Discharge Patterns Of Afferents Research Articles

Human Muscle Spindles Act as Forward Sensory Models

Modern theories of motor control incorporate forward models that combine sensory information and motor commands to predict future sensory states. Such models circumvent unavoidable neural delays associated with on-line feedback control. Here we show that signals in human muscle spindle afferents during unconstrained wrist and finger movements predict future kinematic states of their parent muscle. Specifically, we show that the discharges of type Ia afferents are best correlated with the velocity of length changes in their parent muscles approximately 100-160 ms in the future and that their discharges vary depending on motor sequences in a way that cannot be explained by the state of their parent muscle alone. We therefore conclude that muscle spindles can act as "forward sensory models": they are affected both by the current state of their parent muscle and by efferent (fusimotor) control, and their discharges represent future kinematic states. If this conjecture is correct, then sensorimotor learning implies learning how to control not only the skeletal muscles but also the fusimotor system.

Group III and IV muscle afferent discharge patterns after repeated lengthening and shortening actions

The purpose of this study was to test the hypothesis that group III and IV muscle afferent activity would differ after concentric- and eccentric-type fatiguing tasks. Tibialis anterior afferent activities from adult rats were measured in three conditions: before and after a rest period (C), and after concentric (CC) or eccentric (EC) exercise. Specific activators were used to elicit increases in afferent discharge rates, i.e., electrically induced fatigue (EIF), or potassium chloride (KCl) and lactic acid (LA) injections. After the rest period (POST-condition), the control group displayed a pattern of response to stimuli similar to that obtained in baseline condition (PRE-condition). However, responses were significantly different in the exercise groups: afferent responses were blunted in the CC group and were almost suppressed in the EC group. These results demonstrate that the type of muscular contraction involved in the fatiguing task can affect group III and IV afferent fiber activity differently and, potentially, can differentially affect the regulation of central motor command.

Dynamic Displacement of Normal and Detached Semicircular Canal Cupula

The dynamic displacement of the semicircular canal cupula and modulation of afferent nerve discharge were measured simultaneously in response to physiological stimuli in vivo. The adaptation time constant(s) of normal cupulae in response to step stimuli averaged 36 s, corresponding to a mechanical lower corner frequency for sinusoidal stimuli of 0.0044 Hz. For stimuli equivalent to 40–200 deg/s of angular head velocity, the displacement gain of the central region of the cupula averaged 53 nm per deg/s. Afferents adapted more rapidly than the cupula, demonstrating the presence of a relaxation process that contributes significantly to the neural representation of angular head motions by the discharge patterns of canal afferent neurons. We also investigated changes in time constants of the cupula and afferents following detachment of the cupula at its apex—mechanical detachment that occurs in response to excessive transcupular endolymph pressure. Detached cupulae exhibited sharply reduced adaptation time constants (300 ms–3 s, n = 3) and can be explained by endolymph flowing rapidly over the apex of the cupula. Partially detached cupulae reattached and normal afferent discharge patterns were recovered 5–7 h following detachment. This regeneration process may have relevance to the recovery of semicircular canal function following head trauma.

Effects of the calcium antagonist nifedipine on the afferent impulse activity of isolated cat muscle spindles

The impulse activity of muscle spindles isolated from the cat tenuissimus muscle was investigated under varying concentrations of the L-type calcium channel blocker nifedipine. At a concentration of 25 μM nifedipine impulse activity was clearly diminished in both primary and secondary endings. However, low concentrations of the drug (5–10 μM) exerted unexpected excitatory effects. The dynamic properties of primary endings in particular were augmented; those of secondary endings were also increased, although only slightly. A detailed analysis of the afferent discharge patterns obtained under ramp-and-hold stretches yielded the following effects of 10 μM nifedipine. (1) The initial burst at the beginning of the ramp phase of a stretch was increased in primary endings; (2) the peak dynamic discharge frequency at the end of the ramp phase was considerably increased in most primary endings; (3) the sensitivity of the peak dynamic discharge value to varying amplitudes and velocities of stretch was significantly enhanced in primary endings, and also increased, although only slightly, in secondary endings; (4) the rise in the discharge frequency during the ramp phase of a stretch was augmented in both types of ending, the effect being again stronger in primary endings; (5) the fast adaptive decay of the impulse frequency following the ramp phase of a ramp-and-hold stretch was significantly increased in primary endings, but remained unaffected in secondary endings. The enhanced dynamic properties of primary endings were also observed under small sinusoidal stretch stimuli (10 μm, 40 Hz), where nifedipine induced a significant shift in the position of the 1:1 driven action potentials toward smaller phase values. In view of an increase in tension in the isolated muscle spindle and an increased initial burst in primary endings in the presence of nifedipine, it is suggested that the drug facilitates the attachment of cross-bridges in the poles of the intrafusal muscle fibers. The increase in the dynamic properties of primary endings points to the possibility that the drug preferentially affects the nuclear bag 1 fiber. The inhibitory effect on the afferent discharge rate at high doses of the drug is interpreted as the consequence of a calcium channel block in the membranes of the sensory endings. The membrane potential of sensory endings appears to be highly dependent on sustained Ca 2+ conductance.

