Proprioceptors monitoring forces in a locust hind leg during kicking form negative feedback loops with flexor tibiae motor neurons
Ken Sasaki* and
Malcolm Burrows
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
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Fig. 1. Sensory signals from the lump receptor and distortion of the
femoro—tibial joint during a kick. Electrical activity of the lateral
nerve containing the axons of sensory neurons from the lump receptor, and of
the extensor tibiae muscle was recorded at the same time as images of the
movements of the femoro—tibial joint. The distortion of the lateral
semi-lunar process was plotted from these images, three of which are shown at
the times indicated. Full extension of the tibia in the kick occurred at time
0 ms. The arrows show the changing position of the distal tip of the
semi-lunar process. The distortion of the dorsal femur and the bending of the
semi-lunar process are also shown in tracings from frames at -15, -4 and 0 ms.
The movements of the semi-lunar process in the graph appear jerky because of
the intermittent sampling. Initial flexion of the tibia was accompanied by
spikes in the lateral nerve. During the co-contraction phase (horizontal grey
bar), the sensory spikes of the lump receptor occurred at high frequency as
the semi-lunar process was bent progressively. The extended position of the
tibia following the kick was signalled by sensory spikes in joint receptors.
The vertical dashed lines indicate the different phases of the kick. The large
spikes in the muscle recording are from the fast extensor tibiae motor neuron
(FETi) and the smaller ones from flexor motor neurons.
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Fig. 4. Activity of the lump receptor during electrical stimulation of the extensor
tibiae muscle with a single pulse. The spike of the fast extensor tibiae motor
neuron (FETi) is visible as cross-talk in the recording from the lateral
nerve; its waveform changes when the muscle contracts and moves. (A) The tibia
was held in the fully flexed position and the resulting distortions of the
femoro—tibial joint, measured from high speed images, were followed
40-50 ms after the stimulus by a burst of sensory spikes. (B) When the tibia
was held in a partially extended position, the stimulus evoked a distortion of
the semi-lunar process but no sensory spikes. (C) The tibia was free to move
during the stimulus and there was no distortion and no sensory spikes.
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Fig. 5. Effect of manipulating the actions of the extensor and flexor muscles on
the signalling by the lump receptor. (A,B) The extensor tendon was cut in the
distal femur so that stimulation of the extensor muscle exerted no direct
force on the joint. Instead the stimulus activated flexor tibiae motor neurons
through the central, monosynaptic connections that the fast extensor tibiae
motor neuron (FETi) makes with them, and caused a contraction of the flexor
muscle. (A) With the tibia held in the fully flexed position and the flexor
tendon free to move, a burst of spikes from the lump receptor followed the
stimulus. (B) The tibia in the same locust was held in a partially extended
position, and the stimulus now did not lead to sensory spikes. (C,D) A second
locust in which the extensor tendon was intact. (C) The flexor tendon exerted
force on the joint fixed in the fully flexed position. The stimulus was
accompanied by a burst of sensory spikes. (D) The flexor tendon was clamped so
that force could not be transmitted through it to the joint. No sensory spikes
followed the stimulus. The inset diagrams show the experimental arrangement.
The solid arrows show the flow of effects from the evoked FETi spike; the open
arrows, the movement of the flexor tendon. The recording during the stimulus
has been truncated.
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Fig. 6. Activity of sensory neurons from the lump receptor recorded in the lateral
nerve in response to forces applied to the tendon of the flexor muscle. (A)
With the tibia fully flexed, pulling on the flexor tendon evoked a burst of
sensory spikes. (B) With the tibia extended by 20°, no spikes followed the
applied pull.
