R. Durbaba

Distinctive patterns of static and dynamic gamma motor activity during locomotion in the decerebrate cat

1 Simultaneous recordings were made from gamma (γ) motor axons and from muscle spindle afferents of the medial gastrocnemius (MG) muscle during locomotion in decerebrate cats. The γ‐neurons were identified as static or dynamic (γs or γd) by correlating their behaviour during midbrain stimulation with changes in muscle spindle afferent responses to muscle stretch. 2 On the basis of their behaviour during locomotion, γs neurons could be divided into two groups. One group (type‐1) showed strongly and smoothly modulated discharge increasing in parallel with the active muscle shortening in ankle extension, but with phase advance. The other group (type‐2) also showed a modulated pattern, but with increased firing centred on the flexion phase. The proportions of the two were 13 type‐1 and 7 type‐2. 3 The type‐1 firing pattern accurately predicted the difference in firing frequency for secondary afferents obtained by subtracting from the recordings made during active movements the response of the same units to the movements repeated passively in the absence of fusimotor activity. 4 The type‐2 pattern also became consistent with the difference signal, when operated on by a phase lag appropriate to the effects of bag2 intrafusal fibres. These results suggest that there may be some degree of separate control of chain and bag2 intrafusal fibres. 5 The discharge of γd axons was also found to fluctuate with the locomotor cycle, with a pattern very distinct from that of the γs records. The γd firing frequency rose very suddenly from zero to a maximum at the onset of muscle shortening and continued into the beginning of lengthening. The term ‘interrupted’ discharge is suggested as a useful description. The timing of this discharge was shown to be appropriate for sensitising the primary afferents to detect the onset of stretch.

Patterns of fusimotor activity during locomotion in the decerebrate cat deduced from recordings from hindlimb muscle spindles.

Recordings have been made from multiple single muscle spindle afferents from medial gastrocnemius (MG) and tibialis anterior (TA) muscles of one hindlimb in decerebrate cats, together with ankle rotation and EMG signals, during treadmill locomotion. Whilst the other three limbs walked freely, the experimental limb was denervated except for the nerves to MG and TA and secured so that it could rotate only at the ankle joint, without any external load. Each afferent was characterised by succinylcholine testing with regard to its intrafusal fibre contacts. Active movements were recorded and then replayed through a servo mechanism to reproduce the muscle length changes passively after using a barbiturate to suppress γ‐motor firing. The difference in secondary afferent firing obtained by subtracting the discharge during passive movements from that during active movements was taken to represent the profile of static fusimotor activity. This indicated an increase before the onset of movement followed by a strongly modulated discharge in parallel with muscle shortening during locomotion. The pattern of static firing matched the pattern of unloaded muscle shortening very closely in the case of TA and with some phase advance in the case of MG. The same effects were observed in primary afferents. Primary afferents with bag1 (b1) contacts in addition showed higher firing frequencies during muscle lengthening in active than in passive movements. This indicated increased dynamic fusimotor firing during active locomotion. There was no evidence as to whether this fluctuated during the movement cycles. When the mean active minus passive difference profile of firing in bag2‐chain (b2c) type primary afferents was subtracted from that for b1b2c afferents, the difference was dominated by a peak centred on the moment of maximum lengthening velocity (v). The component of the active minus passive difference firing due to b1 fibre contacts could be modelled by f(t)=av (where a is a constant) during lengthening and by f(t)= 0.2av during shortening. The remainder of the difference signal matched the predictions of the static fusimotor signal derived from secondary afferents. The findings are discussed in relation to the concept that the modulated static fusimotor pattern may represent a ‘temporal template’ of the expected movement, though the relationship of the results to locomotion in the intact animal will require further investigation. The analysis of the data indicates that the combined action of muscle length changes and static and dynamic fusimotor activity to determine primary afferent firing can be understood in terms of the interaction between the b1 and b2c impulse initiation sites.

