Summing responses of cat soleus muscle spindles to combined static and dynamic fusimotor stimulation

This is a study of the summation of responses of primary endings of muscle spindles to combined static and dynamic fusimotor stimulation in the soleus muscle of the anaesthetised cat. Summation, expressed as a summation coefficient, K, was measured under a variety of conditions including (1) at several, fixed muscle lengths using steady rates of stimulation, (2) using ramp-shaped increases in stimulation rates, (3) during passive stretches after muscle conditioning, and (4) during combined stretch plus stimulation. The predominant effect observed was occlusion, that is, the combined response was less than the sum of the two individual responses. The calculated mean K value for responses at fixed length was 0.156 (±0.005 S.E.M.). It was hypothesised that summation arose from electrotonic spread of generator current between the afferent terminals, either directly, or as a result of mechanical interactions between the contracting intrafusal fibres. Summation for responses from pairs of static fusimotor fibres gave a larger mean K value, 0.340 (±0.020 S.E.M.). These findings were interpreted in terms of a model of the muscle spindle where responses to dynamic fusimotor stimulation arise at one impulse generating site, and static fusimotor responses arise at another.     

Summation of responses of cat muscle spindles to combined static and dynamic fusimotor stimulation

This is a study of the process of interaction between the responses of muscle spindles to stimulation of two fusimotor fibres. Combined stimulation of a static and a dynamic fusimotor fibre supplying the same muscle spindle in the soleus muscle of the anaesthetised cat gave a response which was larger than from stimulating each fibre separately, but less than their sum. A similar summation process was observed with pairs of static fusimotor fibres. The mean summation coefficient for the responses to stimulation of 14 pairs of static fusimotor fibres was 0.29 (range 0.14–0.52; S.D. 0.09), while for 42 static:dynamic pairs it was 0.30 (range 0.07–0.89; S.D. 0.20). Mechanisms considered for the summation process were probabilistic mixing of impulse traffic from two or more impulse generators within the terminals of the primary ending of the spindle, the spread of generator current from one encoding site to another and mechanical interactions between contracting intrafusal fibres. In an experiment where single static and dynamic fusimotor fibres were stimulated together, and then stimulation of the static fibre stopped, the size of the continuing dynamic response was larger than when the dynamic fibre had been stimulated alone. This finding suggested some kind of mechanical interaction between the contracting intrafusal fibres and implies that static and dynamic fusimotor effects within a spindle cannot be considered to be entirely independent of one another.     

Intermittent stimulation of fusimotor fibres during slow stretch of muscle spindles in the cat

Responses of muscle spindles of the peroneus tertius muscle of the cat were recorded during intermittent fusimotor stimulation, applied during slow stretch, after muscle conditioning by stimulation of the nerve at the test length or at a length 2.5 mm longer. Some static and all dynamic axons evoked afferent bursts whose amplitude was relatively independent of the level of stretch response. Other static axons produced bursts that grew in size with the stretch.     

The responses of muscle spindles to small, slow movements in passive muscle and during fusimotor activity

We have previously shown that movement detection thresholds at the human elbow joint were less than a degree of joint rotation in the passive limb but were higher if they were measured while subjects co-contracted elbow muscles [A.K. Wise, J.E. Gregory, U. Proske, J. Physiol., 508 (1998) 325-330]. Here we report observations on the responses of muscle spindles of the soleus muscle of the anaesthetised cat to determine their ability to signal small length changes in the passive muscle and during a contraction, under conditions resembling those of the human experiments. After appropriate conditioning of the muscle to control for history effects, primary endings of muscle spindles showed thresholds to ramp stretch at 20 micrometers s-1 of between less than 5 micrometers and 15 micrometers, which translates to 0.05 degrees -0.15 degrees of human elbow joint rotation. Thresholds were much higher following conditioning to introduce slack in the muscle. Since during a voluntary contraction there is likely to be alpha:gamma co-activation, responses of spindles were also recorded during slow stretches (100 micrometers at 20 micrometers s-1) during static fusimotor stimulation, dynamic fusimotor stimulation, combined fusimotor stimulation and fusimotor plus skeletomotor stimulation. Invariably, responses to passive stretch were larger than during motor stimulation. It is concluded that spindles are sensitive enough to signal fractions of a degree of elbow joint rotation and that the rise in threshold observed during a voluntary contraction may be accounted for by the actions of fusimotor and skeletomotor axons on spindle stretch responses.     

