Encoder response of isolated frog muscle spindle elicited by pseudorandom noise stimuli

The present experiments investigated the signal transfer in the isolated frog muscle spindle by using pseudorandom noise (PRN) as the analytical probe. In order to guarantee that the random stimulus covered the entire dynamic range of the receptor, PRN stimuli of different intensities were applied around a constant mean length, or PRN stimuli of the same intensity were used while varying the mean length of the spindle. Subthreshold receptor potentials, local responses, and propagated action potentials were recorded simultaneously from the first Ranvier node of the afferent stem fiber, thus providing detailed insight into the spike-initiating process within a sensory receptor. Relevant features of the PRN stimulus were evaluated by a preresponse averaging technique. Up to tau = 2 ms before each action potential the encoder selected a small set of steeply rising stretch transients. A second component of the preresponse stimulus ensemble (tau = 2-5 ms) opposed the overall stretch bias. Since each steeply rising stretch transient evoked a steeply rising receptor potential that guaranteed the critical slope condition of the encoding site, this stimulus profile was most effective in initiating action potentials. The dynamic range of the muscle spindle receptor extended from resting length, L0, to about L0 + 100 microns. At the lower limit (L0) the encoding membrane was depolarized to its firing level and discharged action potentials spontaneously. When random stretches larger than the upper region of the dynamic range were applied, the spindle discharged at the maximum impulse rate and displayed no depolarization block or "overstretch" phenomenon. Random stretches applied within the dynamic range evoked regular discharge patterns that were firmly coupled to the PRN. The afferent discharge rate increased, and the precision of phase-locking improved when the intensity of the PRN stimulus was increased around a constant mean stretch; or the mean prestretch level was raised to higher values while the intensity of the PRN stimulus was kept constant. In the case when the PRN stimulus covered the entire dynamic range, the temporal pattern of the afferent discharge remained constant for at least 10 consecutive sequences of PRN. A spectral analysis of the discharge patterns averaged over several sequences of PRN was employed. At the same stimulus intensity the response spectra displayed low-pass filter characteristics with a 10-dB bandwidth of 300 Hz and a high-frequency slope of -12 dB/oct. Increasing the mean intensity of the PRN stimulus or raising the prestretch level increased the response power.(ABSTRACT TRUNCATED AT 400 WORDS)     

Transducer action of isolated frog muscle spindle evoked by pseudorandom noise stimuli

The dynamic response properties of the isolated frog muscle spindle receptor were investigated by recording the receptor potential evoked by pseudorandom noise (PRN) stimuli. The entire dynamic range of the receptor was determined by measuring the sensory response either at different intensities of the PRN stimulus (sigma = 8-30 microns) around a constant mean length or at the same intensity while varying the mean length from resting length L0 up to L0 + 150 microns. The 3-dB bandwidth of the test signal was 130 Hz. Random stimuli often evoked brief receptor potentials with variable size but characteristic shape. This shape contained a fast depolarization transient of the receptor potential during the stretching phase of the stimulus and a slowly decaying repolarization transient during release of stretch. The depolarization transient rose faster in proportion to the increasing amplitude of the receptor potential, so that larger receptor potentials were more phasic in character than smaller ones. The repolarization transient exhibited two segments of different exponential decay: The first brief repolarization phase lasted for 5 ms; its decline (tau = 2-5 ms) was faster for larger receptor potentials. The second slowly decaying repolarization transient was the same for different receptor potential amplitudes (tau = 47 ms). Consequently, the slow repolarization transients of succeeding receptor potentials displayed temporal summation. Since the amplitude and shape of the receptor potential remained constant during repeated sequences of PRN stimuli, this test stimulus was the most appropriate for the investigation of dynamic response properties under stationary conditions. Long-term stimulation caused a small shift of the mean membrane voltage towards hyperpolarizing values. This finding together with the marked "off effect" after termination of the stimulus indicate the action of an electrogenic pumping mechanism. The dynamic range of the muscle spindle receptor extended from resting length L0 up to L0 + 100 microns. Within this range static prestretches placed a bias upon the transducing site and effectively enhanced the amplitude of the receptor potential. Further prestretch beyond the dynamic region kept the receptor potential constant at its maximum amplitude. The receptor potential amplitude distribution was not symmetrical about the mean but was skewed in favor of depolarization values responding to the stretch trajectories of the PRN stimulus. Variation of the operating point by increasing the static prestretch also shifted the mode of the response distribution towards depolarization.(ABSTRACT TRUNCATED AT 400 WORDS)     

Small-signal analysis of response of mammalian muscle spindles with fusimotor stimulation and a comparison with large-signal responses.

