-spike averages (PSAs), which could be shown to correspond to the kernels of Wiener’s white noise approach to systems identification. The present approach (the reverse correlation analysis) was applied up to the third order. An experiment consisted of two recordings: one (the source recording) to determine PSAs and the other (the test recording) to provide an input signal for predicting responses. The predictions of different orders were compared with the actual neuronal response (the observation) of the test recording. Four different approximation procedures were developed to adapt prediction and observation and to determine weighting factors for the predictions of different orders. The approximations also yielded the value of the power density P of the input noise signal: at a variety of stimulus parameters, P from approximations had the same magnitude as P determined directly from the input signal amplitude spectrum. The prediction of a sequence of action potentials improved the higher the order of components. 37 of 42 action potentials of a test recording (the observation) could be confidently predicted from PSAs or kernels. Compared with the size of the linear first-order prediction curve, the relative sizes of the second and third-order prediction curves were: 1.0 : 0.47 : 0.26. Received: 15 November 1994/Accepted in revised form: 23 May 1995