Simple Locomotor Reflexes

The neurophysiological significance of the age-old observation that decapitated animals can display coordinated locomotion had been recognized and documented by the mid-18th Century (Mettrie 1745). Clearly, the neuronal machinery in the spinal cord was capable of controlling quite complex activities without descending input from the brain. The notion that all movements were simply chains of reflexes developed a century later (Spencer 1855). In the late 19th and early 20th centuries, the elementary movements involved in locomotion began to be studied in detail, particularly in spinalized or decerebrated dogs and cats (Freusberg 1874; Sherrington 1910; Brown 1911). Sherrington's (1910) study was a tour de force of careful experimentation and highly detailed description and remains a definitive reference work to this day. In it, he described the biomechanical actions of most of the muscles of the cat hindlimb, how these muscles were activated or fell silent in flexion and extension reflexes, and how they participated in what he termed "reflex stepping" (now referred to as air stepping) in spinal cats and "reflex walking," i.e., weight-bearing gait, in decerebrate cats.

6.6.1 The Stretch Reflex

The "stretch reflex" differs in decerebrate and intact animals and since Sherrington's time it has come to be realized that several CNS mechanisms may contribute components of different latency to the stretch reflex response. At the segmental level, muscle spindle Ia afferents activated by muscle lengthening monosynaptically excite homonymous alpha motoneurons which in turn cause the muscle to resist the stretch. In static postures, Ib input generally results in homonymous inhibition, but recently it has been shown that this switches to longer-latency homonymous excitation during locomotion (Conway et al. 1987), at least in cat extensor muscles (the evidence for Ib homonymous excitation in human locomotion is a matter of controversy: see below). Group II input from muscle spindles has also been implicated in long-latency components of stretch reflexes (Matthews 1991; Sinkjaer et al. 2000; Grey et al. 2001). Ia homonymous excitation represents negative displacement feedback, which augments the intrinsic stiffness of active muscles in the face of length perturbations. Ib homonymous feedback, on the other hand, represents positive force feedback. Positive feedback is synonymous with instability and oscillation in engineering systems, but when muscles are the actuators, their non-linear length-tension properties turn out to stabilize the positive feedback loop (Prochazka et al. 1997a; Prochazka et al. 1997b).

FIGURE 6.4 Summary figure showing firing rate profiles of ensembles of group Ia, Ib, and II muscle afferents during medium-speed stepping in normal cats. The data were compiled from numerous single-unit recordings obtained with implanted dorsal root electrodes. Reproduced with permission from Prochazka A. and Gorassini, M., J. Physiol. 507, 293, 1998.

FIGURE 6.4 Summary figure showing firing rate profiles of ensembles of group Ia, Ib, and II muscle afferents during medium-speed stepping in normal cats. The data were compiled from numerous single-unit recordings obtained with implanted dorsal root electrodes. Reproduced with permission from Prochazka A. and Gorassini, M., J. Physiol. 507, 293, 1998.

Segmental stretch reflexes and their electrically-elicited counterparts, H-reflexes, have been studied intensively for many years, partly because they are modulated in interesting ways, but mainly because it is technically relatively easy to elicit and measure them. Studies of this type have been reviewed many times in recent years (Dietz 1996; Prochazka 1996b; Brooke et al. 1997; Dietz 1998; Duysens et al. 2000; Schneider et al. 2000). Human H-reflexes are smaller during locomotion than during static postures and they show phase-dependent fluctuations (Garrett et al. 1981; Garrett and Luckwill 1983; Garrett et al. 1984; Capaday and Stein 1986). It is often assumed that H-reflexes represent transmission in the short-latency pathway from Ia afferents to homonymous motoneurons, though an oligosynaptic contribution cannot be ruled out (Burke 1983). There is evidence that the faster the locomotion and the more difficult the terrain, the greater the suppression of H-reflexes (Capaday and Stein 1987; Llewellyn et al. 1990). It is vigorously debated whether this modulation is centrally generated (Schneider et al. 2000) or due to reafferent signals (Misiaszek et al. 1998). Stretch reflexes elicited during locomotion by rapidly stretching individual muscles (Akazawa et al. 1982; Hiebert et al. 1996) or imposing sudden rotations about joints (Orlovsky and Shik 1965; Sinkjaer 1997; Gritsenko et al. 2001) also show phase-dependent modulations, but these are less predictable than H-reflex modulations (Sinkjaer 1997; Christensen et al. 2001). This is not too surprising, as stretch reflexes comprise not only the Ia-mediated short latency responses but also longer-latency responses involving group II reflexes, group Ib reflexes, and higher-level processing in the CNS (Sinkjaer et al. 1999).

Before one delves too deeply into the mechanisms and modulation of stretch reflexes, however, one should ask how important they are in the control of locomotion and movement anyway. Would an animal be simply unable to support its weight if it had no stretch reflexes? The answer is no, on both experimental and theoretical grounds. Provided that the alpha motoneurons of load-bearing muscles are activated from some source in the nervous system, the muscles develop an intrinsic stiffness that resists stretching and that can in fact be represented as displacement feedback (Partridge 1966). This is easily seen in the stretch reflex model of Appendix Figure 1, whereby in the inner feedback loops muscle stretch results in reactive forces due to the force-length and force-velocity properties of muscle. Muscle afferent feedback mediated by Ia and Ib pathways in the outer loops of the model provides a source of input to alpha motoneurons but it is not the only source. There are many descending and propriospinal pathways that also activate motoneurons, represented by just one input in the model of Appendix Figure 1.

Analysis of responses to loading with this model showed that simple stretch reflexes mediated by spindle Ia afferents for example can at most triple the prevailing muscle stiffness without causing instability (Prochazka et al. 1997a). This is illustrated in Figure 6.5, where Ia gains of 1 and 2 (negative feedback) educed the muscle stretch caused by applied force by factors of about 2 and 3, respectively; the loop became unstable when the gain in the Ia-mediated pathway was set to 3. Though there are several simplifying assumptions in models of this type, their predictions have been shown to be fairly accurate in hybrid experiments in which actual muscles were stretched and "reflexly" activated by electrical stimulation modulated by a signal obtained by filtering the displacement signal with a spindle Ia transfer function (Bennett et al. 1994).

stretch responses to force ramps (0-30N in 1 s> for combinations of la and lb reflex gain

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