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


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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    • "The nature and characteristics of these feedbacks contribute significantly to force control . On the proprioceptive side, muscle, aponeurosis and tendon receptors (e.g., neuromuscular spindles and Golgi tendon organs) provide real-time information on the degree of muscle fibers stretching and tension level, together with body segments' spatial position (Dimitriou and Edin 2010). On the exteroceptive side, vision and pressure are the most important sensory components for force modulation (Sayenko et al. 2012; Lin and Yang 2011). "
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    ABSTRACT: Purpose The aim of the study was to evaluate the force control in the complete absence of visual feedback and the effect of repeated contractions without visual feedback. Methods Twelve physically active males (age 23 ± 1 years; stature 1.74 ± 0.07 m; body mass 71 ± 6 kg) performed isometric tasks at 20, 40 and 60 % maximal voluntary contraction (MVC) for 20 s. For each intensity, a trial with force visual feedback (FB) was followed by 3 trials without FB (noFB-1, noFB-2, noFB-3). During contraction, force and surface electromyogram (EMG) from the vastus lateralis muscle were recorded. From force signal, the coefficient of variation (CV, force stability index), the distance of force from target (ΔF, force accuracy index) and the time within the target (t-target) were determined. From EMG signal, the root mean square (RMS) and mean frequency (MF) were calculated. Results MVC was 679.14 ± 38.22 N. In noFB-1, CV was similar to FB, ΔF was higher and t-target lower (P
    Arbeitsphysiologie 11/2014; 115(3). DOI:10.1007/s00421-014-3036-1 · 2.19 Impact Factor
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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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    ABSTRACT: Dexterous manipulation relies on modulation of digit forces as a function of digit placement. However, little is known about the sense of position of the vertical distance between finger pads relative to each other. We quantified subjects' ability to match perceived vertical distance between the thumb and index finger pads (dy ) of the right hand ("reference" hand) using the same or opposite hand ("test" hand) after a 10-second delay without vision of the hands. The reference hand digits were passively placed non-collinearly so that the thumb was higher or lower than the index finger (dy = 30 or -30 mm, respectively) or collinearly (dy = 0 mm). Subjects reproduced reference hand dy by using a congruent or inverse test hand posture while exerting negligible digit forces onto a handle. We hypothesized that matching error (reference hand dy minus test hand dy ) would be greater (a) for collinear than non-collinear dy s, (b) when reference and test hand postures were not congruent, and (c) when subjects reproduced dy using the opposite hand. Our results confirmed our hypotheses. Under-estimation errors were produced when the postures of reference and test hand were not congruent, and when test hand was the opposite hand. These findings indicate that perceived finger pad distance is reproduced less accurately (1) with the opposite than the same hand and (2) when higher-level processing of the somatosensory feedback is required for non-congruent hand postures. We propose that erroneous sensing of finger pad distance, if not compensated for during contact and onset of manipulation, might lead to manipulation performance errors as digit forces have to be modulated to perceived digit placement.
    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.
    The Anatomical Record Advances in Integrative Anatomy and Evolutionary Biology 04/2011; 294(4):683-93. DOI:10.1002/ar.21347 · 1.54 Impact Factor
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