Implications of Positive Feedback in the Control of Movement

Prochazka, Arthur, Deborah Gillard, and David J. Bennett. Implications of positive feedback in the control of movement. J. Neurophysiol. 77: 3237–3251, 1997. In this paper we review some theoretical aspects of positive feedback in the control of movement. The focus is mainly on new theories regarding the reflexive role of sensory signals from mammalian tendon organ afferents. In static postures these afferents generally mediate negative force feedback. But in locomotion there is evidence of a switch to positive force feedback action. Positive feedback is often associated with instability and oscillation, neither of which occur in normal locomotion. We address this paradox with the use of analytic models of the neuromuscular control system. It is shown that positive force feedback contributes to load compensation and is surprisingly stable because the length-tension properties of mammalian muscle provide automatic gain control. This mechanism can stabilize control even when positive feedback is very strong. The models also show how positive force feedback is stabilized by concomitant negative displacement feedback and, unexpectedly, by delays in the positive feedback pathway. Other examples of positive feedback in animal motor control systems are discussed, including the β-fusimotor system, which mediates positive feedback of displacement. In general it is seen that positive feedback reduces the sensitivity of the controlled extremities to perturbations of posture and load. We conclude that positive force feedback can provide stable and effective load compensation that complements the action of negative displacement and velocity feedback.

Cerebellar ataxia and muscle spindle sensitivity

1. The cerebellum has long been known to participate in movement control. One of the enduring theories of cerebellar function is that it "tunes" and coordinates sensorimotor traffic in other parts of the CNS. In particular, it has been implicated in the control of the sensitivity of muscle spindle stretch receptors through the fusimotor system. 2. The stretch sensitivity of spindle primary endings can be varied approximately over a 10-fold range by fusimotor efferent action. For many years it has been believed that cerebellar dysfunction is associated with reduced drive to the fusimotor system and that this in turn causes hypotonia by reducing the reflex excitation of alpha-motoneurons by spindle afferents. 3. The data on which this hypothesis is based were obtained in anesthetized or decerebrate animals. Little direct information is available on animals or humans performing voluntary movements and exhibiting ataxia or other cerebellar symptoms. 4. We tested the hypothesis by recording from nine muscle spindle afferents in behaving cats before and during reversible inactivation of cerebellar interpositus and dentate nuclei. In normal cats fusimotor action varies with motor task, greatly altering spindle stretch sensitivity. We investigated whether this same range of task-related sensitivity manifested itself during ataxia. 5. We found that the full range of spindle sensitivity was still present during ataxia. We therefore conclude that the cerebellar nuclei studied are not primarily responsible for fusimotor control, nor is the ataxia primarily caused by disordered proprioceptive sensitivity.