ReviewRole of sensory feedback in the control of stance duration in walking cats
Introduction
The movements of appendages for walking and flight generally consist of two major phases: one to propel the animal, and the other to return the propulsive structure to the starting position. These two phases are generally referred to as the power-stroke and return-stroke, respectively, although more specific terms are often used depending on the behavior, e.g., stance and swing for leg movements during walking in vertebrates, retraction and protraction for leg movements in insects, and downstroke and upstroke for wing movements. A major issue in contemporary research on the neurobiology of walking and flight has been to determine the neuronal mechanisms controlling these phase transitions. Charles Sherrington in his classic studies almost a century ago on locomotion in quadrupeds proposed that the phase transitions of leg movements during stepping were produced by sensory signals from leg proprioceptors (Sherrington, 1910). However, almost contemporaneously Thomas Graham Brown (1911) demonstrated that rhythmic alternating contractions of muscles involved in the stance phase (extensor muscles) and swing phase (flexor muscles) could be generated in the absence of any sensory signals from sensory receptors in the legs. Clearly Graham Brown's observation raised the possibility that under some conditions sensory signals are not necessary for establishing the timing of phase transitions, but it did not exclude Sherrington's proposal that sensory signals are used to control one or both of the phase transitions during normal walking. Since the time of these early studies there have been a large number of investigations aimed at determining how the rhythm generating networks in the spinal cord (now termed central pattern generators) are influenced by sensory signals from receptors in the skin, joints and muscles of the legs (see reviews by McCrea, 2001, Pearson, 2003, Prochazka, 1996, Rossignol et al., 2006). This has resulted in the accumulation of substantial evidence supporting the notion that phasic sensory signals are involved in controlling the timing of phase transitions in walking mammals (including humans), and in some circumstances indicated these signals may be the causal event in initiating the switch from one phase to the other. A similar conclusion has been reached in contemporary studies on the walking system of insects (Büschges, 2005) and the flight system of the locust (Pearson and Ramirez, 1997).
In this Chapter, I focus on the mechanisms controlling the phase transition from stance to swing in the walking system of the cat. My reason for this narrow focus is that the cat has provided some excellent preparations to study the sensory control of stepping, and as a result we now have some specific hypotheses for the function of identified groups of sensory receptors in the control of the timing of phase transitions and in the regulation of the magnitude of muscle activity (see Donelan and Pearson, 2004, for a review of the latter). The extent to which these hypotheses can be generalized to other mammals is uncertain, but some striking parallels have been found in between the walking system of the cat and the walking system of humans (Donelan and Pearson, 2004, Duysens et al., 2000, Pang and Yang, 2000). The majority of investigations on phase transitions in the walking cat have been aimed at understanding the transition from stance to swing, and these studies have yielded a substantial body of evidence that this transition is controlled by sensory signals from leg proprioceptors and identified some of the receptors providing these signals. The mechanisms initiating the swing-to-stance transition are not as well understood, although a number of recent findings have indicated that sensory signals do have a role in regulating this transition but perhaps not to the same degree as the signals regulating the stance-to-swing transition (Lam and Pearson, 2001, McCrea, 2001, McVea et al., 2005, Stecina et al., 2005).
The most compelling evidence that sensory signals can regulate the timing of stepping movements in the cat is that when spinal and decerebrate animals walk on a treadmill the rate of stepping in the hind legs matches the speed of the treadmill. This adaptation occurs over a wide range of treadmill speeds (e.g., 0.1 to 1 m/s), and at the higher speeds a transition from a walking/trotting gait pattern to a galloping gait pattern sometimes occurs. As treadmill speed is increased there is a reduction in the duration of the stance phase but relatively little change in the duration of the swing phase. This observation implies that the matching of stepping rate to the speed of the treadmill depends primarily on sensory signals regulating the duration of the stance phase, i.e., the timing of the stance-to-swing transition. Numerous sensory signals could in theory provide the appropriate information to control stance phase duration, but two signals considered to be especially important are associated with the unloading of the ankle extensor muscles and with extension of the hip.
Section snippets
Evidence that unloading the ankle extensor muscles contributes to the control of the stance-to-swing transition
The first indication that unloading the ankle extensor muscles may be necessary for the termination of stance came from the findings of Duysens and Pearson (1980) that loading these muscles could inhibit flexor burst generation in decerebrate walking cats. The muscles were loaded either by a maintained stretch or by electrical stimulation of ventral roots. Loading the muscles by imposing a maintained stretch introduced the uncertainty that flexor burst inhibition could have been produced by
Evidence that hip extension contributes to the control of the stance-to-swing transition
The first indication that input from the hip region could be a factor in initiating the swing phase of stepping in quadrupeds came from observations on the effects of extending the hip in chronic spinal dogs (Sherrington, 1910). Rapid extension of the hip led to contractions of flexor muscles, and sometimes to sequences of rhythmic leg movements. Strong support for this idea came when Grillner and Rossignol (1978) examined quantitatively the relationship between hip extension and the timing of
Integration of sensory and central signals for controlling stance duration
Although we lack a detailed understanding of the organization of the spinal networks generating the basic motor pattern of stepping (McCrea and Rybak, 2008), the network controlling stepping in a single hind leg appears to be organized to produce two basic muscle synergies: one is a complex pattern of activation of mainly flexor muscles during the swing phase, and the other a simpler pattern of activation of mainly extensor muscles during the stance phase. Within each synergy, the timing of the
Acknowledgments
I thank David McVea for his comments on a draft of this paper and for his collaboration on experiments to examine the influence of hip extension in decerebrate walking cats. Supported by a grant from the Canadian Institutes of Health Research.
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