The Consequences of Short-Range Stiffness and Fluctuating Muscle Activity for Proprioception of Postural Joint Rotations: The Relevance to Human Standing

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Abstract
Proprioception comes from muscles and tendons. Tendon compliance, muscle stiffness, and fluctuating activity complicate transduction of joint rotation to a proprioceptive signal. These problems are acute in postural regulation because of tiny joint rotations and substantial short-range muscle stiffness. When studying locomotion or perturbed balance these problems are less applicable. We recently measured short-range stiffness in standing and considered the implications for load stability. Here, using an appropriately simplified model we analyze the conversion of joint rotation to spindle input and tendon tension while considering the effect of short-range stiffness, tendon compliance, fluctuating muscle activity, and fusimotor activity. Basic principles determine that when muscle stiffness and tendon compliance are high, fluctuating muscle activity is the greatest factor confounding registration of postural movements, such as ankle rotations during standing. Passive and isoactive muscle, uncomplicated by active length fluctuations, enable much better registration of joint rotation and require fewer spindles. Short-range muscle stiffness is a degrading factor for spindle input and enhancing factor for Golgi input. Constant fusimotor activity does not enhance spindle registration of postural joint rotations in actively modulated muscle: spindle input remains more strongly associated with muscle activity than joint rotation. A hypothesized rigid α–γ linkage could remove this association with activity but would require large numbers of spindles in active postural muscles. Using microneurography, the existence of a rigid α–γ linkage could be identified from the correlation between spindle output and muscle activity. Basic principles predict a proprioceptive “dead zone” in the active agonist muscle that is related to the short-range muscle stiffness.