Static and dynamic γ-motor output to ankle flexor muscles during locomotion in the decerebrate cat

In locomotion, the flexor muscles of the leg are mainly concerned with the relatively constant task of raising the foot, whereas the extensors have the more variable task of support and propulsion at different speeds. This suggests that the way in which the fusimotor system works may differ between the two muscle groups. Observations previously made of the static and dynamic γ‐motor firing patterns in the ankle extensor medial gastrocnemius (MG) have therefore been repeated in the flexor tibialis anterior (TA). One or more single γ‐motor axons, dissected from a small filament of TA nerve, were recorded simultaneously with a number of single spindle afferents in dorsal rootlets. Cats were decerebrated and locomoted spontaneously on a treadmill. Identification of each γ‐motor axon depended on relating the changes in firing caused by midbrain stimulation to the changes in static and dynamic behaviour of the spindle afferents in response to repetitive ramp and hold stretches. Static γ axons all showed a smooth modulation in frequency, increasing in phase with muscle shortening, superimposed on a minimum frequency of about 20–30 impulses s−1. Dynamic γ axons showed interrupted firing with the frequency rising abruptly from zero at the onset of shortening, and falling again to zero shortly after the onset of lengthening. The frequency during the active periods was relatively constant, even when movement amplitudes varied. The basic similarity in the static and dynamic gamma discharge patterns for the two muscles suggests that the strategy of γ‐motor control is common to both flexors and extensors. The static γ pattern is thought to be a ‘temporal template’ of the expected movement, effectively expanding the dynamic response range of the spindles in active movements. The dynamic γ pattern sensitizes the primary afferents to detect the onset of muscle lengthening and to detect departures from the intended movement trajectory.

Muscle spindle and fusimotor activity in locomotion

Mammals may exhibit different forms of locomotion even within a species. A particular form of locomotion (e.g. walk, run, bound) appears to be selected by supraspinal commands, but the precise pattern, i.e. phasing of limbs and muscles, is generated within the spinal cord by so‐called central pattern generators. Peripheral sense organs, particularly the muscle spindle, play a crucial role in modulating the central pattern generator output. In turn, the feedback from muscle spindles is itself modulated by static and dynamic fusimotor (gamma) neurons. The activity of muscle spindle afferents and fusimotor neurons during locomotion in the cat is reviewed here. There is evidence for some alpha–gamma co‐activation during locomotion involving static gamma motoneurons. However, both static and dynamic gamma motoneurons show patterns of modulation that are distinct from alpha motoneuron activity. It has been proposed that static gamma activity may drive muscle spindle secondary endings to signal the intended movement to the central nervous system. Dynamic gamma motoneuron drive appears to prime muscle spindle primary endings to signal transitions in phase of the locomotor cycle. These findings come largely from reduced animal preparations (decerebrate) and require confirmation in freely moving intact animals.

Role of the Fusimotor System in Locomotion

The contribution of muscle spindles to the control of locomotion depends on the patterns of discharge that occur in static and dynamic gamma motoneurones (gammaS and gammaD). Discharges of gamma-axons to the MG muscle were studied during treadmill locomotion in pre-mammillary, decerebrated cats. All gammaS-efferents increased their rate of discharge at onset of locomotion and were modulated with movement. Type-1 increased their rate with muscle shortening whereas type-2 gammaS efferents increased their discharge rate during muscle lengthening. The type-1 gammaS pattern appears to be a temporal template of the intended movement. The type-2 gammaS pattern may be appropriate for afferent biasing through bag2 intrafusal fibres. The gammaD axons showed an interrupted discharge pattern with sudden onset of firing at the start of muscle shortening and falling quiet shortly after the beginning of lengthening. The gammaD discharge would prepare primary endings to respond with high sensitivity at the start of muscle lengthening.

Chapter 10 Why are there Three Types of Intrafusal Muscle Fibers

Publisher Summary This chapter describes a working scheme for the use of the three intrafusal fiber types. The bag 1 fibers provide control of the stretch sensitivity of primary afferents. Rapid changes in dynamic fusimotor output would be pointless because of the relative slowness of response of the bag 1 fibers and their inability to effectively oppose unloading. The bias levels of primary and secondary afferents could be set by bag 2 activity, but the slowness of bag 2 fiber contraction means that quick changes could not be made in this way. Gamma axons supplying bag 2 fibers alone can be expected, therefore, like dynamic axons, to fire tonically rather than phasically. Finally, the γ motoneurons that would be expected to show rapid modulation during movements should be those jointly supplying bag and chain fibers. The proposed function for the dynamic system is already well supported by spindle recordings in natural movements, but the crucial test for a dual function within the static system is to look for two distinct patterns of natural activity among γ s axons. The prediction is that one group, directed mainly to bag fibers, will fire tonically while the other, directed to chain or to bag 2 and chain fibers, will be modulated roughly in parallel with the active muscle contractions.