Effects of calcium on the discharge pattern of primary and secondary endings of isolated cat muscle spindles recorded under a ramp-and-hold stretch

The impulse activity of muscle spindles isolated from the cat tenuissimus muscle was investigated under varying concentrations of external calcium (Ca 2+). The outer capsule of the muscle spindle represents an effective diffusion barrier for Ca 2+ ions since activity changes were strong and rapid only if the capsule was partly removed from the sensory region of the receptor. The impulse activity of both primary and secondary muscle spindle endings was lowered by an increase in the external Ca 2+ concentration from 1.8 mM (normal Ringer’s solution) to 2.7 mM and raised by a decrease in the Ca 2+ concentration from 1.8 to 0.9 mM. Primary endings were generally more strongly affected than secondary endings. With primary endings the firing rate changed by 23–52% when the external Ca 2+ concentration was altered by 0.9 mM. With secondary endings the discharge frequency changed by 15–24%. The afferent discharge patterns were obtained under repetitive ramp-and-hold stretches and were analyzed with regard to influences of external Ca 2+ ions on the static and dynamic components of the endings’ responses. The stretch sensitivity and the adaptive response of both types of ending increased in the low Ca 2+ solution and decreased in the high Ca 2+ solution, but a specific effect on a single component of the responses to stretch was not observed. These findings indicate an overall change in excitability when the external Ca 2+ concentration was varied. The mechanical properties of the receptor were probably not affected since changes in the Ca 2+ concentration did not elicit a contraction or relaxation of the intrafusal muscle fibers. On the one hand, the observed effects can be explained according to the surface potential theory by an indirect influence of extracellular Ca 2+ ions on ion channels of the sensory nerve terminals, with Ca 2+ ions binding to negative charged sites at the endings’ outer membrane. On the other hand, the results are consistent with the supposition that Ca 2+ ions act directly on ion channels of the sensory membrane of muscle spindle endings.

Are the Hindwing Chordotonal Organs Elements of the Locust Flight Pattern Generator?

ABSTRACT Anatomical and electrophysiological techniques were used to examine the structure, central nervous connections and discharge patterns of afferents arising from the hindwing chordotonal organs in the locust, Locusta migratoria. The hindwing chordotonal organ afferents were found to be sensitive to low-frequency sounds (approx. 3 kHz) and to vibrations of the supporting surface. During flight in tethered animals these afferents were strongly activated. This flight-related activity was weakly modulated and the maximum occurred between depressor bursts. Low-frequency sound pulses were used to activate selectively the hindwing chordotonal organ afferents during rhythmic flight activity in deefferented preparations (all motor nerves cut). Phasic stimulation of the chordotonal organs, time-locked to every cycle, had no effect on the frequency of the centrally generated rhythm as recorded from proximal nerve stumps. Staining of single afferents from the hindwing chordotonal organ showed that they bifurcate in the metathoracic ganglion, with one branch terminating in the ring tract and the other branch projecting to the mesothoracic ganglion via the ipsilateral connective. None of the terminal processes of chordotonal afferents was observed to be located in dorsal neuropile regions containing the processes of flight neurones. Consistent with this finding, the chordotonal afferents were not observed to make synaptic connections to flight interneurones or motoneurones. The main conclusion of this investigation is that the hindwing chordotonal organs do not contribute to the patterning of motor activity for flight. The hindwing chordotonal organs probably function as detectors of vibration and perhaps low-frequency sound.

