Collège de France, 75231 Paris Cédex 05, France
![]() |
ABSTRACT |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Emonet-Dénand, Françoise,
Yves Laporte, and
Julien Petit.
Comparison of the Effects of Stimulating Groups of Static Axons With Different Conduction Velocity Ranges on Cat Spindles.
J. Neurophysiol. 86: 533-535, 2001.
In
cat peroneus tertius muscles, static
axons were prepared in groups
of three to four according to the conduction velocity of their axons
(fast, intermediate, or slow). Effects of stimulating these groups (at
20, 30, and 50 Hz) on spindle ensemble discharges during sinusoidal
stretch (peak-to-peak amplitude, 0.5 mm; frequency linearly increasing
from 0.5 to 8 Hz in 10 s) were compared. Ensemble discharges were
obtained by digital treatment of the discharges in afferent fibers from
all the spindles in peroneus tertius as recorded from the muscle nerve.
Stimulation of each group prevented ensemble discharges from falling to
very low levels during shortening phases. However, this effect was
clearly larger when the group of fast-conducting axons was stimulated.
In view of the known effects of the activation of
bag2 and chain fibers (either separately or
together) on single primary ending discharges during comparable sinusoidal stretches, this stronger effect supports the view that static
axons with faster conduction velocities are more likely to
supply more bag2 fibers than slower ones.
Possibly the proportions of bag2 and chain fibers
activated during motor activity are determined by a recruitment of
static
motoneurons related to their size.
![]() |
INTRODUCTION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Nonspecific static axons,
that is,
axons supplying both chain and bag2
intrafusal muscle fibers in various proportions, were demonstrated in
histophysiological studies (Banks 1991
; Barker et
al. 1973
) as well as in exclusively electrophysiological ones (Celichowski et al. 1994
; Emonet-Dénand et
al. 1998
). The high incidence of these axons contradicts
Boyd's view (Boyd 1986
) that static
axons are
divided into two groups of axons almost exclusively supplying either
bag2 or chain fibers (specific axons). However, static
axons supplying bag2 fibers
whether
specific or nonspecific
tend to have faster conduction velocities than
axons supplying chain fibers only (Banks 1991
;
Emonet-Dénand et al. 1998
). This tendency suggests
that the proportions of the two kinds of intrafusal muscle fiber
activated during various movements could be determined by a recruitment
of static
motoneurons based on their size, very likely matched to
the diameter (and thus to the conduction velocity) of their axons, as
with
motoneurons.
In the present study, to increase the chances of observing this
tendency and its functional consequences, groups of three to four
static axons supplying cat peroneus tertius muscle spindles were
prepared, each one comprising axons in the same (fast, intermediate, or
slow) conduction velocity range. The effects of stimulating each group
were studied on the responses to a sinusoidal stretch of all the
spindles its axons supplied. This was done (see
METHODS) by integrating and smoothing the massed afferent
activity in the muscle nerve of all the spindles of the peroneus
tertius muscle (on average 14 spindles) (Scott and Young
1987
).
![]() |
METHODS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The experiments were carried out on peroneus tertius muscles of
adult cats anesthetized with pentobarbital sodium (Nembutal, 45 mg/kg
ip) supplemented intravenously as required. The electrical activity of
spindle Ia and II afferent fibers was recorded from the thin peroneus
tertius nerve, which was freed from surrounding tissues over 10-15 mm.
This nerve segment, in continuity with the body of the animal and
immersed in oil, was slightly lifted in its middle part by a single
hook-shaped silver recording electrode. When both the number of active
fibers and their discharge frequencies increased, as is the case during
stimulation of several axons (in this muscle the majority of static
axons supply 3 or 4 spindles) (Celichowski et al. 1994
;
Emonet-Dénand et al. 1998
), an electrical activity
with a complex form resulting from the superimposition of action
potentials of afferent fibers was observed. This activity was digitized
at a sampling rate of 10 kHz and recorded with a microcomputer. The
signal was digitally rectified and smoothed by a mobile mean over 30-ms
periods. The contribution of primary endings to the ensemble discharges
obtained in this way was predominant because of the large size of Ia
action potential. Discharges from Golgi tendon were negligible because
no skeletal muscle fibers were activated in these experiments. Action
potentials of
static axons stimulated in ventral root filaments did
not significantly contribute to the ensemble discharges because their
amplitude was very small. Stimulation artifacts were almost completely eliminated.
In each experiment, the function, static or dynamic, of each
functionally single axon prepared (up to 25) was determined by
observing the changes its stimulation elicited in test responses to a
trapezoidal stretch generated by a servo-controlled electromagnetic puller to which the muscle tendon was attached (see
RESULTS). Then all filaments with either single dynamic
axons or with axons whose stimulation elicited weak nonidentifiable
effects were eliminated. These latter axons (whose conduction velocity
was generally lower than 25 m/s) were likely static axons supplying
only one or two spindles because dynamic axons commonly supply more
than four spindles. The conduction velocity range of the static axons
was divided into three approximately equal subranges. Ventral root filaments (3-4) containing single static axons with conduction velocities in a given subrange were mounted on the same stimulation electrode. The effects of stimulating the different groups at 20, 30, and 50 Hz were observed on spindle ensemble discharges during a
sinusoidal stretch (0.5-mm peak-to-peak amplitude) whose frequency
linearly increased from 0.5 to 8 Hz in 10 s. Three resting muscle
lengths were used: 1, 2, and 3 mm shorter than maximal physiological
muscle length (see Emonet-Dénand et al. 1997
). Temperature was maintained at 38°C. On the six experiments devoted to
this study, only two were successfully carried out because of the
difficulties of preparing groups of axons and of maintaining them in
good conditions during prolonged experimental procedures. Nevertheless
the clear difference we observed between the action of the fastest
group and that of the other groups seems to us worth reporting.
