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EDITORIAL FOCUS
Laboratoire de Neurobiologie des Réseaux, Unité Mixte de Recherche 5816, Centre National de la Recherche Scientifique, University Bordeaux 1, 33405 Talence, France
What is the contribution of proprioceptive force feedback in force generation during active movements? This question is of great interest for understanding how the CNS compensates for gravitational load (Duysens et al. 2000
). As an animal walks, the weight on a given leg changes considerably during the stance phase. To compensate for this shift in weight, the motor command system needs to actively adapt the force exerted by the extensor muscles. Indeed, the interplay between centrally programmed activity and feedback activity has motivated research for almost a century (Pearson 1993). Such questions are difficult to address because they require the analysis of the functional role of neural components in a behaving animal. This is one of the merits of the paper by Donelan and Pearson, (this issue, p. 2093–2104). In mammals, the Golgi tendon organ constitutes a type of proprioceptor specialized in force detection. However, its quantitative contribution to load compensation during active movement has until now not been determined. Donelan and Pearson provide, for the first time, a quantitative estimation of the contribution of this type of force feedback to ankle extensor activity during walking.
This question is important because we know that most rhythmic movements of animals are produced by central pattern generators (CPGs) capable of producing patterned activity in the absence of any sensory feedback. CPGs have been described in virtually all vertebrate and invertebrate motor systems studied (Delcomyn 1980). In vitro, these CPGs produce programmed activity termed "fictive" walking, "fictive" swimming, etc., because no movements are produced during these centrally programmed activities (Viala et al. 1978). However, a striking feature of most of these fictive motor activities is their high degree of similarity with activities produced during true movements. What then is the role of sensory feedback in this kind of motor activity? Several roles have been acknowledged, such as precisely tuning the temporal output pattern (Prochazka et al. 1989), facilitating the transition from one phase to the next (Grillner and Rossignol 1978), and reinforcing the ongoing activity (Delcomyn 1980; Rossignol et al. 1988). Apart from this role in shaping the rhythmic motor command, in some extreme cases, proprioceptive feedback cues are so intimately linked to the CPG that proprioceptors can be considered as elements of the rhythmic generator; this was shown for the edge cells in the lamprey spinal cord (Grillner et al. 1991; Rossignol et al. 1988) and the wing stretch receptors of the locust flight system (Pearson 1985).
In this paper, Donelan and Pearson have studied load compensation in the walking system of the cat. Previous work has shown that, during the stance phase, the extensor activity was reinforced by increasing length or load of the muscle (Akazawa et al. 1982; Bennett et al. 1996). Two proprioceptive structures could be involved in this phenomenon: muscle spindle afferents (via Ia sensory fibers) and Golgi tendon organ (via Ib sensory fibers). Two sets of observations indicate that these sensory structures could be involved: 1) both group Ia and group Ib afferents are activated during the stance phase (Prochazka and Gorassini 1998; Prochazka et al. 1989), and 2) the electrical stimulation of group I afferents from ankle extensor muscles prolongs the stance phase and prevents transition to the swing phase (Whelan 1996; Whelan et al. 1995). However, in these experiments, no quantification of the participation of each of these proprioceptive afferents was done.
Using a decerebrate cat walking on a treadmill, the authors varied the length of the isolated medial gastrocnemius (MG) muscle (an extensor of the ankle) during sequences of rhythmic contractions associated with walking in the three other legs. They found that both muscle activity and force increased as the muscle was elongated. The key point of their demonstration consists of differentiating two regions in the EMG from the MG muscle during walking: an early region and a middle region. The increased muscle activity did not involve muscle spindles because, contrary to Golgi tendon organs, the activity of muscle spindles was relatively insensitive to changes in muscle length in the middle region of MG bursts. The authors also show that other proprioceptors, such as group II afferents, were not involved in this increased activity associated with increased force. These results indicate that the pathway of positive force feedback is mediated by the Golgi tendon organs and is isolated from other afferent pathways in their experimental paradigm. The authors propose a simple model of the neuromuscular system involved in load compensation that they use to estimate the gain of the force feedback loop. Using this model, they estimate that force feedback accounts for 20% of the total force at short muscle length (i.e., when walking on a horizontal surface), but may account for 
50% of the total force at longer muscle length (i.e., when walking up slopes). The work of Donelan and Pearson highlights the role of force proprioception in the control of rhythmic movements. They show that it significantly contributes to the adaptation of the output of the nervous system to changing biomechanical constraints. This work is a stimulating example of the interest of studying the motor nervous system in its natural environment: the living animal.
