Introduction Anatomical considerations [2] as well as some physio-
Brain Research 888 2001 348–355 www.elsevier.com locate bres
Interactive report
Summing responses of cat soleus muscle spindles to combined static
1
and dynamic fusimotor stimulation
James B. Fallon, Richard W. Carr, J. Edmund Gregory, Uwe Proske
Department of Physiology , Monash University, Clayton, Victoria 3168, Australia
Accepted 30 October 2000
Abstract
This is a study of the summation of responses of primary endings of muscle spindles to combined static and dynamic fusimotor stimulation in the soleus muscle of the anaesthetised cat. Summation, expressed as a summation coefficient, K, was measured under a
variety of conditions including 1 at several, fixed muscle lengths using steady rates of stimulation, 2 using ramp-shaped increases in stimulation rates, 3 during passive stretches after muscle conditioning, and 4 during combined stretch plus stimulation. The
predominant effect observed was occlusion, that is, the combined response was less than the sum of the two individual responses. The calculated mean K value for responses at fixed length was 0.156 60.005 S.E.M.. It was hypothesised that summation arose from
electrotonic spread of generator current between the afferent terminals, either directly, or as a result of mechanical interactions between the contracting intrafusal fibres. Summation for responses from pairs of static fusimotor fibres gave a larger mean K value, 0.340 60.020
S.E.M.. These findings were interpreted in terms of a model of the muscle spindle where responses to dynamic fusimotor stimulation arise at one impulse generating site, and static fusimotor responses arise at another.
2001 Elsevier Science B.V. All rights reserved.
Theme : Sensory systems
Topic : Somatic and visceral afferents
Keywords : Muscle spindle; Fusimotor; Electrotonic; Stretch; Contraction; Summation
1. Introduction Anatomical considerations [2] as well as some physio-
logical observations have led to the conclusion that the Mammalian muscle spindles, as stretch receptors, are
mammalian spindle is a two compartment receptor [14]. remarkably complicated structures. They consist of a
One compartment contains the bag fibre, its Ia terminal
1
bundle of intrafusal fibres, each supplied with terminals of and a g
fusimotor supply. The second compartment
dynamic
a Ia axon and by terminals of one or more group II axons. comprises the bag
and chain intrafusal fibres, their Ia
2
Added to that is a motor innervation for each intrafusal terminals and a g
fusimotor supply. So the spindle can
static
fibre and an enclosing, fluid-filled connective tissue cap- be thought of as responding to dynamic and static
sule. Muscle spindles have been studied intensively over fusimotor inputs from separate compartments which are
the last 40 years and much new knowledge has been served by branches of the one afferent.
gained. Why spend so much effort on this receptor and its The experiments described here are concerned with the
internal workings? We believe the spindle plays a major interactions that can occur between the two compartments
role in motor control and understanding how it works will of the spindle. Over the years evidence has accumulated in
give us important clues about central nervous strategies in support of the idea that afferent impulses may be generated
the control of posture and movement. at more than one site in the spindle. That has raised the
possibility of interactions, within the spindle afferent tree, between several, converging impulse streams. The current
1
Published on the World Wide Web on 1 December 2000.
view is that the bag terminal is one source of impulses,
1
Corresponding author. Tel.: 161-3-9905-2526; fax: 161-3-9905-
the other being the terminals on bag and chain fibres.
2531.
2
E-mail address : uwe.proskemed.monash.edu.au U. Proske.
Since the Ia axon supplies both compartments, it has been
0006-8993 01 – see front matter
2001 Elsevier Science B.V. All rights reserved. P I I : S 0 0 0 6 - 8 9 9 3 0 0 0 3 1 1 5 - 2
J .B. Fallon et al. Brain Research 888 2001 348 –355
349
postulated that there is mixing of impulse traffic from these withdrawal reflexes and assessing the level of muscle tone.
two sources, leading to pacemaker switching when one The animal’s body temperature was monitored using a
input is at a higher rate than the other [3,6,11]. These rectal probe, and maintained in the range 38618C using a
considerations have led to models of impulse initiation in thermal blanket.
the spindle [4,12]. When discharge rates from different A laminectomy was performed exposing the lumbo-
pacemakers are similar, it has been proposed that there sacral spinal cord from L6 to S2. Dorsal and ventral roots
may be probabilistic mixing of the two impulse streams were cut where they entered the cord and the peripheral
[7]. Finally, on the basis of the amount of summation of Ia portions dissected into small filaments to obtain func-
responses to combined static and dynamic fusimotor tionally single afferent and motor axons. The left soleus
stimulation, it has been proposed that generator current muscle and its tendon were dissected free and the tendon
from one impulse generator may spread along the peripher- attached via a fragment of calcaneum to an electromag-
al afferent tree to influence rates of firing at the second netic muscle stretcher regulated by feedback. Muscle
generator [1]. lengths were referred to the maximum in situ physiological
But does it actually matter whether there is leakage of length L . Muscle tension was monitored using an in-
m
receptor currents between generators? More generally, series strain gauge placed between the stretcher and the
does it matter what kinds of interactions take place muscle. The left hindlimb was extensively denervated,
between different spindle compartments? In a recent study including the hip, but sparing the nerve to soleus. Skin
of the responses of spindles during treadmill locomotion of flaps of the hindlimb and back were fashioned into pools
the decerebrate cat, patterns of fusimotor activity were filled with mineral paraffin oil and warmed with radiant
deduced from discharge profiles of the Ia afferents [17]. heat.
The aim was to obtain insight into central nervous strate- Action potentials were converted to TTL pulses and
gies making use of the fusimotor system during locomo- recorded digitally using a commercial analog to digital
tion. One complication considered was the electrotonic converter PCI-MIO-16E-4, National Instruments Corp.,
interaction from
receptor currents
between impulse
Austin, Texas, USA and a Power Macintosh computer. generators. It was found that when allowance was made for
The recording and analysis were done using the software this kind of interaction, the response profiles predicted
package Igor Pro WaveMetrics, Lake Oswego, Oregon, from known intrafusal activation patterns could be iden-
USA. tified. In other words, understanding the processes within
Afferent axons, dissected in filaments of dorsal root, the spindle allows interpretation of its afferent responses in
were identified as lying in the group I range by their terms of an underlying motor strategy.
conduction velocity. This was calculated from the latency Here we re-examine the evidence for electrotonic spread
of the recorded action potential in the root filament in of current from one generator to the other. In the main, we
response to stimulation of the muscle nerve and the agree with the earlier conclusions that response summation
conduction distance between stimulating and recording seen with combined static and dynamic fusimotor stimula-
electrodes. Afferents were identified as coming from tion is due to electrotonic effects [1]. However, we view
muscle spindles by their ‘in parallel’ behaviour, interrup- this interaction not just as a simple spillover of current
tion of their discharge during a muscle contraction. from one generator site to another, between spindle
Fusimotor axons were isolated in filaments of ventral root compartments which remain independent of one another in
and were identified by the excitatory effect of their all other respects. Some of the observed behaviour is
stimulation on spindle afferents in the absence of extrafus- consistent with the idea that the amount of current gener-
al tension. They were classified as static or dynamic by the ated at one site is influenced by transmission of forces
effect of their stimulation at 100 pulses per second pps between adjacent contracting intrafusal fibres.
on spindle afferent responses to a ramp-and-hold muscle stretch of 5 mm at 10 mm s [8].
Fusimotor axons were stimulated, alone and in pairs, in