1. Response dynamics of primary and secondary muscle spindle endings to small-amplitude sinusoidal stretches were found to be unaltered by tonic repetitive stimulation of fusistatic or fusidynamic fibers. 2. Overall sensitivity of these receptors is decreased by fusistatic stimulation and either unchanged, increased, or decreased by fusidynamic stimulation at rates of 75/s or greater. 3. In the case of primary endings, the results obtained with small-amplitude sinusoidal stretches are not compatible with the response of these receptors to large-amplitude ramp stretches. The difference is explained by dependence of receptor dynamics on stretch amplitude. Fusistatic stimulation tends to prevent those changes in dynamics, whereas fusidynamic stimulation tends to enhance them. 4. In the case of secondary endings, the results obtained with small- and large-amplitude stretches appear to be compatible with a linear model for this receptor (i.e., one with dynamics independent of input parameters). 5. By modulating the frequency of stimulation applied to fusimotor fibers and comparing the resulting afferent response to the receptor response to stretch dynamic characteristics of intrafusal muscle contraction can be deduced. The results suggest that the dynamics of fusiastatic and fusidynamic contraction are the same and, furthermore, that they are the same as those of extrafusal muscle. We note that the result is incompatible with measurements of the time course of twitch and tetanus development and suggest, therefore, that muscle dynamics are a function of contractile state.     

Spindle model responsive to mixed fusimotor inputs and testable predictions of beta feedback effects

Skeletofusimotor (beta) motoneurons innervate both extrafusal muscle units and muscle fibers within muscle spindle stretch receptors. By receiving excitation from group Ia muscle spindle afferents and driving the muscle spindle afferents that excite them, they form a positive feedback loop of unknown function. To study it, we developed a computationally efficient model of group Ia afferent behavior, capable of responding to multiple fusimotor inputs, that matched experimental data. This spindle model was then incorporated into a simulation of group Ia feedback during ramp/hold and triangular stretches with and without closure of the beta loop, assuming that gamma and beta fusimotor drives of the same type (static or dynamic) have identical effects on spindle afferent firing. The effects of beta feedback were implemented by driving a fusimotor input with a delayed and filtered fraction of the spindle afferent output. During triangular stretches, feedback through static beta motoneurons enhanced Ia afferent firing during shortening of the spindle. In contrast, closure of a dynamic beta loop increased Ia firing during lengthening. The strength of beta feedback, estimated as a "loop gain" was comparable to experimental estimates. The loop gain increased with velocity and amplitude of stretch but decreased with increased superimposed gamma fusimotor rates. The strongest loop gains were seen when the beta loop and the gamma bias were of different types (static vs. dynamic).     

Action potential patterns of isolated frog muscle spindle in response to sinusoidal stimulation

Signal transfer in the isolated frog muscle spindle is investigated using the linear frequency domain analysis technique. Sinusoidal stretches of different amplitudes (20-120 micron) and frequencies (0.1-120 Hz) were applied at different levels of static prestretch, ranging from resting length (L0) up to L0 + 400 micron, so that the frequency-response characteristics were measured at different operating points within the dynamic range. The neuronal responses were recorded from the first node of the afferent stem fiber with a modified air-gap technique. By this means, subthreshold receptor potentials, prepotentials preceding the impulse, and the propagated action potentials were recorded simultaneously, thus providing a detailed insight into the encoding process. There is a well-defined dynamic range of receptor responses. At L0, the encoding site is depolarized to its firing level and discharges spontaneous stimulus-independent impulses. The upper limit is given by the saturation of the receptor potential, which keeps the depolarization maximum below the level of sodium inactivation. Therefore a "depolarization block" or "overstretch" does not exist in the muscle spindle; i.e., the receptor retains its ability to encode information over a large range of dynamic and static displacements. Since the dynamic curves of the receptor potential are not symmetrical about their static operating point, the impulse pattern remains modulated throughout the dynamic range, even if small sinusoids are superimposed on a large static prestretch. The afferent discharge pattern is mainly regulated by the modulated AC component of the receptor potential. At low stimulus frequencies (less than 1 Hz) the receptor potential modulates almost linearly about the mean membrane voltage, so that the evoked discharge pattern displays a smooth analog signal, which is close to sinusoidal. Increasing the static prestretch increases both the peak response and the modulation depth of the impulse pattern. In the intermediate frequency range (1-10 Hz), the cycle histogram disintegrates into discrete peaks separated by empty bins, because the nonlinear receptor potential elicites firmly phase-locked action potentials during its fast depolarization transient. Raising the prestretch level improves the precision of phase locking and increases the number of spikes elicited per cycle.(ABSTRACT TRUNCATED AT 400 WORDS)     