![]() |
RESULTS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Identification of the function of single axons
This identification was based on the changes elicited by the
stimulation of single axons at 100 Hz in responses to trapezoidal muscle stretches (ramp stretch, plateau, ramp shortening). As shown by
Fig. 1A, the test response
features were comparable to those of instantaneous frequency records of
primary ending discharges in single Ia fibers except during ramp
shortening because the persistence of secondary ending discharges in
this phase prevented the complete cessation of ensemble discharge.
Figure 1B shows the effects of stimulating at 100 Hz an axon
that can be identified as static by analogy with changes in single Ia
fiber discharges observed in comparable situations. The ensemble
discharge strongly increased at constant length, was further augmented
during the ramp stretch, and maintained a high level during the plateau
phase with a moderate slow decline. During the shortening ramp, the ensemble discharge fell sharply but, even at its lowest level, was
still much higher than before stimulation, a typical feature of static
action. Figure 1C shows the very different changes ascribed to the stimulation of a dynamic axon. The ensemble discharge, after a
moderate increase at constant length, considerably increased during the
ramp stretch and fell markedly as soon as the ramp stretch ended. It
moderately decreased during the plateau phase and during ramp
shortening, fell to a level well below that of the prestimulation
period.
|
Comparison of the effects of stimulating static axon groups
with different conduction velocity ranges
In the experiment illustrated by Fig. 2, three groups of four axons each were prepared. The first one was composed of axons with the faster conduction velocities (46, 40, 40, and 38 m/s), the second of intermediate velocities (34, 33, 30, and 29 m/s), and the third of slow velocities (27, 25, 22, and 21 m/s).
|
Figure 2A shows the spindle ensemble discharge during a
sinusoidal stretch of linearly increasing frequency in the absence of
stimulation. This passive response presents nearly sinusoidal oscillations whose amplitude progressively increased beyond 2- to 3-Hz
stretch frequencies. During the shortening phases, although practically
all primary endings stopped firing, the ensemble discharge did not
entirely cease because of the persistence of most secondary endings discharges.
The changes in the passive response elicited by stimulating at 50 Hz
the group of the slow axons or that of the fast ones are illustrated by
Fig. 2, B and C, respectively. They show that whatever the group stimulated, the minimal level in each oscillation was much higher than in the passive condition (this level had its
highest value during the 0.5-Hz cycle and progressively decreased as
the cycles shortened). However, when the fast-conducting axons were
stimulated (Fig. 2C), the minimal level in each
oscillationespecially in the lower range of stretch frequencies
was
clearly above that observed in corresponding oscillations during the
stimulation of the slower groups (Fig. 2B)
the maximal
level being the same. This difference shows that intrafusal muscle
fibers activated by fast static
axons have a stronger capacity for
counteracting the slowing effect of muscle shortening than muscle
fibers activated by slower axons. Stimulation at lower frequencies (20, 30 Hz) elicited weaker but comparable effects. The resting muscle
length did not affect the difference between groups.
![]() |
DISCUSSION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The stronger action of the faster group of static axons can be
interpreted from the known effects of the activation of
bag2 and chain fibers, either separately or
simultaneously, on single primary ending discharges during comparable
sinusoidal stretch (Emonet-Dénand et al. 1997
). It
was observed that during the phases of muscle shortening, the
coactivation of the two kinds of fiber was capable of preventing
primary endings from falling silent in a way similar to that observed
in Fig. 2, whereas the activation of the fast-contracting chain fibers
alone elicited a quite different pattern especially because the lowest
discharge frequency observed during each oscillation was exactly that
of the stimulation of the axon supplying these fibers (see Fig. 5 in
Emonet-Dénand et al. 1997
). This is why
the stronger action of the group of fast conducting axons supports the
view that among the intrafusal muscle fibers activated by these axons,
the proportion of bag2 fibers is larger than
among intrafusal muscle fibers activated by slower axons. In agreement
with this view, is the observation that activation of the slow
contracting bag2 fiber alone is capable of
counteracting the effects of muscle shortening on primary ending discharges only in the slowest range of shortening velocities, that is,
in the range where the action of fast axon groups is the strongest.
In conclusion, by developing a method for evaluating the activity of
the entire spindle population of a muscle and by comparing the effects
of stimulating groups of static axons of different conduction
velocities, evidence supporting the view that fast conducting static
axons supply more bag2 fibers than slow ones was
obtained, making it possible to consider that the proportions of
bag2 and chain fibers activated during motor
activity could be determined by the size of recruited
motoneurons.
![]() |
ACKNOWLEDGMENTS |
---|
The authors are very grateful to R. Banks and L. Jami for critically reading the manuscript and to S. de Saint Font for preparing it.
This study was supported by the Association Française contre les Myopathies and the Fondation pour la Recherche Médicale.
![]() |
FOOTNOTES |
---|
Present address and address for reprint requests: J. Petit, Faculté des Sciences du Sport et de l'Education Physique, Université de Bordeaux 2, Domaine Universitaire, 12 avenue Camille Jullian, 33607 Pessac Cedex, France (E-mail: julien.petit{at}u-bordeaux2.fr).
Received 8 June 2000; accepted in final form 12 March 2001.
![]() |
REFERENCES |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
Visit Other APS Journals Online |