Proprioceptors monitoring forces in a locust hind leg during kicking form negative feedback loops with flexor tibiae motor neurons
Department of Zoology, University of Cambridge, Downing Street,
Cambridge CB2 3EJ, UK
* Present address: Insect Neurobiology Laboratory, Physiology and Genetic
Regulation Department, National Institute of Agrobiological Sciences, Tsukuba,
Ibaraki 305-8634, Japan
Author for correspondence (e-mail:
mb135{at}hermes.cam.ac.uk)
Accepted 29 November 2002
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Summary |
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The two sensory neurons comprising the lump receptor lie in a groove in the ventral part of the distal femur. The sensory neurons spike if force is applied to the flexor tendon when the joint is fully flexed, but not when it is extended. They also spike as the tendon of the flexor muscle slides into the ventral femoral groove when the tibia is fully flexed during the co-contraction phase of kicking. Their spike frequency correlates with the extent of bending of a semi-lunar process that provides a quantifiable measure of the joint distortions. If the tibia is not fully flexed, however, then muscle contractions still cause distortions of the joint but these are not signalled by sensory spikes from the lump receptor. The lump receptor, therefore, does not respond primarily to the joint distortions but to the movements or force in the flexor tendon.
Contractions of the flexor tibiae muscle caused by spikes in individual flexor motor neurons can evoke spikes in sensory neurons from the lump receptor when the joint is fully flexed. In turn, the sensory neurons cause a hyperpolarisation in particular flexor motor neurons in a polysynaptic negative feedback loop. The lump receptor could, therefore, regulate the output of the flexor motor neurons and, thus, limit the amount of force generated during co-contraction. It may also contribute to the inhibition of the flexors at the end of co-contraction that allows rapid kicking movements to occur.
Key words: joint, joint receptor, motor neuron, sensory feedback, locust, Schistocerca gregaria
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Introduction |
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The hind legs of a locust have proved to be a useful model in which to
examine the interplay between the motor commands, the mechanics of the joints
and muscles, and sensory feedback (Burrows,
1996). These legs are used in walking but are specialised for
powerful jumping and kicking movements. The motor pattern for these movements
consists of three phases (Burrows,
1995
; Godden,
1975
; Heitler and Burrows,
1977a
): first, an initial cocking phase, in which the tibia is
fully flexed about the femur; second, co-contraction of flexor and extensor
tibiae muscles; third, a triggering phase, in which inhibition of the flexor
motor neurons enables a rapid and powerful tibial extension to occur. The
force required for these movements is generated by almost isometric
co-contractions of the large extensor and the smaller flexor tibiae muscles
once a tibia is locked in a fully flexed position. The muscular force
generated during co-contraction bends the tips of the semi-lunar processes at
the femorotibial joints and distorts the distal femur
(Burrows and Morris, 2001
),
storing approximately half of the energy required for rapid extension of the
tibiae (Bennet-Clark,
1975
).
Many proprioceptive sense organs provide feedback to control and modify the
output of the motor neurons used in this motor pattern. Campaniform sensilla
signal the forces in the cuticle and a single-celled tension receptor monitors
the force in a distal bundle of the flexor tibiae muscle
(Matheson and Field, 1995).
The movements and positions of the femorotibial joint are signalled by
a chordotonal organ containing some 90 sensory neurons
(Field and Burrows, 1982
;
Matheson and Field, 1990
;
Usherwood et al., 1968
), a
single strand receptor neuron (Braunig,
1985
) and five joint receptor neurons
(Coillot and Boistel, 1969
;
Heitler and Burrows, 1977b
).
We have sought to determine whether particular proprioceptors at this joint
monitor the distortions of the distal femur and bending of the semi-lunar
processes that occur during jumping and kicking but not during walking,
climbing and other locomotory movements. At all stages in the moulting cycle,
the co-contraction phase of the motor pattern can cause irreparable damage
(Norman, 1995
), but limiting
the production of excessive muscular force might be especially important for
recently moulted animals in which the cuticle will not have fully hardened.
The frequency with which kicks can be elicited falls before and after a moult
and newly moulted animals are unable to generate the characteristic motor
pattern (Norman, 1996
,
1997
).