Are the hindwing chordotonal organs elements of the locust flight pattern generator

1. 1. Anatomical and electrophysiological techniques were used to examine the structure, central nervous connections and discharge patterns of afferents arising from the hindwing chordotonal organs in the locust, Locusta migratoria . 2. 2. The hindwing chordotonal organ afferents were found to be sensitive to lowfrequency sounds (approx. 3 kHz) and to vibrations of the supporting surface. During flight in tethered animals these afferents were strongly activated. This flight-related activity was weakly modulated and the maximum occurred between depressor bursts. 3. 3. Low-frequency sound pulses were used to activate selectively the hindwing chordotonal organ afferents during rhythmic flight activity in deefferented preparations (all motor nerves cut). Phasic stimulation of the chordotonal organs, time-locked to every cycle, had no effect on the frequency of the centrally generated rhythm as recorded from proximal nerve stumps. 4. 4. Staining of single afferents from the hindwing chordotonal organ showed that they bifurcate in the metathoracic ganglion, with one branch terminating in the ring tract and the other branch projecting to the mesothoracic ganglion via the ipsilateral connective. None of the terminal processes of chordotonal afferents was observed to be located in dorsal neuropile regions containing the processes of flight neurones. Consistent with this finding, the chordotonal afferents were not observed to make synaptic connections to flight interneurones or motoneurones. 5. 5. The main conclusion of this investigation is that the hindwing chordotonal organs do not contribute to the patterning of motor activity for flight. The hindwing chordotonal organs probably function as detectors of vibration and perhaps low-frequency sound.

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)

Noise cancellation in the electrosensory system of the thornback ray; common mode rejection of input produced by the animal's own ventilatory movement

1. The use of electroreception in feeding depends on the detection of the weak fields of the prey above the interference produced by the predator's own bioelectric fields. 2. In this study, the ray's ventilatory movements are shown to produce powerful modulation of electroreceptive afferent input. 3. The afferent discharge pattern results mainly from changes of the electric fields within the animal, since it is similar in afferents which innervate ampullary canals of opposite orientation. 4. If inputs from canals of opposite orientation are subtracted by the CNS, the sensitivity to external fields is enhanced, and the ventilatory interference removed by common mode rejection. 5. Recordings from secondary electrosensory neurons provide evidence that the appropriate inputs exist for common mode rejection, and that ventilation related activity is greatly reduced in these cells and virtually absent in recordings from a mesencephalic electrosensory area.

The regularity of muscle spindle discharge in man.

1. The variability of discharge of thirty-nine muscle spindle afferents from the pretibial muscles of normal human subjects was determined for spike train sequences recorded with the ankle joint fixed in 25 degrees plantar flexion, during further stretch and during graded voluntary contractions of the receptor-bearing muscle. 2. In non-contracting muscles with the ankle joint in 25 degrees plantar flexion, a sustained discharge was maintained by twenty-four of the thirty-nine endings. The mean discharge frequency for the active endings was 11.1 Hz (range 4.8--22.1 Hz), the mean coefficient of variation 0.073 (range 0.021--0.183). With further stretch, the discharge of endings maintaining frequencies below 10--12 Hz became more regular. For endings maintaining higher frequencies, changes in the coefficient of variation were small and occurred in either direction. All secondary endings maintained a highly regular discharge, but, at these frequencies, there was no statistically significant difference in the variability of primary and secondary endings. 3. It is considered that these findings are comparable to those of Matthews & Stein (1969) for de-efferented feline spindle endings, and support the view that there is no functionally effective background fusimotor drive to non-contracting muscles of normal human subjects. 4. A voluntary contraction sufficient to accelerate a spindle ending invariably decreased the regularity of its afferent discharge. During voluntary contractions, coefficients of variation up to 0.345 were recorded. However, coefficients as low as 0.1 were not uncommon, and thus the absence of fusimotor drive cannot necessarily be inferred from a regular afferent discharge pattern. 5. With contractions of different strength, the increase in the coefficient of variation did not parallel the increase in discharge frequency. It is concluded that not all fusimotor influences acting on a spindle ending are translated into variability, and that measurements of the variability of discharge do not accurately reflect the level of fusimotor drive. 6. The discharge frequency of some spindle endings decreased slightly in some contractions and this was accompanied by an increase in the variability of discharge. It is suggested that contracting extrafusal muscle fibres can modulate the discharge pattern of spindle endings and contribute to the variability of discharge during a voluntary contraction. 7. In contracting muscles the irregular fusimotor-driven spindle discharge contained a 'hidden' periodicity, but this was not as extensive as has been reported for the cat. No such periodicity could be demonstrated for spindle endings in non-contracting human muscles.

