‘Fusimotor set’: new evidence for α-independent control of γ-motoneurones during movement in the awake cat

Procházka, A.; Hulliger, M.; Zangger, P.; Appenteng, Kwabena

doi:10.1016/0006-8993(85)90632-8

Cited by 214 publications

(99 citation statements)

References 9 publications

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“…Though the estimates are rather crude, the amount of á-linked ã action implied by the present analysis of the triceps surae spindle primary data certainly seems larger than previously proposed in publications from this laboratory (e.g. Prochazka, Hulliger, Zangger & Appenteng, 1985;Prochazka, 1996). From the perspective of biomechanical modelling, the EMGlinked components of spindle secondary firing did not cause major errors in predictions of spindle secondary firing from the length signals alone.…”

Section: Discussioncontrasting

confidence: 60%

Ensemble firing of muscle afferents recorded during normal locomotion in cats

Procházka

Gorassini

1998

The Journal of Physiology

152

129

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The main purpose of this study was to collate population data on the firing characteristics of muscle afferents recorded chronically during normal stepping in cats. Ensemble firing profiles of forty‐seven muscle spindle and tendon organ afferents were compiled from stored data. The relationships between the firing profiles and the displacement and force signals were analysed with the help of mathematical models of the response characteristics of spindle primary and secondary afferents and tendon organs. Whereas the firing of hamstring spindle afferents could be predicted with reasonable accuracy from the length and velocity signals alone, the firing profiles of triceps surae spindle afferents deviated from the predicted profiles, particularly during electromyogram (EMG) activity. This indicated that the components of fusimotor action linked to extrafusal muscle activity were significant in triceps surae, possibly because this muscle is more strongly recruited in the cat step cycle. From the limited data available, it was not possible to identify the ‘best’ or most general mathematical function to predict spindle secondary firing. In the two triceps surae spindle secondary units studied, firing was well predicted by using the simplest possible model, rate proportional to displacement, whereas in the hamstring spindle secondary data, a more complex linear transfer function was needed. The results of modelling the spindle secondary data were consistent with a modest amount of phasic, static fusimotor action linked to EMG activity. The averaged ensemble of tendon organ afferent activity from the triceps surae gave predictions of whole‐muscle force that agreed well with separate triceps force measurements in normal cat locomotion. This supports the idea that ensembles of tendon organ afferents signal whole‐muscle force. Our overall conclusion is that to a first approximation, large muscle afferents in the cat hindlimb signal muscle velocity, muscle length and muscle force, at least in movements of the speed and amplitude seen in locomotion.

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Section: Discussioncontrasting

confidence: 60%

Ensemble firing of muscle afferents recorded during normal locomotion in cats

Procházka

Gorassini

1998

The Journal of Physiology

152

129

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“…This suggests that, when exposed to an unstable environment, the gain of the supraspinal projec-tions of the Ia afferent feedback must be maintained, if the gain of this input at the spinal level decreases. Interestingly, it has been suggested that the gamma drive increases in unstable conditions to increase the gain of the Ia input to supraspinal centers (presumably increasing the resolution of the error signal), while the synaptic gain at the spinal level is reduced (Llewellyn et al 1990;Prochazka et al 1985). The present study, however, focused on the interplay between the Ia feedback at the spinal level and the steadiness of the motor output.…”

Section: Discussionmentioning

confidence: 85%

The optimal neural strategy for a stable motor task requires a compromise between level of muscle cocontraction and synaptic gain of afferent feedback

