Nature and patterns of fusimotor drive
In a previous study (Murphy, 2002) the activity of FDL and FHL γ-efferents was recorded directly in a similar preparation (i.e. premammillary decerebrate cat) to that used here. Two basic patterns were distinguished in both muscles. ‘Tonic’ units fired throughout the step cycle and had less modulation, but higher minimum rates, than ‘phasic’ units which were mainly recruited with ankle extensor EMG activity. In both muscles tonic units had low resting rates (0-8 impulses s−1) while phasic units showed a wider range (0-50 impulses s−1). What are the implications of the present spindle recordings for the nature of these fusimotor patterns? In FHL and FDL tonically active γ-efferents showed a marked increase in mean rate between the resting and locomotor states. Further, only the tonic category usually discharged in the extension and flexion phases. Thus, the increased firing rate and decreased modulation of FDL and FHL spindles during locomotion is most simply explained if most tonic γ-efferents are static in nature.
The spindle afferent data suggest differential phasic fusimotor action during the extension phase in FDL and FHL. Signs of phasic dynamic γ drive occurred only in FHL. While phasic static γ drive was indicated for FDL, modulated static activity could not be excluded with FHL. Regarding FHL, phasic γ-efferents were recruited with ankle extensor EMG activity (Murphy, 2002). The modulation of FHL tonic γ-efferents was lower and peaked shortly after EMG onset (mean, 2 % step cycle). Such activity is unlikely to be responsible for the cyclic variation in modulation of FHL Ia afferents that peaked 53 % (mean) through the step cycle (see Taylor et al. 1985). Since Ia afferents are typically influenced by 1–2 dynamic γ-efferents (Matthews, 1981), these observations suggest that most FHL dynamic γ-motoneurones are phasically recruited during locomotion.
In FDL, phasic γ-efferents were recruited with extension while the tonic category had weak modulation (mean, 10 impulses s−1) and generally peaked before (mean, 9 % step cycle) extensor EMG onset (Murphy, 2002). The marked increase in discharge of half the FDL Ia and group II afferents during extension, peaking 24 % (mean) after EMG onset, therefore suggests that a component of the phasic γ population is static in nature. As dynamic γ-axons excite Ia afferents (but not group II), it is possible that this type is also phasically active in FDL. However, any such γ activity was never dominant, as indicated by the lack of accompanying increases in afferent modulation.
Because about 40 % of FDL afferents (9 of 21, e.g. Fig. 4B) had enhanced discharge rate and reduced modulation throughout the step cycle (due to tonic static γ-efferents), and showed increased firing during extension (involving phasic static γ-efferents), it follows that a given spindle commonly received distinct patterns of static γ discharge through separate γ-efferents (i.e. tonic and phasic). The functional significance of this dichotomy, which implies specificity of locomotor control within the static γ system, is unknown but may be related to the suggestion that there are two types of static γ-axon that differ in the distribution of their effects on bag2 and chain intrafusal fibres (Boyd, 1986; see also, Taylor et al. 1998). Alternatively there may be a need to channel distinct patterns of γ drive via different, but functionally identical efferents. Evidence of two locomotor patterns of static γ discharge has also been reported recently on the basis of recordings from the medial gastrocnemius nerve in decerebrate cats (Taylor et al. 2000b). However, it should be noted that in the original recordings of fusimotor activity from this nerve, static γ sub-groups were not distinguished (Murphy et al. 1984). The reason for the apparent disparity between these studies is currently unclear.
Very little is known about the discharge patterns of identified γ-efferents during locomotion. The data involve hind limb muscles of decerebrate cat preparations (for review see Murphy & Martin, 1993): triceps surae (ankle extensor), medial sartorius (hip/knee flexor) and tibialis anterior (ankle flexor). The tonic static and phasic (α-linked) dynamic γ-drives described here for FHL are very similar to those of triceps surae. Functionally this is appropriate since the muscles share a marked extensor synergy and contribute to anti-gravity support. Tibialis anterior and medial sartorius are active during flexion, and have a strong phasic (α-linked) static γ drive in common. FDL has both a flexor (late stance) and extensor α synergy (Fleshman et al. 1984; Trank & Smith, 1996) during which the muscle shortens and lengthens, respectively (O'Donovan et al. 1982). However, its γ drive does not match other muscles with either synergy since the FDL flexor α burst was not linked to γ activation, and its extensor α drive was accompanied by phasic static γ activation. It would thus appear that α synergy does not necessarily correlate with fusimotor usage. Further, phasic static γ activity in FDL during extension, as predicted from the present results, would not be related to muscle shortening, in contrast to other muscles during rhythmic movements (for review see Murphy & Martin, 1993).
