PROPRIOCEPTIVE CONTROL OF POSTURE IN THE CRAYFISH ABDOMEN*

16 Pages·2005·2.02 MB·English

J. Exp. Biol. (1966), 44, 4SS-468 45 5
With a plates and 6 text-figures
Printed in Great Britain
PROPRIOCEPTIVE CONTROL OF POSTURE IN
THE CRAYFISH ABDOMEN*
BY HOWARD L. FIELDSf
Department of Biological Sciences and Neurological Sciences Program,
Stanford University, Stanford, California
(Received 8 November 1965)
Sense organs responsive to the changes produced by an animal's own musculature
are common in complex, flexible motor systems, and it is probably safe to assume that
proprioceptive feedback is required for these systems to operate with precision. The
crustacean muscle receptor organ (MRO) first described by Alexandrowicz (1951) has,
because of its accessibility, ease of isolation and hardiness, proven particularly amenable
to electrophysiological study. However, the study of this receptor has until recently
been confined to mechanisms of transduction and to the excitatory and inhibitory
control of its output.
The crayfish abdominal musculature is segmented and bilaterally symmetrical. The
extensor musculature in each half-segment consists, as does the flexor system (Kennedy
& Takeda, 1965 a, b), of relatively massive deep muscles and thin superficial ones. It
has been shown (Fields & Kennedy, 1965; Kennedy & Takeda, 1965 a) that the thin
superficial extensors and flexors both give graded electrical and mechanical responses
to repetitive stimulation of the motor nerves and maintain postural tension through
tonic activity on the part of the motoneurones supplying them. The more massive
deep muscles respond with a powerful twitch to single impulses in their motor nerves
(Kennedy & Takeda, 1965 a; Abbott & Parnas, 1965). All available evidence indicates
that, although the powerful contractions responsible for the swimming reflex involve
the deep twitch muscles, most slower movements are accomplished by the thin, slowly
contracting superficial muscles (Kennedy & Takeda, 1965 a).
Paralleling this division into tonic and twitch extensor muscles, the two muscle
receptor organs have been shown to differ from each other both in their response to
maintained stretch (Wiersma, Furshpan & Florey, 1953) and in the properties of their
receptor muscles (Kuffler, 1954) which are arranged in parallel with the adjacent
extensor muscles. The discharge frequency of the lateral MRO is maintained for up
to several hours while the more medial receptor adapts completely within seconds.
The muscle associated with the slowly adapting receptor (RMi) is thin, coarsely
striated and develops tension in graded increments proportional to the discharge
frequency of its motor nerve. The muscle of the rapidly adapting receptor (RM2) is
thicker and more finely striated than RMi and is capable of responding with a twitch
to single impulses in its motor nerve. In addition, it has recently been shown (Fields &
Kennedy, 1965) that RMi is supplied by branches of one or two of the five excitatory
• Supported by giants (to Dr Donald Kennedy) from the U.S. Public Health Service (B-2944) and
the U.S. Air Force Office of Scientific Research (AF-AFOSR).
f Present address: Department of Physiology, University College London, England.
456 HOWARD L. FIELDS
motoneurones supplying the superficial extensors, whereas RM2 is generally supplied
by a branch of one of the motoneurones to the deep twitch extensors.
These facts suggest that the two receptors provide the crustacean central nervous
system with different types of information. In contrast to the rapidly adapting (phasic)
receptor, the tonic receptor is capable of supplying the tonic proprioceptive input
required for operation of the slow, postural muscles. In the absence of motor input
the response of the phasic receptor is more directly related to rate of change of tension
and/or length of its muscle than to the steady-state length of the RM. It may be that
information concerning both change of muscle length and its first time-derivative is a
general requirement for operation of motor systems; in fact, Bessou & Laporte (1962)
have shown that the dynamic response of the primary ending of the vertebrate muscle
spindle is related to rate of change of muscle length, whereas that of the secondary
ending is more directly a function of instantaneous muscle length.
The experiments presented below demonstrate that the tonic receptor functions
specifically in the segmental control of slow, postural movements and strongly suggest
a separation of function between tonic and phasic MROs. A preliminary report of
some of the findings has appeared elsewhere (Fields & Kennedy, 1965).
METHODS
All experiments were carried out on Procambarus clarkii collected locally and main-
tained in tap-water tanks, in which the animals remained in good condition for several
weeks. Three types of preparation were used. Most commonly, the abdomen was
separated from the animal by a cut just anterior to the first abdominal segment, a
procedure which minimized bleeding. Alternatively, intact animals or those in which
the haemolymph had been replaced by van Harreveld's (1936) solution were used. The
parameters measured were not significantly dependent on the method of preparation.
