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Historical Perspective: Centenary Series: 1 |
1 Department of Physiology, Monash University, Melbourne, Victoria, Australia
(Received 15 August 2007;
accepted after revision 31 August 2007; first published online 14 December 2007)
Corresponding author U. Proske: Department of Physiology, Monash University, Clayton, Victoria 3800, Australia. Email: uwe.proske{at}med.monash.edu.au
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In my view, there is one other candidate for top place in Peter's publications. It is the paper with Guy Goodwin and Ian McCloskey, demonstrating that afferents of muscle spindles contribute to the sense of position and movement of our limbs (Goodwin et al. 1972). But instinctively we tend to give priority over observations in psychophysics to new observations in physiology. Still, there are very few of us in the privileged position of being able to consider more than one publication as outstanding in its field.
The paper on the motor innervation of the spindle described for the first time that stimulation of functionally single fusimotor fibres had two quite distinct effects. One fibre type, called ‘dynamic fusimotor fibres’, as well as exciting the spindle while the muscle was held at constant length, selectively increased the dynamic component of the response to a stretch. The second type, called ‘static fusimotor fibres’, excited the spindle more powerfully when it was held at constant length and, rather than increasing, it reduced the dynamic response during a stretch. The majority of primary endings of spindles appeared to be able to be modified in these two distinct ways by fusimotor stimulation. Since that report, the observations have been repeated and extended many times and they have led to volumes of discussion about their significance. That debate continues up to the present day and we are obliged to admit that a full understanding continues to elude us even now.
The only time that my own work came close to this story was during the heyday of spindle physiology. Yves Laporte, Francoise Emonet-Denand, Michael Stacey, David Barker and I showed, using selective degeneration methods, that the static fusimotor fibres terminated on intrafusal fibres as trail endings (Barker et al. 1973). By inference, dynamic fusimotor fibres terminated as plate endings, although that was never shown conclusively.
A clue about how the two kinds of fusimotor fibre exerted their effects on the spindle was provided by some observations made by Michael Brown, working in Peter Matthews's laboratory on frog muscle (Brown, 1971). He suggested that the intrafusal fibre innervated by dynamic fusimotor fibres (Bag 1) resembled frog tonic muscle in its mechanical properties. Local, non-propagated activity was associated with a low turnover rate of cross-bridges between actin and myosin in sarcomeres and a slow contraction. With the stretch rates typically used on spindles, this represented an effective increase in intrafusal fibre viscosity with little accompanying fibre shortening. That led to a large increase in the dynamic response of the spindle during the stretch, but only weak effects when the muscle was held at constant length. For the static fusimotor system, in contrast, intrafusal activity (Bag 2 and Chain) was actively propagated and contractions were faster. The higher cross-bridge turnover rate meant that a stretch of the contracting intrafusal fibre could be resisted with less viscosity than for the passive fibre, leading to a fall in the dynamic response. This was accompanied by substantial intrafusal shortening, producing a large increase in static response.
How did Peter Matthews arrive at his major piece of insight? The key observations that led to the report in the Quarterly Journal were made together with Jan Jansen from Oslo. Jan had originally come to Oxford to work with Charles Phillips. In the event, he agreed to do some experiments with Peter. Together they studied the static and dynamic sensitivities of primary and secondary endings of spindles in the decerebrate cat, before and after reflex stimulation or ventral root section (Jansen & Matthews, 1962).
We now know that in the intercollicular decerebrate cat there is spontaneous fusimotor activity, probably both static and dynamic. Jansen and Matthews found that fusimotor activity (ventral roots intact) did not appear to alter the responses of secondary endings, other than increasing their static response. However, they did obtain evidence for independent control of static and dynamic responses of primary endings. The large dynamic response seen during stretch of the muscle could be selectively and reversibly suppressed by stimulation of the anterior lobe of the cerebellum (their Fig. 9), presumably the result of a strong static fusimotor action. Peter must have noticed this dual behaviour and drawn the important conclusion that it was mediated by two different kinds of fusimotor fibre. In any case, shortly after Jan Jansen's return to Norway, Peter embarked on a series of experiments to put this idea to the test. The significant technical improvement that he incorporated into his new experiments was to isolate, by dissection of the ventral root, functionally single fusimotor fibres. It meant that if there were two types of fusimotor fibre this would be revealed during their selective stimulation; and so it was (Figs 1 and 2 in Matthews, 1962).