Address for reprint requests and other correspondence: D. Cattaert, Laboratoire de Neurobiologie des Réseaux, Unité Mixte de Recherche 5816, Centre National de la Recherche Scientifique, Unversity Bordeaux 1, 33405 Talence, France (E-mail: d.cattaert{at}lnr.u-bordeaux1.fr).
REFERENCES
Akazawa K, Aldridge JW, Steeves JD, and Stein RB. Modulation of stretch reflexes during locomotion in the mesencephalic cat. J Physiol 329: 553–567, 1982.
Bennett DJ, De Serres SJ, and Stein RB. Regulation of soleus muscle spindle sensitivity in decerebrate and spinal cats during postural and locomotor activities. J Physiol 495: 835–850, 1996.[ISI]
Delcomyn F. Neural basis of rhythmic behavior in animals. Science 210: 492–498, 1980.
Donelan JM and Pearson KG. Contribution of force feedback to ankle extensor activity in decerebrate walking cats. J Neurophysiol 92: 2093–2104, 2004.
Duysens J, Clarac F, and Cruse H. Load-regulating mechanisms in gait and posture: comparative aspects. Physiol Rev 80: 83–133, 2000.
Grillner S and Rossignol S. On the initiation of the swing phase of locomotion in chronic spinal cats. Brain Res 146: 269–277, 1978.[CrossRef][ISI][Medline]
Grillner S, Wallen P, Brodin L, and Lansner A. Neuronal network generating locomotor behavior in lamprey: circuitry, transmitters, membrane properties, and simulation. Annu Rev Neurosci 14: 169–199, 1991.[CrossRef][ISI][Medline]
Pearson KG. Are there central pattern generators for walking and flight in insects? In: Feedback and Motor Control in Invertebrates and Vertebrates, edited by Barnes WJP and Gladden MH. London: Croom Helm, 1985, p. 307–315.
Pearson KG. Common principles of motor control in vertebrates and invertebrates. Annu Rev Neurosci 16: 265–297, 1993.[ISI][Medline]
Prochazka A and Gorassini M. Ensemble firing of muscle afferents recorded during normal locomotion in cats. J Physiol 507: 293–304, 1998.
Prochazka A, Trend P, Hulliger M, and Vincent S. Ensemble proprioceptive activity in the cat step cycle: towards a representative look-up chart. Prog Brain Res 80: 61–74, 1989.[ISI][Medline]
Rossignol S, Lund JP, and Drew T. The role of sensory inputs in regulating patterns of rhythmical movements in higher vertebrates. In: Neural Control of Rhythmic Movements in Vertebrates, edited by Cohen AH, Rossignol S, and Grillner S. New York: John Wiley, 1988, p. 201–283.
Viala G, Orsal D, and Buser P. Cutaneous fiber groups involved in the inhibition of fictive locomotion in the rabbit. Exp Brain Res 33: 257–267, 1978.[ISI][Medline]
Whelan PJ. Control of locomotion in the decerebrate cat. Prog Neurobiol 49: 481–515, 1996.[CrossRef][ISI][Medline]
Whelan PJ, Hiebert GW, and Pearson KG. Stimulation of the group I extensor afferents prolongs the stance phase in walking cats. Exp Brain Res 103: 20–30, 1995.[ISI][Medline]
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