Dissections were carried out with the preparations pinned dorsal side up on paraffin
in a Perspex dish filled with van Harreveld's solution. The extensor musculature was
exposed by careful removal of parts of the dorsal exoskeleton and then the hypodermis,
leaving the muscle attachments intact.
Wiersma et al. (1953) found that the nerve trunk supplying the extensor muscles,
a dorsal continuation of the second root, splits into three major branches (see Fig. 1):
the nerve to the profundus muscles (n.p.m.), the nerve supplying the MROs and the
superficial extensors [n.r.m. or dorsal nerve), and the nerve supplying tactile hairs in
the exoskeleton (n.cs. or superficial nerve). In those experiments in which a controlled
source of excitatory input to slow extensor motoneurones was desired, the superficial
nerve—which contains tactile afferents found to be excitatory to these motoneurones—
was dissected free for electrical stimulation, leaving its central connexions intact, and
draped over a pair of micromanipulated platinum wires. Brief (0-2—0-4 msec.) square
pulses were led through an RF isolation unit to these stimulating electrodes. By
comparing the latency and stimulus strength required to elicit motoneurone activity
before and after cutting n.cs., the possibility of direct stimulation of motoneurones
by current spread could be ruled out. When natural stimulation was used, a rninimum
of dissection was required to permit access to the extensor muscles for identification
and recording.
Proprioceptive control of posture in the crayfish abdomen 457
Motoneurone activity was monitored by recording junctional events in muscle
fibres with glass capillary microelectrodes suspended from a micromanipulator by a
fine silver wire. These 'floating' microelectrodes remained in actively contracting
muscle fibres without damage either to the fibres or to the electrode tips. The capil-
laries were filled with 3 M-KC1 and had resistances ranging between 10 and 40 Mii.
Intracellularly recorded signals were led through neutralized capacity preamplifiers
(Amatniek, 1958). Receptor activity was monitored by lifting the intact dorsal nerve
up out of the solution into a pool of paraffin oil with a hook electrode of fine platinum
wire. The signal in this case was led through a Grass P 5 capacity-coupled preamplifier.
In some experiments motoneurone action potentials were also recorded from n.r.m.;
in this manner both muscle and nerve potentials were displayed on a conventional
dual-beam oscilloscope and recorded photographically.
d.e.o /. RM1
RM2
d e a.m.
Fig. 1. Superficial view of the left extensor musculature of segment III in Procambarus clarhd.
RMi, RMi, Receptor muscles; d.e.a.nu, medial head of deep extensor; d.e.a.l., lateral head
of deep extensor; s.e.L, lateral head of superficial extensor; t.e.m., medial head of superficial
extensor; n.r.m., dorsal nerve; rt.p.m., nerve to the deep extensors; n.c.s., superficial nerve; H,
patch of hypodermis; II, second root; T3, tergite of segment III; T\, tergite of segment IV.
In order to study the output of the MROs in as nearly intact a state as possible, and
to correlate receptor output with abdominal position, the following procedure was
employed. A completely intact crayfish was suspended by a carapace clamp, either in
water or air, and a pair of small-diameter pins (Minutenadeln), with insulation removed
only at the tip, were inserted directly through the tergite on one or both sides of a
segment and led through a capacity-coupled preamplifier to the oscilloscope. The two
pins were placed towards the centre of the half-tergite. Under these conditions the
spikes of both fast and slow stretch receptors were large enough to be easily identified,
and could be distinguished from one another by their response to manual flexion of
the tail. The output of the stretch receptor was correlated with movements of the tail
by simultaneously photographing, with separate cameras, the oscilloscope trace and
the crayfish. The animal was illuminated with a stroboscopic light source, which was
arranged in such a way that it also produced a reflexion 'artifact' on the oscilloscope
trace. This allowed correlation of each strobe frame with a segment of the oscilloscope
record. All experiments were carried out at 10-15° C.
458 HOWARD L. FIELDS
RESULTS
Results reported earlier (Fields & Kennedy, 1965) have shown that activity in slow
extensor motoneurones is consistently evoked by stretching the receptor muscles with
a fine wire hook, and en passant recording from the dorsal nerve established that this
motoneurone activity is quantitatively correlated with discharge in the MROs. In the
absence of other excitatory input to the motoneurones the relationship of firing
frequencies in the sensory and motor axones was found to be approximately linear.