The rules that govern the γ system during movement have yet to be fully established. α/γ linkage appears to be the norm in man while α/γ independence is common in the cat (for review see Prochazka, 1996). Different experimental conditions may, however, underlie the apparent discrepancy. In both cases, a major unresolved problem concerns the γ drive to different muscles during the same behaviour. Does it vary? If so, what are the governing rules and functional significance? The present results add to the growing body of evidence, from reduced cat preparations, of muscle-specific γ drive during locomotion (Perret & Berthoz, 1973; Cabelguen, 1981; Bessou et al. 1990; Murphy & Hammond, 1993; Murphy, 2000; Taylor et al. 2000a; Murphy, 2002). Various factors may influence the strategy of γ usage for a particular muscle including its kinematic behaviour (i.e. motion) and activation state (see later).
There are few spindle afferent recordings from FDL or FHL in the intact cat with which to compare the present data (Prochazka et al. 1976; Loeb & Duysens, 1979; Prochazka & Gorassini, 1998). Nevertheless, on the reasonable assumption that the γ locomotor discharge characteristics of the decerebrate cat are representative of the basic patterns during normal movement (Murphy & Martin, 1993; Taylor et al. 2000a; Murphy, 2002), certain functional advantages may arise, depending on the setting of central pathways, from the suggested strategies of γ usage. In FDL and FHL the proposed tonic static γ drive would increase the rate and reduce the sensitivity (i.e. stretch modulation) of Ia and group II afferents during locomotion. Direct recordings of FDL muscle length indicate that marked changes occur over the step cycle, but with little active tension (O'Donovan et al. 1982). It has been proposed that the fusimotor system optimises the sensory information obtained from the spindle to the expected kinematic conditions (Loeb, 1984; Scott & Loeb, 1994). In this context, tonic static γ drive in FDL would be functionally useful in preventing receptor saturation at both ends of the dynamic range. Direct information concerning the normal kinematics of FHL is currently unavailable and a similarity with FDL cannot be assumed because of substantial differences in their moment arms at the ankle (Young et al. 1993).
Concerning motor function, since FHL and triceps surae have similar γ drives and share a prominent anti-gravity function during locomotion, it seems reasonable to suggest a common fusimotor role in contributing to the adjustment of stretch reflex gain to a level appropriate for the ongoing movement (Taylor et al. 1985; Bennett et al. 1996a,b). In FDL, tonic static γ drive may be related to the activation state (low, brief) of the parent muscle. A low Ia afferent sensitivity would minimise stretch reflex responses to peripheral perturbations and support weak (but precise) central α activation.
The various proposals concerning the motor role of γ drive are dependent upon the operative status of central pathways. Experiments involving electrical stimulation of group I muscle afferents in the decerebrate cat have demonstrated homonymous mono- and disynaptic excitation of FDL and FHL α-motoneurones during fictive locomotion (Degtyarenko et al. 1998). The disynaptic pathway was facilitated during extension, as occurs in hindlimb extensors (McCrea et al. 1995). These observations offer a range of potential reflex control strategies involving γ drive and muscle spindle Ia afferents, and tendon organ Ib afferents (for review see Pearson, 1995), including the preceding suggestions. Further, since heteronymous monosynaptic Ia connections exist between FHL and FDL (Fleshman et al. 1984), the intriguing possibility arises that the phasic (α-linked) γ drive of FDL (or FHL) may influence the spindle reflex regulation of its anatomical synergist, even though it is functionally distinct.
Recordings of muscle spindle afferents from the intact cat during natural movements have indicated that fusimotor drive is task- and context-dependent; observations that led to the fusimotor set hypothesis (Prochazka, 1983, 1996; Prochazka & Hulliger, 1983). One aspect of this view is that ‘proprioceptive sensitivity is adjusted at its source by the CNS according to the overall sensorimotor requirements predicted for upcoming movements’ (Prochazka, 1989, p. 289). To date, evidence consistent with muscle-specific fusimotor drive, based on afferent recordings in intact animals, is sporadic (e.g. Loeb & Duysens, 1979). A full appreciation of this feature of fusimotor control may require the development of new techniques that permit direct recordings from identified and classified γ-motoneurones during natural behaviour. If muscle-specific γ drive is prevalent under such conditions then it is compatible with the fusimotor set hypothesis.