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First published online May 8, 2007
Journal of Experimental Biology 210, 1661-1662 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.000695
JEB Classics |
MOTOR INNERVATION OF THE MUSCLE SPINDLE: THE CONTRIBUTION OF BERNHARD KATZ
Imperial College, London
t.taylor{at}imperial.ac.uk
Anthony Taylor discusses Bernhard Katz's 1949 paper entitled: The efferent regulation of the muscle spindle in the frog. A copy of the paper can be obtained from http://jeb.biologists.org/cgi/reprint/26/2/201.
In this article, we go back over 55 years to the paper by Bernhard Katz in
The Journal of Experimental Biology
(Katz, 1949
). Although its
subject has since been researched in more detail and with more sophisticated
techniques, this paper still has much to teach us regarding clear thinking,
simple but elegant experimentation and farsighted discussion.
By the time of this publication, the classical histological studies of the
muscle spindle had shown that it consisted of a bundle of slender striated
muscle fibres enclosed in its central region by a connective tissue capsule,
in both amphibia and in mammals. The central intrafusal fibres in the muscle
spindle are surrounded by sensory receptors that respond to stretch in the
muscle. The capsule is surrounded by the extrafusal fibres, which generate the
muscle's force. In mammals, there are two types of sensory ending, the large
centrally placed primary endings and the smaller adjacent secondary endings
(see Ruffini, 1898). Both
types connect to the spinal cord via myelinated afferent, or sensory,
axons; larger and faster for the primaries than for the secondaries. However,
only one type of ending, similar to the primary, was seen in amphibia. The
intrafusal muscle fibres received a motor nerve supply, which had recently
been shown by Leksell to be derived in mammals from a special group of small
myelinated axons in the spinal ventral roots and referred to as
-efferent (Leksell,
1945). Stimulation of these axons caused no detectable contraction
but excited an afferent discharge from the spindles. This was seen as a means
by which the response of the spindles to muscle length change could be
modified by the central nervous system. At the same time it had been found
(Tasaki and Mizutani, 1944)
that extrafusal muscle fibres in amphibia were innervated by two distinct
motor systems. Motor neurons with large axons caused the familiar large fast
twitches with single stimuli, known as the twitch system, whilst motor neurons
with small axons required repetitive stimulation to cause slow and relatively
weak contractions, known as the tonic system.
There were two questions that Katz sought to answer in the frog
(Katz, 1949). First, whether
the large motor neurons could activate the intrafusal fibres. Second, whether
the small muscle fibre system in the frog acted only to generate tonus (a
state of prolonged muscle tension) in the extrafusal muscle, as described by
Stephen Kuffler and Ralph Gerard (Kuffler
and Gerard, 1947), or whether it could also `regulate the response
of the stretch receptor'. Curiously, Katz did not appear to be aware of
Leksell's results in the cat (Leksell,
1945) but quoted the suggestion of Matthews that in frogs there
was an intrafusal motor innervation from high-threshold axons (i.e. small
diameter) distinct from the extrafusal innervation
(Matthews, 1931).
As proved to be the case in all of Katz's subsequent work, the preparation was well-chosen and the methods elegantly simple. The small extensor longus digitorum, a lower leg muscle, was isolated with its nerve containing about 12 axons, of which three or four were sensory. One recording electrode was placed on the muscle and another close by on the nerve. Adjacent to this, Katz placed a pair of polarising electrodes to allow for differential and reversible block of conduction in the large motor axons, beyond which were the stimulating electrodes. In essence, he observed that stimulation of large, low-threshold, motor axons not only caused extrafusal contraction but also a short burst of afferent impulses. The afferent firing persisted when extrafusal contraction was blocked by critical dosage with the muscle relaxant curare, thus showing that the large motor axons branched to innervate intrafusal muscle fibres.
Another important finding was that when muscle shortening was allowed, the
tendency of extrafusal contraction to silence the spindle was offset by the
intrafusal contraction. Katz discussed the significance of this clearly, with
the proposal that when an extended muscle is contracted actively in life, the
inevitable simultaneous intrafusal contraction would ensure that afferent
activity continues, which would support the contraction against loading by
means of the stretch reflex. This concept was followed up later by recording
the spindle afferent activity from a toad muscle contracting actively against
springs of different compliance (Murthy
and Taylor, 1970).
