Human Muscle Spindles Act as Forward Sensory Models

Computational and Biological Learning Laboratory, Department of Engineering, University of Cambridge, CB2 1PZ, UK.
Current biology: CB (Impact Factor: 9.57). 10/2010; 20(19):1763-7. DOI: 10.1016/j.cub.2010.08.049
Source: PubMed

ABSTRACT Modern theories of motor control incorporate forward models that combine sensory information and motor commands to predict future sensory states. Such models circumvent unavoidable neural delays associated with on-line feedback control. Here we show that signals in human muscle spindle afferents during unconstrained wrist and finger movements predict future kinematic states of their parent muscle. Specifically, we show that the discharges of type Ia afferents are best correlated with the velocity of length changes in their parent muscles approximately 100-160 ms in the future and that their discharges vary depending on motor sequences in a way that cannot be explained by the state of their parent muscle alone. We therefore conclude that muscle spindles can act as "forward sensory models": they are affected both by the current state of their parent muscle and by efferent (fusimotor) control, and their discharges represent future kinematic states. If this conjecture is correct, then sensorimotor learning implies learning how to control not only the skeletal muscles but also the fusimotor system.

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Available from: Michael Dimitriou, Sep 27, 2015
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    • "In addition to the above-mentioned afferents contribution in sensing the digit position, it has been reported that central motor commands contribute to position sense [32]–[38]. Physiological evidence indicates that central and peripheral signals are strongly correlated due to alpha-gamma co-activation [39]–[41] Furthermore, it has been proposed that predicted future sensory states are implemented through the muscle spindles to update the motor commands during point-to-point movements [42]–[45]. Since we passively positioned the digits and controlled for digit contact forces, the extent to which central commands might have been involved in estimating digit position was likely constant across experimental conditions. "
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    PLoS ONE 06/2013; 8(6):e66140. DOI:10.1371/journal.pone.0066140 · 3.23 Impact Factor
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    • "Although far outnumbered by extrafusal fibers, muscle receptors are equal to extrafusal fibers in amount of nervous traffic (Matthews, 1981b). Muscle spindles play multifunctional roles contributing in proprioception , postural and movement control, motor learning and in plasticity of motor behaviors (Windhorst, 2007, 2008), in predicting future kinematic states by acting as forward sensory model (Dimitriou and Edin, 2010), and as suggested, in the genesis and spread of chronic muscle pain (Johansson et al., 1999; Blair et al., 2003; Johansson et al., 2003). They consist of a bundle of intrafusal fibers enclosed in a fusiform connective tissue capsule attached in parallel with the extrafusal fibers. "
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    ABSTRACT: Significant changes in extrafusal fiber type composition take place in the human masseter muscle from young age, 3-7 years, to adulthood, in parallel with jaw-face skeleton growth, changes of dentitions and improvement of jaw functions. As motor and sensory control systems of muscles are interlinked, also the intrafusal fiber population, that is, muscle spindles, should undergo age-related changes in fiber type appearance. To test this hypothesis, we examined muscle spindles in the young masseter muscle and compared the result with previous data on adult masseter spindles. Also muscle spindles in the young biceps brachii muscle were examined. The result showed that muscle spindle composition and distribution were alike in young and adult masseter. As for the adult masseter, young masseter contained exceptionally large muscle spindles, and with the highest spindle density and most complex spindles found in the deep masseter portion. Hence, contrary to our hypothesis, masseter spindles do not undergo major morphological changes between young age and adulthood. Also in the biceps, young spindles were alike adult spindles. Taken together, the results showed that human masseter and biceps muscle spindles are morphologically mature already at young age. We conclude that muscle spindles in the human young masseter and biceps precede the extrafusal fiber population in growth and maturation. This in turn suggests early reflex control and proprioceptive demands in learning and maturation of jaw motor skills. Similarly, well-developed muscle spindles in young biceps reflect early need of reflex control in learning and performing arm motor behavior.
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