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Fig. 7. Different effects of contractions by proximal and distal bundles of the
flexor muscle on signalling by the lump receptor. (A) A single stimulus to the
extensor muscle in an intact leg with the tibia fully flexed was followed by a
burst of spikes from the lump receptor. (B) The same locust but with the
flexor nerve (N5B2) cut in the middle of the femur, thereby preventing the
distal muscle bundles from contracting. The contraction of proximal muscle
bundles caused a burst of sensory spikes. (C,D) A second locust. (C) In the
intact leg, sensory spikes followed the stimulus with the tibia fully flexed.
(D) The flexor tendon was cut between the proximal and distal bundles of
fibres so that the force developed by proximal fibres was not transmitted to
the joint. Contraction of the distal muscle bundles was not followed by spikes
from the lump receptor.
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Fig. 2. Sensory signals and distortion of a semi-lunar process at the
femoro—tibial joint in kicks with only short periods of co-contraction.
(A) An initial spike in the fast extensor tibiae motor neuron (FETi)
accompanied the movement of the tibia into a flexed position and was signalled
by a burst of spikes in sensory neurons from the lump receptor. The tibia then
remained flexed for 500 ms before a kick was generated by an 80 ms long
co-contraction involving 3 FETi spikes. Only a small distortion of the
semi-lunar process resulted and spikes from the lump receptor occurred at low
frequency. (B) A kick following a 150 ms long co-contraction with 5 FETi
spikes. The tibia was fully flexed about the femur before the displayed
recording. The bending of the semi-lunar process was now twice as large and
was accompanied by more sensory spikes during the co-contraction phase.
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Fig. 3. Positive relationship between the frequency of spikes in the lateral nerve
and the extent of distortion of a semi-lunar process during the co-contraction
phase of kicking. (A) Plots of the correlation for 4 individual kicks. In
kicks 1 and 2, the spike frequencies appear to decrease at the end of the
co-contraction period due to the apparent synchronization of the sensory
spikes in the extracellular recording at high frequencies. (B) Pooled data
from 10 kicks by 3 locusts showing a positive relationship between the
frequency of sensory spikes in the lateral nerve during co-contraction and the
distortion of a semi-lunar process.
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Fig. 8. Effects of the force produced by the action of individual flexor motor
neurons on the activity of sensory neurons from the lump receptor. A pulse of
depolarising current was injected into the cell body of a motor neuron to
evoke spikes. (A) Spikes in a slow flexor motor neuron innervating the
proximal muscle bundles did not elicit spikes in the lump receptor. (B)
Similarly a high frequency of spikes in another slow motor neuron innervating
distal muscle bundles did not evoke sensory spikes. A later burst of spikes in
fast flexor motor neurons, not directly related to the applied depolarisation,
caused muscle activity and sensory spikes. The bridge is unbalanced in the
intracellular recordings.
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Fig. 9. Effects on flexor tibiae motor neurons when the lump receptor was
stimulated by pulling on the flexor tendon. (A) A fast motor neuron was
hyperpolarised when spikes from the lump receptor occurred. (B) A second fast
flexor was not affected by the stimulation. (C) A tonic sequence of spikes in
a slow flexor evoked by the intracellular injection of depolarising current
was not altered by spikes from the lump receptor. Grey lines indicate the
membrane potential of a motor neuron before stimulation of the lump
receptor.
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Fig. 10. Effects of spikes from the lump receptor on the synaptic connection between
the fast extensor tibiae motor neuron (FETi) and flexor motor neurons. (A) The
experimental protocol. Antidromic spikes were evoked in FETi by stimulation of
the extensor muscle. 5 stimuli at intervals of 1 s were given before the
flexor tendon was pulled. 4 s after the last stimulus the tendon was pulled
and 5 more stimuli were delivered. The motor neuron was hyperpolarized by the
sensory spikes and the EPSPs were reduced in amplitude. Repetition of the
electrical stimuli after the movement of the tendon showed that the EPSPs
recovered to their previous amplitude. (B) Comparison of the second EPSP
before the sensory stimulus with the second EPSP during the sensory spikes
(grey trace) shows the changes in amplitude.
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© The Company of Biologists Ltd 2003