One can see in Katz's idea the inspiration for subsequent work in mammals
on how the -efferent system described by Leksell
(Leksell, 1945) could be used
in controlling active muscle contraction. It became widely accepted that the
-efferent neurons are generally activated in parallel with the
-motor neurons that supply the extrafusal muscle, a concept referred to
as `alpha–gamma coactivation'. Despite the apparent success of his
method for restricting stimulation to the small motor axons, Katz was not able
to show clear evidence for an effect of them on the intrafusal muscle.
However, it was later evident that tetanic stimulation is necessary to
activate the tonic muscle fibres, which then do indeed excite the spindle
afferents (see review by Eyzaguirre,
1962). However, it was not until the work of Brown that the true
significance of the fast and slow motor fibres in control of the amphibian
spindle became clear (Brown,
1971). The fast group caused an increase in the afferent firing at
any given length (biassing) and some reduction in the sensitivity to stretch.
The slow group caused a marked increase in stretch sensitivity with little
effect on resting frequency. In this way they may be seen to parallel the
behaviour of the static and the dynamic -motor fibres, respectively, in
mammals. These two classes were defined by the effect of their stimulation on
the afferent response to controlled muscle stretch
(Crowe and Matthews, 1964).
Nothing in science is ever quite new, but in this paper Katz showed ways of
studying the complexities of the muscle spindle that have been widely
influential since. In 1949, recovery from the chaos of World War II had
scarcely started, apparatus was relatively primitive and laboratory facilities
improvised. Katz had only returned to England from service in the Royal
Australian Air Force in 1946 to join A. V. Hill at University College London.
Any lack of resources was more than compensated for by the keen intellectual
atmosphere of the time. The frequent meetings of the Physiological Society,
rotating around all the Physiology departments, provided unlimited scope for
critical discussion of the latest work, and researchers vied with each other
to provide vivid live demonstrations (e.g.
Katz, 1950). It is evident that
Katz was strongly motivated to study the biophysical basis for physiological
mechanisms and would choose whatever preparation was most convenient and
appropriate for the current task, which at that time was to understand the
mechanisms of sensory reception. Consequently, he went on to use the frog
muscle spindle to study the local currents leading to the initiation of
sensory impulses and made no further contributions to understanding the motor
innervation of muscle spindles. Nevertheless, one can see that his one paper
on this subject inspired others and started a period of vigorous research,
revealing complexities which are still engaging widespread interest amongst
students of motor control (for reviews, see
Matthews, 1981;
Taylor et al., 1999).
References
Brown, M. C. (1971). The response of frog
muscle spindles and fast and slow muscle fibres to a variety of mechanical
inputs. J. Physiol. 218,1
-17.
Crowe, A. and Matthews, P. B. C. (1964). The
effects of stimulation of static and dynamic fusimotor fibres on the response
to stretching of the primary endings of muscle spindles. J.
Physiol. 174,109
-131.
Eyzaguirre, C. (1962). Motor regulation of the vertebrate spindle. In Symposium on Muscle Receptors (ed. D. Barker), pp. 155-166. Hong Kong: Hong Kong University Press.
Katz, B. (1949). The efferent regulation of the
muscle spindle in the frog. J. Exp. Biol.
26,201
-217.
Katz, B. (1950). The electric response at a sensory ending. J. Physiol. 109,9P -10P.
Kuffler, S. W. and Gerard, R. W. (1947). The small motor system to skeletal muscle. J. Neurophysiol. 19,383 -394.
Leksell, L. (1945). The action potential and excitatory effects of the small ventral root fibres to skeletal muscle. Acta Physiol. Scand. 10 (Suppl.), 31.
Matthews, B. H. C. (1931). The response of a
muscle spindle during active contraction of a muscle. J.
Physiol. 72,153
-174.
Matthews, P. B. C. (1981). The muscle spindles, their messages and their fusimotor supply. In Handbook of Physiology. The Nervous System. Motor Control (ed. J. M. Brookhart and V. B. Mountcastle). Bethesda: American Physiological Society.
Murthy, K. S. K. and Taylor, A. (1970). Muscle spindle response to active muscle shortening in Bufo marinus. J. Physiol. 213,28P -29P.
Ruffini, A. (1898). The minute anatomy of the
neuromuscular spindles of the cat, and on their physiological significance.
J. Physiol. 23,190
-208.
Tasaki, I. and Mizutani, K. (1944). Comparative studies of the activities of the muscle evoked by two kinds of motor nerve fibres. Part I. Myographic studies. Jap. J. Med. Sci. 10,237 -244.
Taylor, A., Ellaway, P. H. and Durbaba, R. (1999). Why are there three types of intrafusal muscle fibres? Progr. Brain Res. 123,121 -132.[Medline]
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