Central effects of phasic and tonic receptors
By separately stretching RMi and KM 2 it was shown that activity in the slow
receptor alone is sufficient to evoke firing of ipsilateral slow extensor motoneurones
but has no demonstrable effect on motoneurones supplying the deep extensors. Dis-
charge of the fast stretch receptor, even at frequencies exceeding those which in the
slow receptor are adequate to evoke motoneurone firing, produced no observable
activation of either superficial or deep extensor motoneurones. Fig. 2 demonstrates
Fig. 2. Difference in central effect of tonic and phasic MROs. Upper trace, an intracellular
recording from a slow extensor muscle fibre in s.e.l.; lower trace, an extracellular recording of
activity in the dorsal nerve. The phasic MRO (large spike) is ineffective in activating the slow
extensor motoneurone which produces the junctional potentials, whereas activity in the tonic
MRO (smaller spikes) evokes tonic activity in this motoneurone.
the apparent lack of functional overlap of the two receptors. In this experiment most
of the excitatory drive to the active motoneurone was produced by the slow receptor.
The mechanical arrangement was such that stretching KM2 unloaded tension on
KM 1; thus fast and slow receptors were activated alternately. Excitatory junctional
potentials occurred in slow extensor motoneurones only in response to KMx discharge.
Although there is no direct evidence for any central effect of the fast MRO except
self-inhibition (Eckert, 1961 a), it seems likely that its reflex function is associated with
control of the phasic deep extensors. The deep extensors are twitch muscles, incapable
of developing the fine gradations in tension required for slow changes in tail position;
and, in contrast to the superficial extensors, they do not show the tonic activity re-
quired for maintenance of a set position of the abdomen. No reliable method of
centrally activating fast extensors was found and consequently the role or the phasic
MRO in co-ordination of abdominal movements has not been established.
Much more detailed information was obtained concerning the central effects of the
tonic receptor. It was observed that the response of a motoneurone to discharge in
the tonic MRO, evoked by mechanical stretch of RMi, was highly dependent on
other sources of excitatory input. By electrical stimulation of tactile afferent fibres
Proprioceptive control of posture in the crayfish abdomen 459
In n.c.s. the level of central excitability could be raised high enough so that single
impulses in the slow MRO produced single motoneurone discharges (Fig. 3). How-
ever, under these conditions, the motoneurone followed receptor impulses on one-to-
one fashion only over a limited frequency range, dropping out at frequencies greater
than about two to three impulses per second. The latency from MRO spike to the
following motoneurone spike under conditions of one-to-one following was about
30 msec. Even under conditions of frequency division (i.e. more than one receptor
impulse per motoneurone impulse), the latency from the immediately preceding
receptor impulse to the motoneurone impulse remained at this value, provided drive
from other sources did not activate the motoneurone (see Fig. 3). However, this
latency figure gives little information about the number of interposed synapses since
the conduction velocity of fine fibres in the ganglionic neuropile is unknown.
-u.
20 mV.
300 msec.
Fig. 3. Central interaction of tactile and stretch receptor input to tonic motoneuronea. A nerve
containing only tactile afferent fibres (n.c.s.) was electrically stimulated (dots) at gradually
increasing intensity. RMi was stretched slightly to produce a steady background discharge in
the tonic MRO. Arrow labelled n in the upper trace indicates a spike in the tonic MRO; arrow
labelled m indicates an extracellular muscle potential, associated with the intracellular junctional
potential recorded in a slow extensor muscle fibre (lower trace). Stimulus intensity was greater
in B than A, and consequently each MRO impulse was more effective in eliciting a moto-
neurone impulse. In C, the stimulus intensity was equal to that in A but the MRO was dis-
charging at a higher frequency so that each MRO impulse is less effective m producing a
motoneurone impulse.
Identity of the motoneurone activated by the tonic MRO
In several experiments intracellular recordings were made in large numbers of
superficial extensor muscle fibres in one segment while RMi was stretched and the
output of the tonic MRO was recorded. It was observed that MRO discharge con-
sistently activated only one size of junctional potential in each fibre. It has been
established, however, that the superficial extensors are supplied by five excitatory
efferent fibres as well as an inhibitor (Kennedy, Evoy & Fields, 1966). By recording
extracellularly from the muscle it was found that receptor discharge evoked a single
large muscle potential. It therefore appears certain that MRO discharge activates only
one of the five ipsilateral slow excitatory motoneurones in its segment.