We have focussed on two of the joint receptor neurons called collectively
`the lump receptor'; the three remaining joint receptors respond to extension
of the femorotibial joint beyond 80°
(Coillot, 1974). These two lump
receptor neurons lie in a groove between the posterior wall of the femur and
the ventral invagination, or lump in the ventral femur
(Heitler and Burrows, 1977b
).
The posterior arm of the tendon of the flexor tibiae muscle slides into this
groove when the tibia is fully flexed before a kick or a jump and rests
directly on the receptors. The two sensory neurons respond to movement or
force applied to the flexor tendon only when the femorotibial joint is
in the fully flexed position (Heitler and
Burrows, 1977b
). Although cutting the nerve containing the axons
of these receptors does not influence the co-contraction of flexor and
extensor muscles, it does reduce the occurrence of kicking or jumping
(Heitler and Burrows, 1977b
;
Jellema and Heitler, 1997
;
Jellema et al., 1997
).
To determine the possible functional roles of the lump receptor in
monitoring events during kicking, we recorded its activity and the distortion
of the semi-lunar processes. We analysed whether individual flexor motor
neurons could differentially activate the lump receptor through their
particular innervation patterns of the flexor muscle and the different forces
they generate at the flexor tendon. Finally, we determined whether sensory
neurons of the lump receptor make feedback loops with flexor motor neurons,
building on the single example of such an effect reported by Heitler and
Burrows
(1977a,b
).
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Materials and methods |
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Images of the femorotibial joint during a kick, or during direct electrical stimulation of the extensor tibiae muscle were captured with a high speed camera (Redlake Imaging, San Diego, California, USA) and associated computer at 1000 frames s-1 and with an exposure time of 0.5 ms. Selected images were stored as computer files for later analysis with Motionscope software (Redlake Imaging). Images shown in the figures were timed from the point (0 ms) when the tibia reached full extension. Movements of the distal tip of a semi-lunar process at the femorotibial joint were measured from these images relative to a fixed point on the ventral femur. Video images on one computer were synchronized with the electrical recordings on a second computer, by generating 1 ms pulses from a hand-held switch when a kick was observed. These pulses were recorded as electrical events with the electrophysiological data and as light signals on the images.
Intracellular recordings were made in the metathoracic ganglion from the
cell bodies of motor neurons innervating the flexor tibiae muscle of the left
hind leg. The ganglion was exposed by removing the ventral cuticle of the
thorax and then stabilized on a wax-coated silver platform. The thorax was
perfused continuously with saline
(Usherwood and Grundfest,
1965) at 20-22°C. The sheath of the metathoracic ganglion was
treated with protease (Sigma type XIV) for 30 s to facilitate the penetration
of glass microelectrodes filled with 2 mol l-1 potassium acetate
and with resistances of 40-80 M
. The flexor motor neurons were
identified by the following criteria. First, the presence of a monosynaptic
excitatory postsynaptic potential (EPSP) caused by an antidromic spike in the
fast extensor tibiae (FETi) motor neuron
(Burrows et al., 1989
). Second,
spikes evoked in the impaled flexor motor neuron by pulses of depolarizing
current caused spikes that evoked flexion movements of the tibiae and could be
matched with muscle potentials recorded extracellularly from flexor tibiae
muscle bundles. Within the pool of flexor tibiae motor neurons, individuals
could be classified as slow or fast-like, according to their threshold for
spike initiation when depolarizing current was injected, by the frequency of
evoked spikes and by the tibial movement they evoked.
To exert force on the tendon of the flexor tibiae muscle, it was exposed in
some experiments by removing the ventral cuticle of femur in the left hind
leg. After removal of the first and second proximal bundles of muscle fibres
(Sasaki and Burrows, 1998),
the tendon was grasped with fine forceps attached to a vibrator (Ling Dynamic,
type 101). The tendon could then be moved linearly to mimic flexion movements
of the femorotibial joint. The two main leg nerves, N5B1 and N5B2, were
cut in the middle of the femur to remove inputs from mechanosensory neurons
distal to the cut, except those innervated by the lateral nerve. The tendon of
the extensor tibiae muscle was also cut at the same level so that extensor
contractions could not cause sensory feedback.