Re-afferent effects of individual static and dynamic gamma-stimuli during maintained fusimotor stimulation

The ability of maintained dynamic and static fusimotor stimulation to modulate the primary afferent response of the muscle spindle in the rhythm of gamma-stimulation was investigated using a highly sensitive method for modulation detection. The effect of 41 gamma-fibers (13 dynamic; 28 static) on 38 primary afferents obtained from the tibialis anterior muscle of the cat was studied. It was found that maintained stimulation of 10 out of the 13 dynamic (77%) and of 25 out of the 28 static (89%) gamma-fibers could evoke significant modulations of the primary afferent response in the rhythm of fusimotor stimulation at a minimum of one stimulation rate. Moreover, both static and dynamic gamma-stimulations could evoke significant primary afferent modulations almost over the entire range of stimulation rates studied (30-300 stimuli per second). These results show that both gamma-systems can modulate the primary afferent response in the rhythm of fusimotor stimulation over a wide range of stimulation rates; thus the central nervous system may be provided with re-afferent information about the effect of each individual gamma-motoneuron discharge. Some hypotheses for the internal spindle mechanism responsible for the afferent modulations are discussed.     

Re-afferent effects of individual static and dynamic γ-stimuli during maintained fusimotor stimulation

The ability of maintained dynamic and static fusimotor stimulation to modulate the primary afferent response of the muscle spindle in the rhythm of γ-stimulation was investigated using a highly sensitive method for modulation detection. The effect of 41 γ-fibers (13 dynamic; 28 static) on 38 primary afferents obtained from the tibialis anterior muscle of the cat was studied. It was found that maintained stimulation of 10 out of the 13 dynamic (77%) and of 25 out of the 28 static (89%) γ-fibers could evoke significant modulations of the primary afferent response in the rhythm of fusimotor stimulation at a minimum of one stimulation rate. Moreover, both static and dynamic γ-stimulations could evoke significant primary afferent modulations almost over the entire range of stimulation rates studied (30–300 stimuli per second). These results show that both γ-systems can modulate the primary afferent response in the rhythm of fusimotor stimulation over a wide range of stimulation rates; thus the central nervous system may be provided with re-afferent information about the effect of each individual γ-motoneuron discharge. Some hypotheses for the internal spindle mechanism responsible for the afferent modulations are discussed.     

Histological identification of (static) skeletofusimotor innervation to a cat muscle spindle

Two skeletofusimotor (β) axons were identified histologically in cat tenuissimus muscle. The axons supplied the distal poles of 3 intrafusal muscle fibers of the nuclear chain type and two extrafusal fibers of the fast twitch type. The observations strengthen the case for the existence of static β-innervation to cat muscle spindles.     

Effects of slow muscle stretch on the responses of primary and secondary endings to small amplitude periodic stretches in de-efferented soleus muscle spindles

The responses of primary and secondary endings of de-efferented soleus spindles to small amplitude periodic stretches superimposed on slow ramp stretches have been studied. For primary endings, the responses become progressively larger especially during the last period of the ramp whereas for secondary endings, after an initial period of moderate growth, the amplitude of the responses display a relative reduction precisely when the responses of the primary endings are the largest. These differences can be interpreted in terms of progressive increase in stiffness of the striated polar portions of the intrafusal muscle fibers.     

Static and dynamic fusimotor interaction and the possibility of multiple pace-makers operating in the cat muscle spindle

The interaction of static and dynamic fusimotor activation on the firing of primary muscle spindle afferents has been studied in the cat soleus muscle at constant length and during sinusoidal stretching. Cycle histogram analysis revealed summation of static and dynamic action during the peak of the afferent response to sinusoidal stretching, while static action completely occluded the dynamic effect during the trough of the response. Occlusion was complete as long as, for single fusimotor activation, the static-induced trough response exceeded the dynamic-induced one by about 25%. The investigation of inter-spike interval distributions obtained at constant muscle length revealed occlusion of dynamic by static action in 8 out of 13 cases. A model of multiple spike generation in primary spindle afferents is considered which is based on two or more pacemakers arranged in parallel, with a common pacemaker in series.     

Retractor bulbi muscle responses to oculomotor nerve and nucleus stimulation in the cat

This study demonstratesthe presence of retractor bulbi motoneurons within the oculomotor nucleus which activate muscle units within all 4 slips of the cat retractor bulbi muscle. These muscle units are mechanically different and physiologically separate from retractor bulbi muscle units innervated by the abducens nerve. The retractor bulbi muscle, then, is innervated by two separate pools of motoneurons whose axons are carried in two different cranial nerves. These observations of mechanical properties of retractor bulbi muscle suggest that the oculomotor retractor bulbi motor units may be activated during patterned eye movements.     

Responses of snake muscle spindles to mechanical and electrical stimulation.

Responses of the sensory ending of snake muscle spindle to mechanical and electrical stimulation were examined. In the short-capsule spindle the dynamic index increases more rapidly with increase in initial muscle length. The threshold muscle length for initiating a long sustained discharge from the short-capsule spindle is significantly higher than that for the long-capsule spindle while the position sensitivity is similar in the two types of spindle. The relation between rate of discharge of the ending and current applied to the impulse initiating site was found to be similar in both types of spindle.     