This observation could be explained in two different ways. The MRO might have
460 HOWARD L. FIELDS
anatomical connexions with only one segmental motoneurone. Alternatively, the MRO
might project to the other motoneurones, but their level of excitability could be lower
than that of the one activated by MRO discharge, i.e. the other motoneurones could
constitute a sort of 'sublimal fringe'. The results of several kinds of experiments
support the first interpretation. (1) It was possible to activate motoneurones by
electrical stimulation of interneurones isolated from connectives of the ventral nerve
Time-
Fig. 4. Differential effect of tonic MRO input on several motoneurones. Impulse frequency
in tonic MRO (upper curve) and three tonic motoneurones (lower curves) plotted as a function
of time for successive 1 sec. intervals. Only one of the motoneurones (continuous line) is
significantly affected by the output of the tonic MRO. Solid bars below MRO plot indicate
periods of stretch applied to RMi, first bar extends for a 5 sec. interval.
cord. This was accomplished by dorsal dissection of the extensor and part of the
flexor musculature posterior to the site of recording, thus exposing the ventral nerve
cord dorsally. Small bundles of fibres were then separated from the cord and electri-
cally stimulated. Stimulation of certain bundles could activate several motoneurones
at the same time; RMi was then intermittently stretched and relaxed. The effect of
MRO input under these conditions was to increase the frequency of impulses in only
one of the active motoneurones. (2) Even in the rare cases when an increase in dis-
charge frequency of two motoneurones was observed to accompany MRO activity,
the effect was considerably more pronounced in one than the other. (3) It was observed
in many preparations that isolation of one of the ganglia in the abdominal cord from
the rest of the CNS, by cutting the connectives anterior and posterior to the ganglion,
resulted in a marked increase of spontaneous efferent activity in the second root,
Proprioceptive control of posture in the crayfish abdomen 461
including the slow extensor motoneurones. Utilizing such isolated preparations, it was
possible, by matching spike amplitudes in the nerve trace with muscle junctional
potentials, to identify unambiguously three spontaneously active units and to correlate
their activity with the discharge frequency of the slow MRO. Fig. 4 graphically
demonstrates that segmental MRO input affects only one of the three motoneurones
and that the central excitability of the motoneurone (as measured by level of spon-
taneous activity) is not the factor that determines which one will be so activated. This
evidence is not quite conclusive since the study utilized an isolated ganglion; extra-
segmental connexions could conceivably mediate MRO effects, even on motoneurones
in its own segment.
There is evidence that the motoneurone activated by the MRO has properties that
distinguish it from the other slow extensor motoneurones. First, it has a wide distribu-
tion to slow extensor muscle fibres. In several preparations, serial penetrations of
numerous muscle fibres in all components of the superficial extensors revealed that
without exception they were innervated by a motoneurone which could be activated
20 mV.
0 5 sec.
Fig. 5. Common innervation of RMi and a slow extensor muscle fibre. Electrical stimuli
delivered to n.r.m. at gradually increasing intensity at i/sec, with the second root cut centrally.
Lower trace, extracellular recording from n.r.m. (spike is that of the tonic MRO); upper trace,
an intracellular record from a muscle fibre in i.e.l. A sudden increase in MRO discharge
frequency occurs at the same threshold as a junctional potential in the muscle fibre, demon-
strating common innervation of that fibre and RMi.
by stretching RMi. In most preparations these fibres showed spontaneous activity,
and by correlating the spontaneous junctional potentials with spikes simultaneously
recorded en passant in the dorsal nerve it was established that this spontaneously
active fibre was identical to that activated by the MRO. In most but not all cases this
fibre also had the lowest threshold among the motor axons to tactile stimulation.
The question of whether this fibre innervates RMi has been examined, and the
results suggest that it does not. In the numerous experiments in which RMi was
stretched to produce motoneurone activity there was no case in which a sudden
increase in receptor output followed the first recorded junctional potential, though
such an increase was generally seen in response to electrical stimulation of moto-
neurones which branch to supply RMi (see Fig. 5). Furthermore, while low-intensity
segmental tactile stimulation was quite effective in activating the motoneurone also
driven by the tonic MRO, such stimulation did not generally cause an increase in
MRO discharge frequency. In two experiments the motoneurones activated by the
MRO was clearly identified in en passant nerve recordings by correlating its spike
with the junctional potentials evoked by MRO discharge. When this motoneurone was
driven by low-level stimulation of n.c.s., there was no increase in the impulse frequency
of the tonic MRO. It thus seems clear that if this motoneurone does supply RMi its
contribution to tension development is minimal.