The results are based on recordings from 52 locusts. 15 kicks by four locusts and 24 electrical stimulations of the extensor tibiae muscle in seven locusts were recorded with high-speed images. Intracellular recordings were made from 32 flexor motor neurons with simultaneous extracellular recordings from the lateral nerve in 20 locusts.
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Results |
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Interpretation of the sensory spikes
We believe the spikes in the lateral nerve that occurred during initial
flexion and during the co-contraction phases of a kick were from the lump
receptor. Spikes of similar amplitudes were activated in separate experiments
(see Figs
4,5,6,7)
by evoked contractions of the extensor and flexor muscles and occurred only
when the tibia was fully flexed. They were also evoked by applying force to
the flexor tendon when the tibia was fully flexed. In both of these phases of
the kick motor pattern, two spike amplitudes could sometimes be recognised and
occasionally larger amplitude spikes resulted from the apparent coincidence
between these spikes. They could, therefore, correspond to the two sensory
neurons of the lump receptor. By contrast, the spikes that occurred when the
kick was completed could be evoked by forcibly extending the tibia beyond
80°, indicating that they had the same response properties as those of the
joint receptors (Coillot, 1974;
Coillot and Boistel, 1969
).
The sensory neurons from hairs on the femur innervated by the lateral nerve
did not appear to be activated during kicking.
|
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Correlation of lump receptor spikes with kicking movements
All kicks showed the same basic sequence of motor and sensory activity,
though the detail varied between kicks of different strength and velocity of
tibial movements (Figs 2,
3). In some kicks, the tibia
was fully flexed about the femur for some time before the co-contraction phase
was initiated. The initial flexion of the tibia was signalled by a burst of
sensory spikes (Fig. 2A), but
while the tibia was in the fully flexed position few spikes occurred in the
lateral nerve (Fig. 2A,B).
Kicks with a brief co-contraction phase that contained few FETi spikes led to
the semi-lunar processes being bent by only a small amount
(Fig. 2A). This was signalled
by a low frequency of sensory spikes. If the co-contraction phase was longer
and contained more FETi spikes then the bending of the semi-lunar processes
was greater (Fig. 2B) and the
frequency of spikes recorded in the lateral nerve was higher
(Fig. 3A). In each kick, the
frequency of spikes rose steadily during the co-contraction phase as the
semi-lunar processes were progressively bent. The overall frequency of these
sensory spikes reached 500 Hz in some kicks with a contribution from at least
two neurons. Just before some kicks occurred, the frequency of the summed
sensory spikes appeared to fall (Fig.
3A), because of the coincidence of spikes in the summed
extracellular recording that was also reflected in their changing amplitude.
When data for 10 kicks were pooled, there was a positive correlation between
the number (=0.647, P<0.03, Spearman rank correlation test)
and frequency (
=0.652, P<0.05,
Fig. 3B) of spikes in the
lateral nerve and the amount of bending in the semi-lunar processes. This
suggests that during a kick the lump receptor monitors the bending of the
semi-lunar processes, or some other correlated event(s) at the
femorotibial joint.
|
|
Lump receptor responses to experimentally generated forces at the
femorotibial joint
To determine what events at the femorotibial joint led to spikes in
the lump receptor, we manipulated the different active forces and examined the
effects of joint angle on these forces. Contractions were evoked in the
femoral muscles. A single electrical stimulus to the extensor tibiae muscle
activates the terminals of its two motor neurons (a slow, SETi and a fast,
FETi) leading to an orthodromic spike in each that leads to a twitch
contraction of the muscle fibres. The electrical stimulus also evokes
antidromic spikes that are carried toward the metathoracic ganglion. The
antidromic spike in FETi activates a monosynaptic pathway to the flexor motor
neurons that can evoke flexor spikes and a contraction of the flexor muscle
(Burrows et al., 1989;
Hoyle and Burrows, 1973
).
