Phasic and tonic modulation of impulse rates in gamma-motoneurons during locomotion in premammillary cats

149

129

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.

Section: Discussionsupporting

confidence: 88%

Ensemble firing of muscle afferents recorded during normal locomotion in cats

Procházka

Gorassini

1998

149

129

“…In contrast, the dynamic sensitivity of gastrocnemius (total = 14; Cabelguen, 1981) and soleus (total = 21; Taylor et al 1985) Ia afferents consistently exhibited large increases during homonymous muscle contraction under the influence, in the latter case, of coactivated dynamic y-efferents (Murphy et al 1984) whose modulation (mean, 23 impulses/s) was similar to that of TA phasic units in the present study (mean, 21 impulses/s). The increase in dynamic sensitivity of soleus Ia afferents is particularly striking since it occurred against a background level of static y-efferent activity (mean, 51 impulses/s; Murphy et al 1984) that is considerably higher than the mean rate during walking of TA tonic units (18 5 impulses/s). Thus with the assumptions, which are not unreasonable (Cabelguen 1979(Cabelguen , 1981, that ankle flexor and extensor I a afferents are influenced through similar degrees of spindle innervation by static and dynamic y-efferents and have similar sensitivities to these inputs, not only is a direct equivalence between phasic/tonic and dynamic/static yefferents, respectively, unlikely but, since TA Ia afferents consistently showed a decrease in dynamic sensitivity during muscle contraction (Cabelguen, 1981), it is y-JIOTONE,TUROANTE DISCHARGE DUtRLVG LOCOMOTION probable that few, if any, of their dynamic y-efferents, one or two of which are the general supply to a spindle (Boyd, 1980), corresponded to phasic units.…”

Section: P R Murphy and G R Haimond Discussioncontrasting

confidence: 50%

“…In marked contrast, resting y firing is high in ankle extensor nerves in the same preparation (Murphy et al 1984). During (16) were phasically recruited with homonymous ENG activity, while the remainder (5) were tonically active throughout the step cycle ( Fig.…”

Section: Resultsmentioning

confidence: 91%

The locomotor discharge characteristics of ankle flexor gamma‐motoneurones in the decerebrate cat.

Murphy

Hammond

1993

SUMMARY1. The discharge patterns of ankle flex.or, tibialis anterior (TA), y-motoneurones were recorded during locomotion in the decerebrate cat.2. At rest y-efferents had no background discharge. During locomotion two patterns of y activity could be distinguished. Most units (16) were phasically recruited with homonymous electroneurogram (ENG) activity, while the remainder (5) were tonically active throughout the step cycle.3. The modulation of phasic units was greater (P < 001) than tonic neurones. Phasic units had lower (P < 0-02) mean, but higher (P < 0-01) peak, rates during the step cycle.4. The discharge rate of both types of efferent increased around the onset of ENG activity and peaked during ENG activity, or shortly after its cessation. The conduction velocities of phasic and tonic units overlapped widely.5. It is proposed, on the basis of muscle spindle afferent recordings during locomotion, that TA phasic and tonic units correspond to static and dynamic ymotoneurones, respectively. This correspondence is functionally advantageous for the role of ankle flexor muscles during locomotion. Thus phasic static y discharge during flexion would aid muscle contraction via increased I a afferent activity, while tonic dynamic y firing would enhance I a afferent stretch sensitivity throughout the step cycle. Such enhancement during flexion would oppose unexpected muscle lengthening while, during extension, it would contribute to reciprocal inhibition of ankle extensor muscles.6. The results are discussed in relation to strategies of y usage during rhythmic movements. It is postulated that, for such behaviour, muscle contraction is accompanied by coactivity in static and dynamic y-motoneurones. A functional rationale is suggested for this strategy.

“…Some of the earliest observations of spindle discharge in hindlimb and forelimb muscles in decerebrate animals (Perret & Busser, 1972;Perret & Berthoz, 1973) strongly suggested the presence of static fusimotor modulation in parallel with á_activity. Later, more detailed studies involving recording from hindlimb extensor ã-axons (Murphy, 1982;Murphy et al 1984;Murphy & Hammond, 1990) or spindles (Taylor, Stein & Murphy, 1985;Bennett, De Serres & Stein, 1996) have supported the idea that one group of ã_motoneurones fires tonically whilst another group fires in a modulated fashion, but identified the latter as dynamic. Evidence from chronic recordings from cat hindlimb spindles has been interpreted as indicating that the observed behaviour could be explained by essentially tonic levels of static and dynamic fusimotor firing, though with the possibility of some additional static modulation approximately in parallel with á-activity (Prochazka et al 1987).…”

Section: Discussionmentioning

confidence: 99%

“…Thus, in alert locomoting cats, Prochazka, Hulliger, Trend & Durmuller (1987) could explain the recorded spindle afferent firing on the basis of purely tonic levels of static and dynamic firing with no modulation. On the other hand, from observations in the high decerebrate locomoting cat it was deduced that static fusimotor firing was maintained at a tonic level while dynamic discharge was strongly modulated (Murphy, Stein & Taylor, 1984). Human microneurography has indicated changes in fusimotor activity during limb movements, but these changes have not been specified as static or dynamic (Vallbo, 1985;Ribot, Roll & Vedel, 1986).…”

mentioning

confidence: 99%

Fusimotor Influence on Jaw Muscle Spindle Activity during Swallowing‐Related Movements in the Cat

Taylor

Hidaka

Durbaba

et al. 1997

The activity patterns of muscle spindle afferents in jaw‐closer muscles were studied during reflex swallowing movements in anaesthetized cats. Simultaneous records were made of the electromyogram (EMG) in masseter and anterior digastric muscles and of the unloaded jaw movements. The underlying patterns of fusimotor activity were deduced by comparing afferent discharges occurring during active swallowing with those occurring when exactly the same movements were imposed passively. The interpretation of spindle behaviour was greatly facilitated by characterizing the afferents according to the evidence for their contact with the various intrafusal muscle fibres, derived from testing with succinylcholine. It was also valuable to have two different types of afferent recorded simultaneously. There was clear evidence of fusimotor activity occurring during active jaw closing so as to oppose the spindle silencing. This effect was most marked in b2c‐type afferents (probably secondaries) and was therefore attributed to a modulation of static fusimotor discharge approximately in parallel with α‐activity. Afferents with evidence of bag1 fibre contacts (primaries) showed much greater sensitivity to muscle lengthening during active movement than when the movement was imposed. This difference was exaggerated when anaesthesia was deepened for the passive movements. This was interpreted as evidence for a higher level of dynamic fusimotor activity maintained during active movements than at rest. The results support the view that for a variety of active jaw movements, static fusimotor neurone firing is modulated roughly in parallel with α‐activity but leading it so as to counteract spindle unloading. Dynamic fusimotor neurone firing appears to be set at a raised level during active movements. Anaesthesia appears to depress activity in the α‐motoneurones more than in γ‐motoneurones.