The distribution and abundance of muscle spindles

The distribution and abundance of muscle spindles

Brain Research Bulletin 75 (2008) 502–503 Commentary The distribution and abundance of muscle spindles Uwe Proske ∗ Department of Physiology, Monash...

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Brain Research Bulletin 75 (2008) 502–503

Commentary

The distribution and abundance of muscle spindles Uwe Proske ∗ Department of Physiology, Monash University, Clayton, VIC 3800, Australia Received 3 October 2007; accepted 3 October 2007 Available online 31 October 2007

Abstract This commentary suggests that the distribution and abundance of muscle spindles in different muscles is related to their role as signallers of muscle fascicle length. Large muscles comprising many fascicles will therefore have more spindles than smaller muscles. © 2007 Elsevier Inc. All rights reserved. Keywords: Muscle spindle; Proprioception; Kinaesthesia

In his letter to the Editor, written in response to a recent review by Windhorst [9], Kokkorogiannis poses the following question: what does the abundance and distribution of muscle spindles tell us about their role in motor control? To begin with, I would like to draw a distinction between two very different roles muscle spindles play in motor control, as pointed out by Merton [5]. The review by Windhorst focuses on one aspect, the unconscious, automatic reflex regulation of posture and movement. The second, quite distinct, role is in proprioception, more specifically, kinaesthesia, the sense of position and movement of body parts [7]. The distinctness of these two roles is brought out by the very different contributions made to them by the fusimotor system. As Windhorst points out (P165), in locomotion specific roles have been proposed for the static and dynamic fusimotor systems. By contrast, during voluntary movements co-activation of fusimotor fibres poses a problem for spindles as kinaesthetic sensors. The current view is that fusimotor-evoked spindle impulses are a potential source of ambiguity and they are therefore postulated to be simply subtracted out at supraspinal levels, as a means of allowing access to length and movement-related spindle information [4]. Kokkorogiannis bases his questions about the role of muscle spindles on a survey he carried out some time earlier [3]. In that work he concluded that, (1) spindles tended to lie in the oxidative parts of a muscle and (2) this preference was able to



DOI of original article:10.1016/j.brainresbull.2007.10.001. Tel.: +61 3 9905 2526; fax: +61 3 9905 2531. E-mail address: [email protected]

0361-9230/$ – see front matter © 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.brainresbull.2007.10.003

account for their distribution and abundance. In his letter to the editor he points out that these observations must be incorporated into any attempt aimed at explaining the physiological function of muscle spindles. For the first point I am going to opt for the intuitively most obvious explanation. Muscle spindles commonly lie within the oxidative portions of a muscle, including close to blood vessels, because of their metabolic requirements. Spindles typically generate significant levels of background activity, no matter what the muscle length and we now know that this plays a role in spinal reflex action as post-activation depression [6]. Given the complexity of the receptors, the presence of multiple sensory and motor terminals and ongoing activity, it seems reasonable to suppose that metabolic requirements are responsible for spindles adopting an “angiotypic” distribution. The second point is less straight-forward. Kokkorogiannis poses the question, why should a muscle like the human gluteus maximus contain as many as 625 spindles while muscles concerned with finely skilled movements like the intrinsic muscles of the hand contain only 20–50 spindles? This trend is represented across muscles by a power law relation between the size of the muscle and its spindle content [3]. I do not have a simple answer to this question but would like to put forward a proposal that may provide a clue. In 1983, Hall and McCloskey [2] confirmed the old observation, first made by Goldscheider in 1889 that in humans detection thresholds for imposed movements are lower at proximal joints than at distal joints. Hall and McCloskey went on to show that thresholds for different limb segments could be made the same by expressing them in terms of muscle fascicle length changes. They concluded

U. Proske / Brain Research Bulletin 75 (2008) 502–503

from their data that muscle fascicle length was a parameter of importance for the central nervous system. My colleagues and I [8] entered the debate by pointing out that the lengths of muscle spindles across muscles were not very different [1]. Yet muscle fascicles were very much longer in the larger muscles. If detection threshold in terms of percent fascicle length change was about the same for all muscles, it argued that where the spindles were much shorter than the adjacent fascicles they signalled length changes in only a portion of the fascicle [8]. In intrinsic hand muscles spindles were much more likely to run from one end of the muscle to the other than in a muscle like gluteus maximus. Perhaps the large number of spindles in muscles like gluteus maximus is a reflection of the number of fascicles comprising such muscles. To conclude, if, as seems to be the case, muscle fascicle length is a physiological variable of importance for the central nervous system, it is conceivable that muscles with a larger number of fascicles require more spindles, particularly since each spindle is likely to signal length changes in only a portion of the fascicle. The problem is less acute in smaller muscles with fewer fascicles, where spindles are likely to span the full length of the muscle. If all of this is correct then it is interesting to reflect on the fact that one clue about the distribution and abundance of spindles comes from their role in proprioception.

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Conflict of interest None. References [1] I.A. Boyd, The structure and innervation of the nuclear bag muscle fibre system and the nuclear chain muscle fibre system in mammalian muscle spindles, Phil. Trans. Roy. Soc., Lond. B 245 (1962) 81–136. [2] L.A. Hall, D.I. McCloskey, Detection of movements imposed on finger, elbow and shoulder joints, J. Physiol. 335 (1983) 519–533. [3] T. Kokkorogiannis, Somatic and intramuscular distribution of muscle spindles and their relation to muscular angiotype, J. Theor. Biol. 229 (2004) 263–280. [4] D.I. McCloskey, S.C. Gandevia, E.K. Potter, J.G. Colebatch, Muscle sense and effort: motor commands and judgements about muscular contractions, in: J.E. Desmdt (Ed.), Motor Control Mechanisms in Health and Disease, Raven Press, New York, 1983, pp. 151–167. [5] P.A. Merton, Human position sense and the sense of effort, Symp. Soc. Exp. Biol. 18 (1964) 387–400. [6] E. Pierrot-Deseilligny, D. Burke, The Circuitry of the Human Spinal Cord, Cambridge, New York, 2005. [7] U. Proske, Kinesthesia: the role of muscle receptors, Muscle Nerve 34 (2006) 545–558. [8] U. Proske, A.K. Wise, J.E. Gregory, The role of muscle receptors in the detection of movements, Prog. Neurobiol. 60 (2000) 85–96. [9] U. Windhorst, Muscle proprioceptive feedback and spinal networks, Brain Res. Bull. 73 (2007) 155–202.