Identified proprioceptive afferents and motor rhythm entrainment in the crayfish walking system.

1. In crayfish, Pacifastacus leniusculus, remotion of a walking leg stretches the thoraco-coxal (TC) muscle receptor organ (TCMRO), located at the leg's articulation with the thorax. In vitro, alternate stretch and release of the fourth leg's TCMRO entrained the centrally generated rhythmic motor output to that leg, with the remotor phase of the rhythm entraining to TCMRO stretch, the promoter phase to release. This coordination of motor bursts to afferent input corresponds to that of active, rhythmic movements in vivo. 2. Entrainment was rapid in onset (stable coordination resulting within the first or second stimulus cycle) and was relatively phase-constant (whatever the stimulus frequency, during 1:1 entrainment, remotor bursts began near the onset of stretch and promotor bursts began near the onset of release). Outside the range of 1:1 entrainment, 2:1, 1:2, and 1:3 coordination ratios (rhythm:stimulus) were encountered. Resetting by phasic stimulation of the TCMRO was complete and probabilistic: effective stimuli triggered rapid transitions between the two burst phases. 3. The TCMRO is innervated by two afferents, the nonspiking S and T fibers, which generate graded depolarizing receptor potentials in response to stretch. During proprioceptive entrainment, the more phasic T fiber depolarized and hyperpolarized more rapidly or in advance of the more tonic S fiber. These receptor potentials were modified differently in the two afferents by interaction with central synaptic inputs that were phase-locked to the entrained motor rhythm. 4. Injecting slow sinusoidal current into either afferent alone could entrain motor rhythms: promoter phase bursts were entrained to depolarization of the S fiber or hyperpolarization of the T fiber, whereas the converse response was obtained for remotor phase bursts. 5. During proprioceptive entrainment, tonic hyperpolarization of the S fiber weakened entrained promotor bursts and allowed remotor burst durations to increase. Hyperpolarizing the T fiber weakened entrained remotor bursts and allowed promotor bursts to occur during stretch. These results suggest that the staggered receptor potentials of the two afferents alternately excite opposite burst phases of the rhythm during proprioceptive entrainment. 6. Injecting brief current pulses into either afferent perturbed the timing of entrained bursts in opposite ways, suggesting that, during proprioceptive entrainment, the membrane potential trajectories of the two afferents have reciprocal triggering effects on burst transitions. 7. We infer that entrainment results from 1) complete resetting of burst transitions in a two-phase central oscillator, 2) opposing feedback pathways mediated by a phasic and a tonic afferent, 3) temporally staggered afferent receptor potentials, and 4) the ability of afferent receptor potentials to trigger burst transitions.     

Effects of hypodynamia-hypokinesia on the muscle spindle discharges of rat soleus muscle

The aim of this study was to determine whether Ia and II fiber discharges of soleus muscle spindles were modified after a 14-day period of hypodynamia (absence of weight bearing) and hypokinesia (reduction of motor activity). Fifty-one and 38 afferent fibers were studied, respectively, in control and hypodynamia-hypokinesia (HH) groups. Under deep anesthesia (pentobarbital, 30 mg/kg), a L3-L6 laminectomy was performed. Unitary potentials from the L5 dorsal root were recorded in response to ramp-and-hold stretches applied at two stretch amplitudes (3 and 4 mm) and four stretch velocities (6, 10, 15, and 30 mm/s) and to sinusoidal stretches applied at four stretch amplitudes (0.12, 0.25, 0.5, and 1 mm) and six stretch frequencies (0.5, 1, 2, 3, 6, and 10 Hz). In both animal groups, the Ia fibers showed higher dynamic index values, smaller linear range, and higher vibration sensitivity than the II fibers. They also exhibited a pause in their discharges during the stretch release contrary to II fibers, which displayed no pause in their responses. After HH, our results showed that for both fiber types all parameters measured under ramp-and-hold stretches (except the static sensitivity) were significantly increased and under sinusoidal stretches, the vibration sensitivity increased, and the response amplitude only increased at 0.12-mm stretch amplitude. The linear range of Ia afferents was limited to 0.12 mm, whereas it was unchanged for the II fibers. After HH, the stretches could be better transmitted to the muscle spindles, probably resulting from changes in passive mechanical properties of the soleus.     