The cat step cycle; responses of muscle spindles and tendon organs to passive stretch within the locomotor range

To assess the extent to which muscle afferent discharge might assist in the control of stepping we have recorded firing patterns of a representative number of spindle and tendon organ afferents from isolated soleus and gastrocnemius muscles in anesthetized cats while subjecting these muscles to ‘locomotor’ range stretches as established in a previous study^9,10. Attention was directed to passive stretches with particular emphasis on simulation of the F component of the swing phase of stepping which stretch is presumable unaccompanied by fusimotor input to the spindles. The data reveal the value of using physiological range stretches for bringing out: (1) the acceleration (or ‘acceleration-like’) and displacement sensitivity of Ia afferents in addition to the generally accepted rate sensitivity; (2) the rate sensitivity of group II afferents in addition to the generally accepted displacement sensitivity; and (3) the passive stretch responsiveness of Ib afferents in addition to the now accepted much greater sensitivity to active contractile forces. The low passive stretch responsiveness of muscle spindles and tendon organs encountered by Severin et al.³³ during controlled walking of the high decerebrate cat is shown to be not attributable to an inadequate extent, range and rate of stretch during the F phase of the step. There is suggestion that feeble F phase firing could results from visco-elastic effects attributable to rhythmic alpha and gamma motoneuron discharge during the repetitive stretch-shorten cycles of locomotion and to the prior activity of each receptor type in the immediately preceding stance phase of the step. The data are also shown to have relevance for the active stretch of the E² component of the stance phase of stepping and emphasize the extent to which co-activation of Ia, group II and Ib afferents would occur during this lengthening contraction phase of the step.     

Observations on static and dynamic responses of muscle stretch receptors in kittens

In 5-19-day-old kittens anesthetized with Saffan, the discharges of de-efferented triceps surae muscle receptors were recorded from afferent fibers in dorsal root filaments. The conduction velocities of the afferent fibers ranged between 7 and 30 m/s. Receptors were identified as spindles on the basis of their response to muscle stretch and, whenever possible, the pause in their discharge during muscle contraction. Spindles responding with sustained discharges to muscle extensions of less than 1 mm could be found in 5-8-day-old kittens, provided the muscles was left 'in situ', with intact skin, tendon and aponeuroses. However, such responses were rare before 10 days, and the majority of receptors essentially displayed phasic responses to muscle stretch, in agreement with previous observations. In responses to sinusoidal muscle stretching of 0.1-0.5-mm amplitude, kitten receptors were easily driven to discharge one impulse per cycle at frequencies of 10-15 Hz. But unlike adult spindles, they could not follow higher frequencies unless the amplitude of stretch was increased. The maturation of dynamic responses is slower than that of static responses in kitten spindles. In the first postnatal weeks, small changes in muscle length are poorly signaled to the central nervous system.     

Discharge rate and reflex responses of fusimotor neurons during muscle ischemia

Reflex effects of muscle ischemia on fusimotor neurons were investigated in decerebrate cats. Nerve impulses of single fusimotor neurons were recorded from filaments cut out of otherwise intact nerves to triceps surae muscles. Muscle ischemia was induced by clamping a. and v. femoralis. Fusimotor discharge rate was counted before, during, and after ischemia of both resting and contracting muscles. Muscle contractions were induced either by direct electrical stimulation or reflexly by muscle stretch. No changes were found in either the mean discharge rate or in the reflex response of fusimotor neurons to muscle stretches and contractions during muscle ischemia. It could be concluded that group III and IV muscle afferent fibers, responding to contractions of the ischemic muscle, have no reflex effects on fusimotor neurons. It also does not seem probable that fusimotor neurons contribute to ischemic muscular cramps.     

Lack of summation of dynamic and static components in the responses of cat tendon organs

Discharges of single tendon organs of cat peroneus tertius muscle were recorded during tetanic contractions of motor units. On combined stimulation of several motor units activating the same tendon organ, the static components of responses sum, although not linearly, whereas the dynamic component of a response superimposed on a pre-existing discharge does not sum at all with this discharge.     

Response characteristics and classification of muscle spindles of the masseter muscle in the cat

For the classification of primary and secondary spindle endings in jaw-closing muscles, the relationship between physiologic properties of these endings and conduction velocities of their afferent fibers was analyzed. Unitary discharges of afferent fibers from masseter muscle spindles were recorded in themesencephalic trigeminal nucleus (Mes V) by microelectrodes. Conduction velocities of masseter spindle units in the Mes V showed a bimodal distribution with the division at 36 m/s. The units conducting at more than 54 m/s and those conducting less than 36 m/s were categorized as the primary and secondary endings, respectively, on the basis of their responses to muscle stretches, vibratory stimuli, and to suxamethonium (SCh) administration (200 μg/kg, i.v.). On the other hand, spindle units conducting at between 36 and 54 m/s, which were designated as the intermediate spindle unit, showed a great variety in their responses to the same stimuli. In addition, the number of intermediate spindle units was about twice as large as that of the well-defined units. Because the spindle units in the Mes V were rather clearly divied into two groups on the basis of their sensitivity to vibration and to SCh irrespective of their conduction velocities, the intermediate spindle units may effectively be categorized on the same basis. There are several possible reasons to account for the high proportion of intermediate spindles.