Elsevier

Clinical Neurophysiology

Volume 132, Issue 11, November 2021, Pages 2870-2889
Clinical Neurophysiology

Review
Central pattern generator and human locomotion in the context of referent control of motor actions

https://doi.org/10.1016/j.clinph.2021.08.016Get rights and content

Highlights

  • Human locomotion likely results from changes in neurophysiological parameters that shift stable body equilibrium in space.

  • Central pattern generator and descending systems set the threshold muscle lengths at which motoneurons and reflexes begin to act.

  • Proprioceptive feedback is vital for converting central influences on motoneurons into shifts of threshold muscle lengths.

Abstract

Unperturbed human locomotion presumably results from feedforward shifts in stable body equilibrium in the environment, thus avoiding falling and subsequent catching considered in alternative theories of locomotion. Such shifts are achieved by relocation of the referent body configuration at which multiple muscle recruitment begins. Rather than being directly specified by a central pattern generator, multiple muscles are activated depending on the extent to which the body is deflected from the referent, threshold body configuration, as confirmed in previous studies. Based on the referent control theory of action and perception, solutions to classical problems in motor control are offered, including the previously unresolved problem of the integration of central and reflex influences on motoneurons and the problem of how posture and movement are related. The speed of locomotion depends on the rate of shifts in the referent body configuration. The transition from walking to running results from increasing the rate of referent shifts. It is emphasised that there is a certain hierarchy between reciprocal and co-activation of agonist and antagonist muscles during locomotion and other motor actions, which is also essential for the understanding of how locomotor speed is regulated. The analysis opens a new avenue in neurophysiological approaches to human locomotion with clinical implications.

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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