Modification by lidocaine of the discharges of primary endings of muscle spindles in cat tenuissimus muscle

The effects of lidocaine (1–20 μ/ml) on afferent discharge patterns of primary endings of muscle spindles in cat tenuissimus muscle were investigated. Discharge from the endings, recorded in Ia afferent axons, was evoked by ramp stretch of the muscle, stimulation of single static or dynamic fusimotor axons or by a combination of stretch and fusimotor stimulation. Spontaneous discharge of the endings at the initial length of the muscles was reduced by 2–5 μg/ml and abolished by 10–15 μg/ml lidocaine. The static but not the dynamic discharge elicited by muscle stretch was blocked by concentrations of 10–15 μg/ml. The same concentrations abolished static adn dynamic fusimotor influences on primary ending discharge. However, in one experiment where the spindle was microscopically observed, fusimotor stimulation still resulted in contraction of the intrafusal muscle even when fusimotor stimulation failed to elicit changes in discharge response patterns of the primary endings. These findings indicate that lidocaine interferes with the encoding mechanism prior to block of impulse conduction in either the fusimotor or afferent axons.

The afferent discharge pattern of atrial mechanoreceptors in the cat during sinusoidal stretch of atrial strips in situ.

1. The differences in spike discharge from atrial mechanoreceptors in vivo suggest the existence of different receptor types. To test this possibility, and to see how atrial receptors compare with other mechanoreceptors, their response was studied under comparable stimulus conditions.2. Sinusoidal length changes, with frequencies from 1 to 10 Hz and amplitudes of 1.5-5.0 mm at a given static extension, were imposed in situ on strips of atrial receptor areas of cats.3. The receptor response was evaluated from functional single fibres in terms of number of spikes per stimulus period, average discharge rate, instantaneous spike frequency, and phase angle between forcing function and instantaneous frequency.4. Irrespective of the fibre type, atrial fibres appear to originate from identical mechanoreceptors which sense length at low stimulus frequency and low stimulus amplitudes, but also sense velocity in the high frequency range and with large stimulus amplitudes.5. The difference in the discharge pattern and in the functional behaviour of the atrial fibres in vivo can be explained on the basis of identical receptors.6. The difference in the temporal occurrence of the atrial burst is still open to debate, but probably is related to the site of the receptor.

Studies on the blood pressure-sensitive receptors in the rabbit kidney in vivo.

1) Spontaneous afferent discharges were recorded from nerve fibers dissected from the renal nerves in vivo.2) Raising the systemic blood pressure by mechanical and chemical means caused an increase in the discharge rate. It decreased with a reduction in the systemic blood pressure by mechanical or reflex means.3) The time course of the change in the discharge rate has a strong resemblance to that of the systemic blood pressure.4) The afferent discharge rate was approximately proportional to the systemic blood pressure levels.5) The afferent discharge pattern was irregular and asynchronous with the heartbeat.6) It is concluded that these renal receptors send information about blood pressure levels in the renal artery to the central nervous system.

Muscle afferents of trigeminal mesencephalic tract nucleus and mastication in chronic monkeys.

The nature of masticatory movement and related muscle spindle afferent activity was studied on awake monkeys. The pressure acting on the molar surface of the tooth and masseter EMG may develop in two phases, i. e. an early jaw movement and a late biting. Out of 20 identified spindle afferents, 10 units in ten monkeys showed a rate increase during jaw-muscle closing and the remaining 10 units showed a decrease of the rate. Although there were two phases to the masseter contraction, no correlation was found between the two phases and the spindle afferent discharge pattern. It was concluded that during voluntary jaw closing the fusimotor activation occurred simultaneously with masseter muscle activation.

Afferent discharges from arterial mechanoreceptors in the kidney of the rabbit

1. Afferent discharges were observed in dissected filaments or single nerve fibres of renal nerves in the rabbit.2. Increasing the arterial perfusion pressure in excised kidney preparations caused an increase in afferent discharge rate. Increasing the venous pressure was without effect. Receptor discharge patterns were compatible with those of the slowly adapting type.3. In vivo, increasing the systemic blood pressure by means of the sinus reflex caused an increase in afferent discharge rate. Afferent discharge patterns showed no synchronicity with heart beat, irrespective of the blood pressure levels.4. It is suggested that mechanoreceptors are present around the arterial walls in the kidney and that they send information about blood pressure levels in the renal artery to the central nervous system.