Evidence that the secondary as well as the primary endings of the muscle spindles may be responsible for the tonic stretch reflex of the decerebrate cat

1. The size of the tonic stretch reflex of the soleus or gastrocnemius muscle of the decerebrate cat has been compared with the size of the reflex contraction elicited in the same muscle by high-frequency vibration applied to its tendon.2. On the assumption that vibration preferentially excites the primary endings of the muscle spindles it may be used to estimate the relation between the reflex response and the frequency of the Ia input to the spinal cord. On this basis, the increase in tension evoked by increasing extension is too great to be explained by the increase in Ia input with extension previously found on single fibre recording in comparable preparations.3. When vibration was superimposed on stretch reflexes elicited by different extensions, the size of the additional contraction elicited by the vibration remained approximately constant. If the stretch and vibration reflexes both depended entirely upon the Ia pathway, then occlusion between them would have been expected instead of the simple summation which was found.4. The absence of occlusion was not due to variation of the contractile strength of the muscle with its extension. This was shown by finding that the reflex contraction of soleus produced by stimulating the medial gastrocnemius nerve also remained the same size when elicited at different lengths of the muscle.5. The reflex effects were studied of superimposing alternate stretches and releases of 0.2 mm, on extensions of several mm. The small stretches elicited responses which were larger than expected from the response to large stretches, and which were approximately the same size at different mean lengths of the muscle.6. It is concluded that the tonic stretch reflex of the decerebrate cat cannot readily be explained solely by the increase in Ia discharge produced by stretching, as usually believed. Instead, it is suggested that the group II afferent fibres from the secondary endings of the muscle spindle also play an important part in its production.     

A muscle spindle model for primary afferent firing based on a simulation of intrafusal mechanical events.

1. A muscle spindle model for primary afferent firing is presented that contains two components representing a gamma d-dependent (bag1) and gamma s-dependent (bag2/nuclear chain) intrafusal fiber. Each of the intrafusal fibers is composed of a linear elastic element representing the sensory part and a muscle fiber representing the muscular part. 2. The muscular part of the bag1 was modeled as a slow twitch, that of the bag2 as a fast twitch muscle fiber. 3. The sensory regions were linear length transducers, generating a rising depolarization on increasing stretch. The input of both bags was fused by taking the largest depolarization to determine a generator potential. The rate of primary afferent firing depended on this generator potential as well as on its rate of change. 4. To simulate the high sensitivity of muscle spindles to small amplitudes of stretching, a model analogue of cross-bridge fixation (or stiction) has been included in the muscular part of the bag1 fiber. This makes use of one hundred cross-bridge regions that release one after the other, provided a certain breaking force is exceeded. 5. The values of the mechanical parameters that defined the model were selected by a computerized search procedure. 6. The values found by means of this procedure allowed the model to provide an accurate simulation of experimental data on ramp-and-hold stretches (for 6 different stretch velocities under variable conditions of fusimotor activity). 7. On sinusoidal stretches at a frequency of 1 Hz the spindle model responded with about one-half the discharge modulation reported in experimental studies. Its phase advance tended to be slightly lower than that observed for real spindles. 8. Frequency response curves showed the same high sensitivities at high frequencies as those observed in real spindles. 9. Close evaluation of the model compared with experimental results in literature reveal its merits as well as its limitations. Because the model is structural rather than phenomenologic, it provides insight into how intrafusal events may contribute to observed firing properties of real muscle spindles.     