Dideriksen

Negro

Farina

2015

Journal of Neurophysiology

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Dideriksen JL, Negro F, Farina D. The optimal neural strategy for a stable motor task requires a compromise between level of muscle cocontraction and synaptic gain of afferent feedback. J Neurophysiol 114: 1895-1911, 2015. First published July 22, 2015 doi:10.1152/jn.00247.2015.-Increasing joint stiffness by cocontraction of antagonist muscles and compensatory reflexes are neural strategies to minimize the impact of unexpected perturbations on movement. Combining these strategies, however, may compromise steadiness, as elements of the afferent input to motor pools innervating antagonist muscles are inherently negatively correlated. Consequently, a high afferent gain and active contractions of both muscles may imply negatively correlated neural drives to the muscles and thus an unstable limb position. This hypothesis was systematically explored with a novel computational model of the peripheral nervous system and the mechanics of one limb. Two populations of motor neurons received synaptic input from descending drive, spinal interneurons, and afferent feedback. Muscle force, simulated based on motor unit activity, determined limb movement that gave rise to afferent feedback from muscle spindles and Golgi tendon organs. The results indicated that optimal steadiness was achieved with low synaptic gain of the afferent feedback. High afferent gains during cocontraction implied increased levels of common drive in the motor neuron outputs, which were negatively correlated across the two populations, constraining instability of the limb. Increasing the force acting on the joint and the afferent gain both effectively minimized the impact of an external perturbation, and suboptimal adjustment of the afferent gain could be compensated by muscle cocontraction. These observations show that selection of the strategy for a given contraction implies a compromise between steadiness and effectiveness of compensations to perturbations. This indicates that a task-dependent selection of neural strategy for steadiness is necessary when acting in different environments.

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“…However, the available data were inconsistent with regard to the time course of the imposed movements. Furthermore, it was clear from the very high firing rates evoked that imposed movements were associated with high levels of dynamic fusimotor action as previously verified in acute experiments (Prochazka, Hulliger, Zangger & Appenteng, 1985). We therefore opted to compare responses of the models with profiles synthesized on the basis of parameters obtained from the literature.…”

Section: Resultsmentioning

confidence: 92%

Models of ensemble firing of muscle spindle afferents recorded during normal locomotion in cats

Procházka

Gorassini

1998

The Journal of Physiology

145

146

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In spite of many years of research there is still much uncertainty regarding the nature of proprioceptive signals and the role of these signals in kinaesthesia and movement control. The uncertainty mainly concerns the firing characteristics of the most numerous proprioceptors, the muscle spindles. From many studies in anaesthetized animals it is known that mammalian muscle spindle afferents respond to muscle displacement and velocity and that these responses are strongly modulated by ã_fusimotor activity emanating from the central nervous system. Fusimotor action not only increases the firing rate of spindle afferents at a given muscle length ('bias'), it also controls the sensitivity of the afferents to changes in muscle length ('gain'). Just how the mammalian nervous system controls fusimotor action in daily life remains the subject of controversy (for review, see Prochazka, 1996). The firing rate of muscle spindles can also be affected by mechanical factors such as tendon strain, changes in pennation angle, Journal of Physiology (1998) 1. The aim of this work was to compare the ability of several mathematical models to predict the firing characteristics of muscle spindle primary afferents recorded chronically during normal stepping in cats. 2. Ensemble firing profiles of nine hamstring spindle primary (presumed group Ia) afferents were compiled from stored data from 132 step cycles. Three sets of profiles corresponding to slow, medium and fast steps were generated by averaging groups of step cycles aligned to peak muscle length in each cycle. 3. Five models obtained from the literature were compared. Each of these models was used to predict the spindle firing profiles from the averaged muscle length signals. The models were also used in the reverse direction, namely to predict muscle length from the firing profiles. A sixth model incorporating some key aspects of the other models was also included in the comparisons. 4. Five of the models predicted spindle firing well, with root mean square (r.m.s.) errors lower than 14% of the modulation depth of the target profiles. The key variable in achieving good predictions was muscle velocity, the best fits being obtained with power-law functions of velocity, with an exponent of 0·5 or 0·6 (i.e. spindle firing rate is approximately proportional to the square root of muscle velocity). The fits were slightly improved by adding small components of EMG signal to mimic fusimotor action linked to muscle activation. The modest relative size of EMG-linked fusimotor action may be related to the fact that hamstring muscles are not strongly recruited in stepping. 5. Length was predicted very accurately from firing profiles with the inverse of the above models, indicating that the nervous system could in principle process spindle firing in a relatively simple way to give accurate information on muscle length. 6. The responses of the models to standard ramp-and-hold displacements at 10 mm s¢ were also studied (i.e. velocities that were an order of magnitude lower than that during ...

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‘Fusimotor set’: new evidence for α-independent control of γ-motoneurones during movement in the awake cat

Cited by 214 publications

References 9 publications

Ensemble firing of muscle afferents recorded during normal locomotion in cats

Ensemble firing of muscle afferents recorded during normal locomotion in cats

The optimal neural strategy for a stable motor task requires a compromise between level of muscle cocontraction and synaptic gain of afferent feedback

Models of ensemble firing of muscle spindle afferents recorded during normal locomotion in cats

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