This is not the place to give a detailed account of the subsequent developments of our ideas about the role of the muscle spindle and its fusimotor innervation. However, several simple points are worth making. In my lectures to students I begin by pointing out the dual role of spindles, enunciated so clearly by Pat Merton. He refers, on the one hand, to the role of spindles in the stretch reflex and, on the other, to their contribution to the kinaesthetic sense. He concludes, ‘Until the underlying incompatibility of these two notions is felt one cannot properly appreciate the character of the problems that face us in this field’ (Merton, 1964). When we think about the functional role of spindles, it is worth keeping this problem in mind.
When, in my lecture I try to assign functional significance to the fusimotor innervation of spindles, I take the view put much more elegantly by Peter himself (Matthews, 1981). The static fusimotor system prevents spindle silencing during muscle shortening, allowing the central nervous system to receive feedback throughout the movement. The dynamic system is unable to do that since it is associated with an intrafusal contraction that is too slow to follow extrafusal shortening. It is probably concerned with gain control during small perturbations and with phase lead and maintenance of spindle sensitivity during large movements.
Recent experiments on humans have shown that during voluntary movements there is evidence of coactivation of both static and dynamic fusimotor neurones (Kakuda & Nagaoka, 1998). We will have to keep that in mind when thinking about the role of spindles in human motor control, including their capacity to signal kinaesthetic information during active movements. Other recent experiments on decerebrate cats walking on a treadmill (Taylor et al. 2006) have led to the conclusion that static fusimotor activation may act as a ‘temporal template’ of the expected movement, thereby expanding the range of movements over which the spindle is able to provide an adequate feedback signal. The dynamic fusimotor pattern deduced from these studies suggests that this is concerned with detection of the onset of muscle lengthening during locomotion, as well as allowing the spindle to promptly signal any departure from the intended trajectory of the movement.
To conclude, the account of two distinct types of fusimotor fibre by Peter Matthews in 1962 represented a major step forward in our understanding of the physiology of the mammalian muscle spindle. The step is so significant that we are still trying to digest its full meaning.
References
Barker D, Emonet-Denand F, Laporte Y, Proske U & Stacey MJ (1973). Morphological identification and intrafusal distribution of the endings of static fusimotor axons in the cat. J Physiol 230, 405–427.
Brown MC (1971). The responses of frog muscle spindles and fast and slow muscle fibres to a variety of mechanical inputs. J Physiol 218, 1–17.
Goodwin GM, McCloskey DI & Matthews PBC (1972). The contribution of muscle afferents to kinaesthesia shown by vibration induced illusions of movement and by the effects of paralysing joint afferents. Brain 95, 705–748.
Jansen JKS & Matthews PBC (1962). The central control of the dynamic response of muscle spindle receptors. J Physiol 161, 357–378.
Kakuda N & Nagaoka M (1998). Dynamic response of human muscle spindle afferents to stretch during voluntary contraction. J Physiol 513, 621–628.
Matthews PBC (1962). The differentiation of two types of fusimotor fibre by their effects on the dynamic response of muscle spindle primary endings. Q J Exp Physiol Cogn Med Sci 47, 324–333.
Matthews PBC (1981). Evolving views on the internal operation and functional role of the muscle spindle. J Physiol 320, 1–30.
Merton PA (1964). Human position sense and sense of effort. Symp Soc Exp Biol 18, 387–400.[Medline]
Taylor A, Durbaba R, Ellaway PH & Rawlinson S (2006). Static and dynamic 
-motor output to ankle flexor muscles during locomotion in the decerebrate cat. J Physiol 571, 711–723.
Acknowledgements
I would like to thank Peter Matthews for his helpful comments on the background to his paper and on this manuscript.
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