Movement reduces the dynamic response of muscle spindle afferents and motoneuron synaptic potentials in rat

Among the mechanisms that may result in modulation of the stretch reflex by the recent history of muscle contraction is the history dependence observed under some conditions in the response properties of muscle spindles. The present study was designed to test one report that in successive trials of muscle stretch-release, spindle afferent firing during stretch, i.e., the dynamic response shows no history dependence beyond the initial burst of firing at stretch onset. Firing responses of spindle afferents were recorded during sets of three consecutive trials of triangular stretch-release applied to triceps surae muscles in barbiturate-anesthetized rats. All 69 spindle afferents fired more action potentials (spikes) during the dynamic response of the first trial, excluding the initial burst, than in the following two trials. The reduced dynamic response (RDR) was nearly complete after trial 1 and amounted to an average of approximately 12 fewer spikes (16 pps slower firing rate) in trial 3 than in trial 1. RDR was sensitive to the interval between stretch sets but independent of stretch velocity (4-32 mm/s). RDR was reflected in the synaptic potentials recorded intracellularly from 16 triceps surae alpha-motoneurons: depolarization during muscle stretch was appreciably reduced after trial 1. These findings demonstrate history dependence of spindle afferent responses that extends throughout the dynamic response in successive muscle stretches and that is synaptically transmitted to motoneurons with the probable effect, unless otherwise compensated, of modulating the stretch reflex.     

Aftereffects in the responses of cat muscle spindles

Responses have been recorded from primary endings of muscle spindles in the cat soleus muscle. Changes in spindle responsiveness were measured following a period of conditioning that consisted of a series of rapid stretches or of tetanic ventral root stimulation. In the testing procedure the response of a single spindle afferent was recorded to stimulation of a dynamic fusimotor axon during a slow stretch. Changes in gross afferent discharge coming from the muscle were measured by integrating the activity recorded in dorsal roots. If, after conditioning stretches, the muscle was immediately returned to its initial length, the spindle responded to the test fusimotor stimulation with a high-frequency burst of afferent impulses. If the muscle was held stretched for 3 s after conditioning the response to the brief test tetanus was small or "depressed." It has been suggested that conditioning stretches result in detachment of stable crossbridges in intrafusal fibers and that these bridges then reform over the next few seconds at whatever length the muscle happens to have at the time. When it is long, shortening the muscle back to the initial length leads to the development of slack in intrafusal fibers because of the passive stiffness they have acquired from the presence of the stable bridges. Under these conditions a brief test fusimotor tetanus will lead to a depressed response because the slack must first be taken up before a full response can be generated. It was possible to reverse the depression by interposing an extrafusal contraction during the period between the conditioning and test sequences. It is suggested that lateral compression from the contracting extrafusal fibers and the stretch they impose as they relax reduces any intrafusal slack and thereby reduces the depression. A more quantitative measure of intrafusal slack than the test for depression is to determine the delay in onset of the afferent response to a longer fusimotor tetanus. The delay was short a long initial muscle lengths where, if the muscle was left undisturbed, it soon disappeared completely and spontaneously. It is suggested that at long lengths passive tension in the muscle tends to remove any slack in intrafusal fibers and therefore removes any after effects. The rise in resting discharge of muscle afferents after a conditioning tetanus applied to the ventral root ("postcontraction sensory discharge") can be accounted for by the same hypothesis.(ABSTRACT TRUNCATED AT 400 WORDS)     

Impulse activity and receptor potential of primary and secondary endings of isolated mammalian muscle spindles.

1. An isolated muscle spindle preparation from a tail muscle of cat is described. The afferent response to a ramp-and-hold stretch was recorded in individual axons from identified primary and secondary endings. 2. Primary endings exhibit a prominent dynamic response, including an initial burst. They also show a well-maintained static discharge. Secondary endings also show a well-sustained static discharge but generally have a much lower dynamic sensitivity. The response of primary and secondary endings of the isolated spindle are similar to the typical responses seen in vivo in groups Ia or group II afferent fibres respectively. 3. Following impulse blockade by tetrodotoxin, the receptor potential was recorded from primary and from secondary endings in response to ramp-and-hold stretch. 4. During the dynamic phase the receptor potential of primary endings consists of a depolarization which has two components. (a) An initial component occurs early during ramp stretch, depends in rate of rise and amplitude on velocity of stretch and is reduced on repetitive stretch; it appears to be responsible for the initial burst. (b) A late dynamic component, which follows, is also dependent on stretch velocity and produces the late dynamic discharge. At the end of ramp stretch the receptor potential falls, and may undershoot, the static level. There is a subsequent adaptive fall during hold stretch, then a maintained static level of receptor potential. On release from stretch the membrane is hyperpolarized. 5. Secondary endings usually show a smaller dynamic response, lacking the initial component seen in primary endings. They also generally lack an undershoot following the ramp and have less of a post-release hyperpolarization. 6. Static levels of receptor potential in both primary and secondary endings are related to amplitude of stretch. 7. The receptor potentials of primary and secondary endings account for the major features of the impulse responses of these endings to ramp-and-hold stretch. In primary endings the dynamic frequencies may also depend upon a sensitivity of the impulse initiating site to rate of change of receptor current.     

