ReviewCentral pattern generator and human locomotion in the context of referent control of motor actions
Introduction
In 1911, Graham Brown demonstrated the existence of a central pattern generator (CPG) of locomotor-like EMG activity in the absence of proprioceptive influences (reflexes) resulting from deafferentation. Since then, numerous studies have addressed the question of how CPG and reflex influences are integrated on α-motoneurons (MNs) to produce the observable EMG patterns during locomotion and other motor actions in intact animals and humans. These studies showed that the CPG not only elicits coordinated rhythmical activity of numerous muscles of the body, but also controls reflex influences on this activity by facilitating or inhibiting α-MNs at specific phases of the locomotor cycle (Grillner, 1975, Shik and Orlovsky, 1976, Zehr and Duysens, 2004). This phenomenon, called “reflex gating” (Evarts, 1973, Dietz, 1993) is important for adjusting CPG function to changing environmental conditions, particularly elicited by external perturbations such as stumbling that may elicit falling (Dietz, 2003). On the other hand, proprioceptive reflexes can also exert powerful influences on the CPG, for example, by transiently ceasing the rhythmical activity and converting it into postural, tonic EMG activity to maintain body posture after the end of locomotion (Crenna and Frigo, 1984). Reflex reactions to perturbations can also shift the phase of CPG, an important phenomenon called “phase resetting” often observed when it is necessary to prevent falling (e.g., Feldman et al., 2011). Thus, neither the role of the CPG, nor that of proprioceptive reflexes should be underestimated in the generation of normal locomotion. However, despite numerous studies, there is no consensus on the understanding of how central and reflex influences are integrated by α-MNs to produce EMG patterns during intact locomotion or other motor actions. Several studies have assumed that these influences are summated according to the superposition principle, i.e., the net EMG pattern is considered to be the sum of EMG responses that would have been caused by the CPG and reflexes separately (Capaday and Stein, 1987, Ivanenko et al., 2006, Markin et al., 2012). Studies of H-reflex (e.g. Capaday and Stein, 1987) and other reflex responses of MNs at different phases of human walking usually conclude that EMG patterns during normal human gait are basically produced by the CPG with relatively less contribution of proprioceptive reflexes, and that the relative contribution of the CPG and reflexes to EMG patterns is phase-dependent. These conclusions should be considered with caution since the superposition principle is not valid for nonlinear, threshold input/output functions of MNs (Feldman, 2019). Thus, the question of how central and reflex influences are integrated by α-MNs to produce EMG patterns during motor actions, still needs to be addressed, both for the understanding of normal motor control processes as well as for the understanding of how they are affected after neurological injury or disease. Finding a solution to the fundamental problem of the integration of central and proprioceptive influences on MNs is essential for designing rehabilitation strategies for diminishing movement deficits resulting from neurological lesions.
In this review, we will use available neurophysiological properties of α-MNs to offer a solution to the integration problem. We will emphasize the role of sensory systems in maintaining stable equilibrium or, in colloquial terms, balance of forces during postural control, by generating resistance to deviation from the current equilibrium. We define human locomotion as resulting from active and feedforward transfer of stable body equilibrium from one location in the environment to another in the direction of locomotion to a chosen target. This approach requires a departure from the existing biomechanical schemes mainly focusing on rhythmicity rather than on the physical essence of locomotion. We will emphasize distinctive physiological features of new concepts compared with those used in other descriptions of human locomotion (Capaday, 2002, Dietz, 2003, Ivanenko et al., 2006). The physiological meaning of the new notions will be clarified, and clinical implications will be discussed. The review will be concluded by summarising the major points addressed, with suggestions of future directions in the analysis of human locomotion.
Section snippets
The integration problem
As we see it, the integration problem persists, not because of a lack of appropriate experimental material, but rather, due to the limitations of the conventional theoretical biomechanical and computational frameworks in which the problem is usually considered. It is appropriate to quote here Albert Einstein who said that “we cannot solve problems by using the same kind of thinking we used when we created them” (Kleckner, 2018). In other words, the tenets of conventional theories of motor control are
Parametric control of α-motoneurons in a spatial frame of reference
Although characteristics of different muscles are very diverse, the principal mechanisms underlying the control of α-MNs of human arm, leg, oculomotor muscles (EOMs), and cat hindlimb muscles are surprisingly similar (Fig. A1, Fig. A2): MNs of all these muscles are controlled by changing parameter λ with Eqs. (A.1)–(A.3) that define the conditions for muscle activation and de-activation.
Known physiological properties of α-MNs underlie the origin of λ, such as properties of the threshold
Change in the referent body location and configuration may underlie human gait
Each actual body configuration or posture, Q, is described geometrically by a set of respective joint angles or degrees of freedom (DFs) of the body. All possible body configurations Q, can be considered as comprising a spatial FR, the origin point of which is defined as the referent body configuration (R), the specific “threshold” body posture at which MNs of both single and multi-joint muscles begin to be recruited or de-recruited (Feldman, 2015). In another formulation, if λ is the
Summary and future directions
Even detailed biomechanical and/or neurophysiological descriptions seem insufficient to advance understanding of how motor behavior is controlled. Progress depends on a correct choice of a theoretical framework in which experimental facts are coordinated in a logical system or theory (Einstein, 1922). Experimental findings support the theory in which motor outcome emerges in task-specific, spatial frames of reference following indirect, referent or parametric control of motor actions, in
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This work was supported by a grant from National Science and Engineering Research Council (NSERC) of Canada (AGF). DP was supported by the Fonds de la Recherche en Sante du Quebec.
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