30 Exp. B10L 44, 3
462 HOWARD L. FIELDS
Other central effects of the tonic MRO
Other segmental influences of slow MRO input were sought but not found. In
several preparations the inhibitor axon was spontaneously active, and could be identi-
fied by correlating hyperpolarizing junctional potentials in the muscle fibres with
spikes of a specific amplitude in the dorsal nerve record. In other cases the inhibitor
was selectively driven by electrical stimulation of ' command' interneurones isolated
in the ipsilateral 5-6 connective of the abdominal nerve cord (cf. Kennedy et al. 1966).
In no case did MRO input have a clear-cut effect on impulse frequency in the inhibi-
tory nerve, although in some preparations a slight, transient decrease in discharge
frequency of the inhibitor accompanied maintained activity in the tonic MRO.
In several experiments activity in the slow flexor motoneurones was recorded while
the RMs were stretched. This was accomplished by dissecting the MROs free of the
extensor musculature and then exposing the flexor muscles by a separate ventral
dissection; alternatively, the MROs were left intact and a contralateral dorsal dissec-
tion was extended through to the superficial flexor muscles. In neither case was any
effect of MRO discharge observed upon flexor motoneurone activity. Apparently
discharge of the tonic receptor has a rather limited segmental effect, namely, the
excitation of one slow extensor motoneurone and self-inhibition via the accessory
nerve reflex (Eckert, 1961a). This conclusion is consistent with Eckert's (1961a)
finding that stretching the RMs activates just two efferent fibres in the dorsal nerve.
The distribution of reflex excitation produced by the tonic receptor was studied by
recording junctional potentials in ipsilateral superficial extensor muscle fibres in
adjacent segments and contralaterally in the same segment. It was found that stretching
RMi evoked ipsilateral motoneurone activity in both the next anterior and next
posterior segments but had a negligible contralateral effect in the same segment. This
is a somewhat unexpected rinding in view of the fact that the contralateral extensors
will be synergistic to ipsilateral extensors in all abdominal movements, whereas the
ipsilateral extensors in adjacent segments may act as antagonists in some movements.
By simultaneous recording of ipsilateral motoneurones in segments 2, 3, and 4 it
was determined that, in response to a given stretch of RMi in segment 3, the increase
in impulse frequency of the activated motoneurone in segment 3 was 10 times greater
than that in either segment 2 or 4. This segmental specificity contrasts sharply to that
displayed by the accessory nerve reflex described by Eckert (1961 a); in this reflex the
accessory nerves of adjacent segments are activated to the same extent as those in the
reference segment.
Contraction of adjacent extensors
In order to interpret segmental interactions a study of the effect of contraction of
the extensors in adjacent segments on MRO discharge was undertaken (cf. Wiersma
et al. 1953). It was found that stimulation of motoneurones to the deep extensors in
adjacent segments caused a phasic output in both phasic and tonic receptors, and that,
generally, contraction of fast extensors in the posterior segment was more effective
than contraction of those in the anterior segment. Repetitive stimulation of slow
extensor motoneurones in both adjacent segments resulted in a gradual increase in
tonic MRO output which attained a final frequency dependent on rate of stimulation.
Proprioceptive control of posture in the crayfish abdomen 463
Correlations of behaviour and MRO activity
MRO discharge was monitored in a completely intact crayfish while abdominal
movements were simultaneously photographed (see Methods). Fig. 6 (Plate 1) shows
that receptor output sometimes varied widely with small changes in abdominal posi-
tion ; conversely, there was often no receptor output even though the abdomen varied
extensively in degree of flexion. Receptor output sometimes actually increased when
the segment shortened; this is opposite to the response expected on anatomical con-
siderations. It was repeatedly observed that if the abdomen was manually flexed from
a set position it returned to that position, often with remarkable precision. The slow
MRO discharge increased when the tail was manually flexed, and was progressively
silenced as the initial position was re-approached. Fig. 6 (Plate 1) shows that active
extension was preceded by a burst in the tonic MRO which became silent as the new
position was approached, as one would predict if the RMs were activated along with the
extensor muscles. Experimental evidence such as that of Fig. 7 (Plate 2) demonstrates
clearly that receptor output is more directly a function of displacement from some set
abdominal position than of absolute degree of flexion of the abdomen. In Fig. 7 (Plate 2)
abdominal position in frame 3 is very nearly the same as that in frame 4 but MRO
activity is much greater at 3 than at 4. In 3 the position was attained by manual
displacement of the abdomen from a centrally set position, whereas in 4 the abdomen
is in a ' desired' position, i.e. there is no artificial displacement. These results seriously
damage the concept of the MRO as a simple length-measuring device and suggest
instead that it may operate as an error detector, signalling deviation of abdominal
position from some 'desired' position.