Responses of neurones in motor cortex and in area 3A to controlled stretches of forelimb muscles in cebus monkeys.

1. The experiments were designed to investigate the effects of longitudinal muscle displacements on neurones of the motor cortex of anaesthetized Cebus monkeys and thus test the hypothesis that signals from muscle spindles may modify motor cortical output. The effects of sinusoidal stretching of the extensor digitorum communis (EDC) at frequencies varying from 6 to 300 Hz and of step and rhomboidal stretches were studied in neurones of the motor cortex. For comparison, neurones of the primary receiving area for low-threshold muscle afferents, cortical area 3a, were also included in this study. Neurones of the motor cortex were subdivided into corticospinal (PT) neurones and non-corticospinal (non-PT) neurones. 2. Threshold stretch amplitudes were clearly higher for neurones of area 4 (PT and non-PT) than for 3a neurones. However, a conspicuous fall in threshold stretch amplitude was observed for all three neurone populations when the frequency of sinusoidal stretching was increased (highest frequency: 300 Hz). A small number of non-PT and PT neurones responded to vibration amplitudes of less than 100 mum and some of these low-threshold cells of area 4 also responded to rhomboidal stretches of 8 mm/sec ramp velocity and 80 mum plateau amplitude. Increasing the stretch amplitude to twice threshold nearly doubled the output magnitude in all three cell types. Neurones of area 3a and non-PT neurones of area 4 had similar latencies, and these were significantly shorter than the latencies of PT neurones tested with trains of high frequency vibration. Dynamic response patterns were observed in all three cell types, but most frequently in 3a neurones. 3. It is concluded that, in Cebus monkeys, signals from both primary and secondary muscle spindle endings from forelimb muscles reach the motor cortex. Under the present experimental conditions, the input from the primaries to the motor cortex was effective only if these spindle receptors were driven maximally by vibratory stimuli. The particularly low probability of stretch-evoked discharges of cortico-spinal neurones in the anaesthetized preparation may be explained by a low gain in transmission from input to output cells of the motor cortex.     

Classification of human muscle stretch receptor afferents: a Bayesian approach

1. A sample of 124 human muscle afferents originating from the finger extensor muscles were recorded from the radial nerve in the upper arm. A method is described to formalize the classification of units in muscle spindle primary and secondary afferents and Golgi tendon organ afferents on the basis of a few, nonrigorous assumptions. The classification was based on experimental data that largely have been described in a series of previous papers, although some additional data were collected in the present study. 2. The units were subjected to five tests providing identification data: twitch contraction test, ramp-and-hold stretch, small-amplitude sinusoidal stretches superimposed on ramp stretch, stretch sensitization, and isometric contraction/relaxation. From these five tests the following eight response features were extracted: response to maximal isometric twitch contractions, type of stretch sensitization, correlation between discharge rate and contractile force, response to sudden isometric relaxation, presence or absence of an initial burst, deceleration response, prompt silencing at slow muscle shortening, and driving by small-amplitude sinusoidal stretches. 3. A Bayesian decision procedure was adopted to classify the units on the basis of the eight discriminators. As a first step, units were provisionally classified into muscle spindle primary and secondary afferents, and Golgi tendon organ afferents, by intuitively weighting their responses to the identification tests. Prior probabilities were estimated on the basis of the provisional classification. The eight response features were analyzed and tabulated for all afferents, and the likelihood functions of the tests were directly calculated on the basis of these data.(ABSTRACT TRUNCATED AT 250 WORDS)     

The 'initial burst' of human primary muscle spindle afferents has at least two components