Modulation of primary afferent discharge by dynamic and static gamma motor axons in cat muscle spindles in relation to the intrafusal fibre types activated

1 Recordings were made from muscle spindle primary afferents from medial gastrocnemius and soleus muscles of the cat to study the modulating effects of varying γ‐motor stimulation frequency at constant muscle length. Stimulus trains had a mean frequency of 50 Hz and were sinusoidally frequency modulated at 1 Hz, with an amplitude of modulation of ± 5 to ± 30 Hz. 2 When dynamic γ‐axons (γd) were selected for their pure effect on bag1 fibres, they were found to have very little modulating effect on afferent firing. 3 Static γ‐axons (γs) were tested with a random stimulus and correlation method to determine whether they acted purely on bag2 fibres, purely on chain fibres or on both together. Pure bag2γs‐axons had weak modulating effects with large values of phase lag. Pure chain connections were effective in modulating with very little phase lag, but their mean gain was low. Mixed bag2 and chain axons were most effective and showed phase shifts proportional to gain. 4 The effects of muscle length changes recorded previously from locomotor movements were also tested, with and without accompanying stimulation of mixed γs‐axons with pulse trains recorded from γs‐axons. This γs stimulation had a powerful effect in increasing afferent discharge during muscle shortening. The difference in afferent firing between the stimulated and non‐stimulated conditions accurately predicted the profile of the γs stimulation. 5 The results are discussed in relation to the ways in which the γ‐motor system may be used in natural movements.

Classification of longissimus lumborum muscle spindle afferents in the anaesthetized cat

Recordings have been made from 127 single muscle spindle afferents from the longissimus lumborum muscles of anaesthetized cats. They have been characterized by their responses to passive muscle stretch and the effects of succinylcholine (SCh) and by their sensitivity to vibration. The use of SCh permitted the assessment for each afferent of the influence of bag1 (b1) and bag2 (b2) intrafusal muscle fibres. From this, on the assumption that all afferents were affected by chain (c) fibres, they were classified in four groups: b1b2c (41.9%), b2c (51.4%), b1c (1.3%) and c (5.4%). All the afferents with b1 influence were able to respond one to one to vibration at frequencies above 100 Hz and were considered to belong to primary endings. On the basis of the vibration test, 64% of the b2c type afferents appeared to be primaries and 36% secondaries. Of the units classified as primaries, 41% were designated as b2c and would not therefore be able to respond to dynamic fusimotor activity. The significance of this relatively high proportion of b2c‐type spindle primary afferents is discussed in relation to the specialized postural function of the back muscles.

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

1 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. 2 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. 3 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. 4 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.

Spinal projection of spindle afferents of the longissimus lumborum muscles of the cat

The connections and monosynaptic projections of muscle spindle afferents of individual heads of the longissimus lumborum have been studied in cats by natural stimulation, by electrical stimulation and by spike‐triggered averaging from single identified afferents. The spindle afferents were classified by sensitivity to vibration and by the effect of succinylcholine on their response to ramp‐and‐hold muscle stretches. Axonal conduction and synaptic effects were recorded as field potentials and focal synaptic potentials during systematic exploration of the spinal cord in segments L1 to L4 with extracellular metal microelectrodes, singly and in linear arrays. Ascending branches of afferent axons within the cord had a significantly higher mean conduction velocity (CV: 56.5 m s−1) than descending branches (40.8 m s−1). The CV of ascending branches was significantly positively correlated with a measure of the strength of intrafusal bag2 muscle fibre contacts, but not to a measure of bag1 contacts. Two sites of monosynaptic excitatory projection in the cord were identified, namely to the intermediate region (laminae V, VI and VII) and to ventral horn region (laminae VIII and IX). In tests of 154 single afferents, signs of central projection were detected for 60, providing 122 regions of maximum negative focal synaptic potentials (FSPs) of mean amplitude 7.51 μV. Their longitudinal spacing indicated that axons gave off descending collaterals at intervals of 1.5–3.5 mm. Based on the amplitude of FSPs, the projection of secondary afferents is stronger than that of primaries in the intermediate region and possibly also in the ventral horn region. Evidence is also presented that spindle afferent input from different heads of the longissimus converges into any given spinal segment and that input in one spinal root projects to adjacent segments. It is concluded that the organization of the longissimus monosynaptic spindle input favours relatively tonic and diffuse stretch reflexes.