DISCUSSION
The analysis of the innervation pattern and reflex effects of the tonic MRO as
described above indicates that the following sequence of events takes place in naturally
occurring extension of the tail. When the segmental slow extensor motoneurone(s)
which supply RMi are activated, the muscle of the tonic MRO contracts and the
receptor discharge increases; this in turn feeds back as excitation to the most widely
distributed of the slow motoneurones. As the extensor muscles shorten, tension in
RMi decreases, resulting in a decreased frequency of firing in the sensory neurone.
The validity of this postulated sequence is supported by results showing that tactile
stimulation may cause a transient rise in the frequency of receptor discharge which
in turn evokes motoneurone discharge (Fields & Kennedy, 1965). Since the impulse
frequency of the MRO is a linear function of tension, which is in turn directly related
to the initial length of RMi (Krnjevic' & Van Gelder, 1961), the magnitude of the
sensory discharge fed back in response to motoneurone activity will depend on the
initial length of RMi.
Merton (1950, 1953) was the first to describe the role of the muscle spindle in terms
of servo theory. Although it may be questioned whether this approach adds anything
that could not be intuitively understood (see Granit, 1962), it provides a simple
descriptive framework for discussion and may lead to insights that are not intuitively
obvious. The experiments described above strongly indicate that the slow stretch
receptor functions as part of a follow-up length servo system similar to that described
30-2
464 HOWARD L. FIELDS
by Merton. The simplified block diagram of Fig. 8 illustrates the relationships of the
major components of the system. It is similar to a schematic of the mammalian spindle
system devised by Partridge & Glaser (i960). Presynaptic drive to the slow extensor
motoneurone(s) that supply RMi determines the set point. The output, tail position
(in this case, lengthening of the reference segment), represents a balance between the
various inputs including segmental motoneurone activity (negative, i.e. shorten the
reference segment) and the opposing forces of flexor contraction, gravity and contrac-
tion of extensors in adjacent segments (positive, i.e. lengthen the reference segment).
The stretch receptor acts as an error detector which responds to differences between
Gravity,
flexors,
adjacent
X extensors
JLJL
-*j NI Motoneuron \-
Motor Extensor + 3
Impulses/sec Position of
centre muscle
|N| MotoneurorT}- segment
(length)
Impulses/sec.
Accessory
nerve Impulses/sec
D
Impulses/sec
E Receptor \M\
soma and Receptor Receptor tk-
dendrltes dendrltes muscle
Fig. 8. Block diagram of the servo control system for regulation of tonic contraction. Large rec-
tangles represent structures named within; small squares represent transducing functions;
N, neuro-neural synapse; M, neuromuscular junction; T, converts tension to length change
(i.e. series and parallel visco-elastic properties of the slow extensor muscles); L, converts length
change to tension (visco-elastic properties of RMi); R, converts dendritic deformation to
membrane depolarization (receptor potentials). Open circles represent summing points and
closed circles represent pick-off points for feedback loops, (i) Reference input, related to
'desired' position (i.e. set point); (2) actuating signal (excitatory input to motoneurone sup-
plying .RMi); (3) controlled variable (net tension in extensors); (4) by altering the mechanical
properties oiRMi, i.e. its length-tension curve, activity in the motor nerve to RMi determines
the discharge rate of the MRO at any given length. RMi length equals segment length. If
segment length is greater than 'desired', RMi tension produces a generator potential (5)
which exceeds threshold for MRO discharge, the error signal (6); (7) inhibitory junctional
potential set up by accessory nerve activity.
the set point (at which its output is zero) and the actual tail position; the magnitude of
this error is, of course, given by the impulse frequency of the MRO. MRO discharge
activates one of the extensor motoneurones, resulting in shortening of the segment and
reduction of the error. By altering excitatory input to the motoneurone supplying
RMi the set point can be varied, allowing the servo loop to operate over a wide range
of abdominal positions. Such a system enables the crayfish to adjust the force of slow
extensor contraction to any level that might be required to compensate for changes
in load or, as pointed out by Barlow (1961), muscle power (i.e. resulting from fatigue
or contraction of synergists). Such a system also seems to be operating in certain