Ten muscle spindle primary afferents from the extensor digitorum communis muscle of man were studied with single unit afferent recordings. Responses to slow test stretches with three different pre-history conditions were assessed to investigate the contribution of rapid stretches to the stretch sensitization phenomenon. In two of the conditions, the slow test ramps were preceded by rapid stretch after which the parent muscle of the receptor was either (a) kept short for 5 seconds or (b) kept long for 3.2 seconds and then returned to the short muscle length for 5 seconds. The third condition (c) consisted of a slow stretch from short to long muscle length followed by a rapid return to the short muscle length, in turn followed by 5 seconds at the short muscle length. Afferent responses were depressed when the muscle had been kept at the long length after the rapid stretches (condition b) and enhanced when the muscle had been kept at the short length (conditions a & c). A prominent 'initial burst' was only present in the afferent discharge when the parent muscles of the primary endings had been kept short (condition a). A second, more prolonged burst was present for conditions (a) and (c) but was lacking or inconspicuous when the muscle had been kept long after rapid stretches (condition b). The rapid stretches in the stretch sensitization paradigm appear to be a primary factor not only for the enhanced responses of sensitized primary afferents but also for the depressed responses of desensitized primary afferents.     

Static and Dynamic Properties of Golgi Tendon Organs in the Anterior Tibial and Soleus Muscles of the Cat

The responses of tendon organs of the anterior tibial muscle have been studied during twitch contraction, passive stretch, fused tetanic contractions and sinusoidal stretching in Nembutal anesthetized cats. The majority of the tendon organs had similar thresholds to active contraction and passive stretch tension. Some tendon organs were found to discharge spontaneously in the relaxed muscle. An approximate power function relationship has been found between steady state impulse frequency and muscle tension. The receptor properties are compared with those of soleus tendon organs. It is concluded that static and dynamic properties of Golgi tendon organs in the anterior tibial and the soleus muscles fall within the same range of variation, and that apparent discharge dissimilarities can be explained as due to differences in muscle mechanics.     

The ‘initial burst’ of human primary muscle spindle afferents has at least two components

Ten muscle spindle primary afferents from the extensor digitorum communis muscle of man were studied with single unit afferent recordings. Responses to slow test stretches with three different pre-history conditions were assessed to investigate the contribution of rapid stretches to the stretch sensitization phenomenon. In two of the conditions, the slow test ramps were preceded by rapid stretch after which the parent muscle of the receptor was either (a) kept short for 5 seconds or (b) kept long for 3.2 seconds and then returned to the short muscle length for 5 seconds. The third condition (c) consisted of a slow stretch from short to long muscle length followed by a rapid return to the short muscle length, in turn followed by 5 seconds at the short muscle length. Afferent responses were depressed when the muscle had been kept at the long length after the rapid stretches (condition b) and enhanced when the muscle had been kept at the short length (conditions a & c). A prominent ‘initial burst’ was only present in the afferent discharge when the parent muscles of the primary endings had been kept short (condition a). A second, more prolonged burst was present for conditions (a) and (c) but was lacking or inconspicuous when the muscle had been kept long after rapid stretches (condition b). The rapid stretches in the stretch sensitization paradigm appear to be a primary factor not only for the enhanced responses of sensitized primary afferents but also for the depressed responses of desensitized primary afferents.     

Receptor potentials and electrical properties of nonspiking stretch-receptive neurons in the sand crab Emerita analoga (Anomura, Hippidae).

Receptor potentials and electrical properties of nonspiking stretch-receptive neurons in the sand crab Emerita analoga (Anomura, Hippidae). Four nonspiking, monopolar neurons with central somata and large peripheral dendrites constitute the sole innervation of the telson-uropod elastic strand stretch receptor in Emerita analoga. We characterized their responses to stretch and current injection, using two-electrode current clamp, in intact cells and in two types of isolated peripheral dendritic segments, one that included and one that excluded the dendritic termini (mechanosensory membrane). The membrane potentials of intact cells at rest (mean +/- SD: -57 +/- 4. 4 mV, n = 30), recorded in peripheral or neuropil processes, are similar to the membrane potentials of isolated dendritic segments and always less negative than membrane potentials of motoneurons and interneurons recorded in the same preparations. Ion substitution experiments indicate that the membrane potential is influenced strongly by Na+ conductance, probably localized in the mechanotransducing terminals within the elastic strand. The form of the receptor potential in response to ramp-hold-release stretch remains the same as stretch amplitude is varied and is not dependent on initial membrane potential (-70 to -30 mV) or recording site: initial depolarization (slope follows ramp of applied stretch), terminated by rapid, partial repolarization to a plateau (delayed depolarization) that is intermediate between the peak depolarization and the initial potential and sustained for the duration of the stretch. Responses to depolarizing current pulses are similar to stretch-evoked receptor potentials, except for small amplitude stimuli: an initial peak occurs only in response to stretch and probably reflects elastic recoil of the extracellular matrix surrounding the dendritic terminals. The rapid, partial repolarization depends on holding potential and is abolished by 4-aminopyridine (4-AP; 10 mM), implicating a fast-activating, fast-inactivating K+ conductance; TEA (60 mM) abolishes the remaining slow repolarization to the plateau. In intact cells, but not dendritic segments, regenerative depolarizations can arise in response to stretch or depolarizing current pulses; they are reduced by CdCl2 (10 microM) in the saline containing TEA and 4-AP and probably reflect current spread from Ca2+ influx at presynaptic terminals in the ganglion. We found no evidence for other voltage-activated conductances. Unlike morphologically similar "nonspiking" thoracic receptors of other species, E. analoga's nonspiking neurons are electrically compact and do not boost the analogue afferent signal by voltage-activated inward currents. The most prominent (only?) voltage-activated extra-ganglionic conductances are for potassium; by reducing the slope of the stretch-plateau depolarization curve, they extend each neuron's functional range to the full range of sensitivity of the receptor.     