The co-contraction phase was simulated in 7 locusts by electrically stimulating the extensor tibiae muscle with the tibia held fully flexed against the femur and unable to extend (Fig. 4A). Each stimulus and the resulting spike in FETi was followed by a transient bending of the semi-lunar processes, distortion of the dorsal, distal cuticle of the femur and, some 40-50 ms later, by a burst of spikes in the lump receptor. The peak frequency of the spikes was about 200 Hz. The spikes continued throughout the 80 ms period that the semi-lunar processes were maximally bent, and stopped when the bending relaxed. If, however, the same stimulus was applied to the extensor muscle when the tibia was clamped at an angle greater than 20° and thus unable to extend further, the semi-lunar processes were still bent but no sensory spikes occurred in the lateral nerve (Fig. 4B). Finally, if the same stimulus was given to the extensor muscle when the tibia was allowed to extend freely, then the semi-lunar processes did not bend and no sensory spikes occurred (Fig. 4C). These experiments indicate that bending of the semi-lunar processes or cuticular distortions at the femorotibial joint are not directly responsible for evoking the sensory spikes.
We, therefore, tested whether forces generated in the tendons of either the flexor or extensor tibiae muscles were responsible (Fig. 5). First, in three locusts, the extensor tendon was cut in the distal tibia and a single electrical stimulus was delivered to the muscle as above. When the tibia was held fully flexed about the femur, an FETi spike was followed by a burst of spikes from the lump receptor similar to those seen in an intact leg (Fig. 5A). Force generated by contraction of the extensor muscle could not be transmitted to the femorotibial joint but the flexor muscle was activated through the central pathway. Repeating the same stimulus with the tibia extended by more than 20° and free to move did not evoke any sensory spikes (Fig. 5B). In a further three locusts, the flexor tendon was exposed in the distal femur so that it could be clamped reversibly, but the extensor tendon was intact. When the tibia was held fully flexed about the femur and the flexor tendon was unclamped, the usual burst of spikes from the lump receptor followed stimulation of the extensor muscle (Fig. 5C). When the flexor tendon was clamped so that force or movement generated in the flexor muscle could not be transmitted to the joint, no sensory spikes were evoked (Fig. 5D). These experiments indicate that the lump receptor responds to force or movements of the flexor tendon but not to the force generated by the extensor muscle.
This conclusion was tested further in five locusts by pulling on the flexor
tendon to apply different forces in the direction that would cause the tibia
to flex (Fig. 6). With the
tibia in the fully flexed position, pulling on the tendon evoked a burst of
spikes in the sensory neurons from the lump receptor
(Fig. 6A). If the tibia was
fixed at an angle of 20° or more, however, the same amount of applied
force did not evoke any sensory spikes
(Fig. 6B). This observation
therefore confirms the result of Heitler and Burrows
(1977b).
Effect of flexor tibiae contraction on lump receptor activity
The muscle fibres that form the main body of the flexor muscle are grouped
into 10-11 pairs of bundles that insert onto a common central tendon
(Sasaki and Burrows, 1998).
These muscle bundles are innervated by different sets of motor neurons, the
axons of which run in small side branches of N5B2. Cutting particular nerve
branches can, therefore, selectively abolish the contraction of certain
bundles and could be used to test whether all parts of the muscle contributed
to the excitation of the lump receptor. A nerve branch was cut in the middle
of the femur of three locusts, dividing the muscle into an innervated proximal
part and a denervated distal part (Fig.
7A,B). Before the nerve was cut, an electrical stimulus to the
extensor tibiae muscle with the tibia fixed in the fully flexed position,
evoked a burst of spikes in the sensory neurons from the lump receptor
(Fig. 7A). Following the cut,
when only the proximal part of the muscle could contract, the same stimulus
evoked a burst of spikes of lower frequency
(Fig. 7B).
To test whether selective contraction of distal flexor muscle bundles was equally effective, the flexor tendon was cut between the 4th and 5th pairs of muscle bundles with N5B2 intact (Fig. 7C,D). In the control experiment before the cut was made, stimulation of the extensor muscle evoked a burst of spikes in the lump receptor (Fig. 7C). After the cut, however, the force generated by the distal muscle bundles alone did not evoke spikes in the lump receptor (Fig. 7D).