Processing vibratory stimuli in isolated frog muscle spindle

Summary Experiments were performed on isolated frog muscle spindle receptors to study the particular transducer and encoder mechanisms involved in the signal transfer of high frequency sinusoids (vibration). In order to systematically investigate the signal transfer over the entire dynamic range of the receptor, vibration stimuli were applied to the intrafusal muscle bundle at different prestretch levels, so that the isolated receptor potential or the afferent impulse train were recorded at different operating points. The vibration-induced receptor potential displayed severe distortion, because the depolarization during stretch rose steeply, whereas the repolarization transient during release of stretch declined more slowly. The positive peak velocity values of the depolarization transient increased with increasing stimulus frequency, although the ac-component of the receptor potential decreased. The negative peak velocity values of the repolarization transient remained constant throughout the frequency range. The amplitude of the receptor potential grew larger when vibration of constant amplitude was applied at increasing levels of prestretch, revealing another non-linearity of the transducer. These two types of non-linearity were influential in determining the afferent discharge pattern. Each fast depolarization transient facilitated the generation of a single action potential, which therefore could be firmly phase-locked to a small segment of the vibratory movement. Due to its short risetime, the depolarization transient tended to prevent multiple firing during one stimulus cycle. The prolonged depolarizing afterpotential of the evoked action potential operated in the same direction. Increasing prestretch greatly enhanced the responsiveness of the spindle to vibration. Thus, under appropriate conditions, the afferent discharge was driven in 11 synchrony with the vibration. An analysis is given of the after-effects of repetitive activity at the receptor site. The progressive decline of the mean membrane voltage during long lasting stimulation and the post-tetanic hyperpolarization (off-effect) on termination of the vibration suggest the action of an electrogenic pumping mechanism. As a consequence, the afferent impulse train possessed a complex structure segmented into several transient and steady states, which differed in impulse rate, phase response, and in the degree of phaselocking     

The contribution of mechanical factors to the early adaptation of the spindle response

1. Adaptation in terms of the early fall of the receptor potential was studied in isolated frog spindles. The contribution of gross mechanical changes to the decline of the response was determined by comparing the responses obtained under constant length and under constant tension.2. It was found that the early adaptation under constant stretch increased with increasing lengthening of the spindle for stretches up to 25-30% of the resting length and decreased with still stronger stretches. When the spindle was stretched by 100% or more the static phase of the receptor potential reached nearly the same height as the dynamic peak and the early adaptation approached zero.3. The early adaptation decreased with decreasing velocity of linearly rising stretch and approached zero for stretches below about 0.5 mm/sec.4. For different strengths of a steplike stretch the amount of early adaptation was linearly related to the fall in tension over the same period. The relative amount of tension fall, however, was always less than the corresponding fall of the response.5. The early adaptation was 15-20% smaller under constant tension than under constant length for stretches below the level giving the maximum dynamic peak.6. The results suggest that a comparatively small amount of the early adaptation of the spindle response to constant stretch is related to gross alterations in length in different regions of the spindle. The main part of the adaptive fall of the response is probably related to functional properties of the sensory membrane and to the ionic mechanism underlying the production of the receptor potential.