Individual motor neurons were then activated by intracellular injection of current into their somata to test whether the contraction they evoked activated the lump receptor. Intracellular stimulation of a slow flexor motor neuron evoked spikes that were also recorded in proximal muscle bundles, but did not activate the lump receptor (Fig. 8A). A high frequency of spikes in a slow flexor motor neuron innervating the distal muscle bundles also did not evoke sensory spikes in the lump receptor (Fig. 8B). By contrast, when several fast-like flexor motor neurons innervating the proximal muscle fibres spiked spontaneously after the applied depolarisation, the contractions they evoked activated spikes in sensory neurons from the lump receptor (Fig. 8B).
|
Effect of lump receptor on flexor tibiae motor neurons
To determine whether sensory feedback from the lump receptor could regulate
the action of flexor motor neurons, intracellular recordings were made from
members of the pool of nine flexor motor neurons while the lump receptor
spikes were evoked by pulling on the flexor tendon
(Fig. 9). Three of seven
fast-like flexor motor neurons were hyperpolarized when the lump receptor
spiked (Fig. 9A). By contrast,
the remaining four fast-like motor neurons showed little or no change in
membrane potential during sustained spiking by the lump receptor
(Fig. 9B). Similarly, in four
slow motor neurons, no change in their synaptic inputs, or in the frequency of
a tonic sequence of their spikes (Fig.
9C), could be detected during spikes of the lump receptor evoked
by force applied to the flexor tendon.
|
The spikes from the lump receptor, that resulted in a hyperpolarization in three of seven fast flexors, also altered the synaptic inputs in these motor neurons generated by spikes in FETi (Fig. 10A,B). In each of the three flexor motor neurons, the excitatory synaptic potentials (EPSPs) evoked by FETi spikes were reduced in amplitude when the flexor tendon was pulled and spikes occurred in the lump receptor. The reduction was seen in individual EPSPs compared with the same position in the sequence (Fig. 10B) or in averages of the responses from before, during and after the applied stimulus. The lump receptor could, therefore, reduce the probability of spikes being generated in flexor motor neurons and, thus, act in a negative feedback loop to reduce flexor tension during the co-contraction phase of a kick.
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Discussion |
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Signalling by the lump receptor
The sensory neurons of the lump receptor of a hind leg are only excited
when the femorotibial joint is fully flexed. When the joint is in this
position, movements of the flexor tendon or force exerted on it by
contractions of the flexor muscle, or co-contractions with the extensor muscle
excite the lump receptor. When the tibia is not fully flexed, co-contractions
of the extensor and flexor muscles distort the femoral cuticle of the joint
but do not excite the lump receptor. Similarly, contractions of the extensor
alone do not excite the lump receptor although they can cause cuticular
distortions. The most likely stimulus is the movement of the flexor tendon
past the receptor, or its downward pressure on it when the tibia is moving
toward or is in the fully flexed position. It is only at full flexion of the
tibia that the flexor tendon engages fully with the cuticular lump in which
the receptor lies (Heitler and Burrows,
1977b). The lump receptor, therefore, signals the extent of a
co-contraction in a kick by directly monitoring the flexor tendon and only
indirectly the distortions of the femorotibial joint caused by the
muscle contractions. The restriction of the lump receptor to signalling at
full tibial flexion suggests that it functions only during jumping and
kicking. The energy required for these movements cannot be generated unless
the tibia is fully flexed and the flexor tendon is locked over the cuticular
lump (Heitler, 1977
). By
contrast, the normal walking movements do not involve full flexion of a hind
leg and signalling by the lump receptor would not be expected.
Multipolar receptors also occur at the femorotibial joint of the
middle legs of a locust (Mucke,
1991; Williamson and Burns,
1978
) even though these legs do not have the same structural
specialisations for jumping and kicking as do the hind legs. Most notably they
lack a femoral lump, so the lines of action of the muscle tendons are
different (Heitler, 1974
).
Three of these receptors, as in the hind leg, respond to extension of the
tibia beyond 80° but the action of the other two neurons, which attach to
the ventral arthrodial membrane of the femur, has not been reported
(Williamson and Burns, 1978
).
Our preliminary observations indicate that these two receptors respond to
direct pressure on the flexor tendon or to movements of the arthrodial
membrane when the flexor tendon of a middle leg moves between angles of
20-30°. In these legs, therefore, these ventral receptors may signal force
or movements of the flexor tendon during normal walking, when clinging to a
twig or hanging on a grass stem. The specialisations of the hind legs for
kicking and jumping would then be seen to have been accompanied by a changed
and more restricted role for their equivalent receptors in monitoring events
during co-contractions leading to kicking and jumping.
Negative sensory feedback loops with a pool of flexor motor
neurons
The flexor tibiae muscle consists of 10-11 pairs of muscle bundles that
insert onto a common central tendon. Different muscle bundles are innervated
by different numbers of excitatory motor neurons
(Sasaki and Burrows, 1998)
from the pool of approximately nine flexor motor neurons
(Phillips, 1980
). The proximal
muscle bundles are innervated by seven motor neurons, including two fast and
three intermediate motor neurons. The muscular force generated by spikes in
one of these fast motor neurons can excite the lump receptor. The contractions
of these muscle bundles are then regulated by a negative feedback loop acting
through a polysynaptic pathway to inhibit particular fast flexor motor
neurons. In this way, the activity of certain flexor motor neurons innervating
particular parts of the muscle can excite the lump receptor while
simultaneously being regulated by sensory feedback from it. The feedback loops
formed by the lump receptor act in parallel to those from other receptors,
such as the femoral chordotonal organ at the femorotibial joint
(Field and Burrows, 1982
;
Matheson and Field, 1990
;
Usherwood et al., 1968
), or
the tension receptor in the most distal bundle of the flexor tibiae muscle
(Matheson and Field,
1995
).
Explanations for the large number of neurons in a particular motor pool are
thought to lie in a subdivision of function among the members, a subdivision
of action by different parts of the muscle by virtue of different innervation
patterns, intrinsic differences in the properties of the muscle fibres, or a
combination of these factors (Skorupski et
al., 1992). Subdivision of connections and hence possible actions
are seen within the flexor tibiae motor pool. For example, campaniform
sensilla on the tibia of a middle leg directly excite a fast but not a slow
flexor motor neuron (Newland and Emptage,
1996
). Similarly, fast flexor motor neurons are excited only by
fast imposed movements of the apodeme of the femoral chordotonal organ in a
hind leg, whereas the opposite is true for a slow motor neuron
(Burrows, 1987
;
Field and Burrows, 1982
).
Although the different flexor motor neurons receive many synaptic inputs in
common, each has specific dynamic responses to movements of the
femorotibial joint (Newland and
Kondoh, 1997
). The specific feedback loops made by the lump
receptor suggest further subdivision of function among members of the flexor
motor neuron pool. Fast-like flexor motor neurons innervating proximal muscle
fibres excite the lump receptor and are themselves inhibited by the sensory
signals from it. Slow flexor motor neurons are less likely to excite the lump
receptor and are apparently unaffected by feedback from it.
How might sensory signals from the lump receptor contribute to
kicking?
Cutting the lateral nerve containing the axons of the joint receptors
reduces the probability of evoking a kick by some 30%, but removing the
femoral chordotonal organ causes a 70% reduction
(Jellema et al., 1997).
Section of the lateral nerve, however, has no effect on the duration of the
co-contraction phase or the number of spikes produced by FETi during the
co-contraction (Jellema and Heitler,
1997
) but does result in more spikes in FETi after the kick and a
prolongation of the time before the tibia is flexed once again. The latter
effects have, however, been attributed to the three extension sensitive joint
receptors and not to the lump receptor
(Jellema and Heitler, 1997
).
Could the high frequency of spikes in the sensory neurons from the lump
receptor towards the end of the co-contraction contribute to ending this phase
of the motor pattern and allow a kick to occur? At the end of the
co-contraction, excitatory flexor motor neurons are rapidly hyperpolarized and
stop spiking and at the same time, the two inhibitory motor neurons that
innervate the flexor muscle are excited
(Burrows, 1995
;
Heitler and Burrows, 1977a
).
This allows the force developed by the extensor muscle during the
co-contraction to be delivered rapidly and propel the extension of the tibia.
The timing of the sensory signals from the lump receptor suggests that they
could progressively reduce the effectiveness of excitation to the flexors
during co-contraction and to the final inhibition. The distribution of the
polysynaptic inhibitory pathway to particular fast-like flexor motor neurons
suggests that other parallel pathways also operate. It will, therefore, be
important to determine whether the lump receptor makes connections with the
many interneurons that are involved in control of leg movements. The negative
feedback loops could limit the force that is generated in a kick to that which
the cuticle can sustain, and thus avoid damage to the joint, particularly in
recently moulted locusts in which hardening is not yet complete.
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Acknowledgments |
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