Control of Cricket Stridulation by a Command Neuron:
Efficacy Depends on the Behavioral State
BERTHOLD HEDWIG
Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, United Kingdom
INTRODUCTION
The coordinated release and control of episodic or rhythmic
motor patterns by central commands or sensory information
involves neuronal processes of general importance for a neurobiological analysis of behavior. Neuronal design principles
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underlying the release and coordination of different motor
activities are being increasingly understood (Dickinson 1995;
Edwards et al. 1999; Getting 1989; Kristan and Shaw 1997;
Morton and Chiel 1994; Pearson 1993; Stein 1978). The central release and activation of rhythmic and/or stereotyped motor activity seems to be controlled mainly by labeled lines;
command neurons that activate dedicated networks, or pattern
generators for specific motor programs (Edwards et al. 1999;
Kupferman and Weiss 1978; Larimer 1988; Wiersma and
Ikeda 1964). More plastic motor activity generated by distributed networks seems to be activated by populations of command-like interneurons (Kien 1983; Larimer 1988). Understanding the design principles for the control of motor patterns
leads to the question of how the control mechanisms interact
when incompatible motor patterns are evoked simultaneously.
Experimental paradigms have been used in which different
motor patterns are generated under changing experimental
conditions. These demonstrate that distributed circuits may be
reconfigured to produce a new output, whereas dedicated networks for particular motor patterns may interact by various
degrees of inhibition (Dickinson 1995; Kristan and Shaw 1997;
Morton and Chiel 1994).
The stridulatory behavior of crickets offers a favorable opportunity to study the intersegmental control of rhythmic motor
patterns. Three motor programs drive the wing movements that
produce the acoustic signals calling, rivalry, and courtship
songs. The motor programs are generated within the thoracic
ganglia and are only released under appropriate behavioral
situations (Huber et al. 1989). Evidence from extracellular
electrical stimulation of the brain or descending axons (Bentley
1977; Huber 1960, 1964; Otto 1971) indicates that the brain
controls the occurrence of the stridulatory motor patterns via
descending interneurons. Huber (1960, 1964) assumed that the
brain drives the thoracic stridulatory chirp pattern by descending rhythmic activity, but the stimulation experiments of Otto
and Bentley indicated that a temporal pattern of descending
activity is not required. The first aim of this study was therefore
to identify the descending brain neurons that control stridulatory behavior and to analyze how the thoracic stridulatory
network is set into action by central commands [some of these
results have been reported in a short communication (Hedwig
1996)]. The second aim was to analyze principle control mechanisms of stridulatory behavior by eliciting another incompatible reaction. In resting crickets cercal wind stimulation evokes
escape running (Gras and Hörner 1992; Stabel et al. 1985).
Cercal wind stimulation of stridulating crickets can alter and
impair the song pattern (Dambach et al. 1983) or evoke a
silencing reaction, during which stridulation transiently stops
0022-3077/00 $5.00 Copyright © 2000 The American Physiological Society
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Hedwig, Berthold. Control of cricket stridulation by a command
neuron: efficacy depends on the behavioral state. J. Neurophysiol. 83:
712–722, 2000. Crickets use different song patterns for acoustic
communication. The stridulatory pattern-generating networks are
housed within the thoracic ganglia but are controlled by the brain.
This descending control of stridulation was identified by intracellular
recordings and stainings of brain neurons. Its impact on the generation
of calling song was analyzed both in resting and stridulating crickets
and during cercal wind stimulation, which impaired the stridulatory
movements and caused transient silencing reactions. A descending
interneuron in the brain serves as a command neuron for calling-song
stridulation. The neuron has a dorsal soma position, anterior dendritic
processes, and an axon that descends in the contralateral connective.
The neuron is present in each side of the CNS. It is not activated in
resting crickets. Intracellular depolarization of the interneuron so that
its spike frequency is increased to 60 – 80 spikes/s reliably elicits
calling-song stridulation. The spike frequency is modulated slightly in
the chirp cycle with the maximum activity in phase with each chirp.
There is a high positive correlation between the chirp repetition rate
and the interneuron’s spike frequency. Only a very weak correlation,
however, exists between the syllable repetition rate and the interneuron activity. The effectiveness of the command neuron depends on the
activity state of the cricket. In resting crickets, experimentally evoked
short bursts of action potentials elicit only incomplete calling-song
chirps. In crickets that previously had stridulated during the experiment, short elicitation of interneuron activity can trigger sustained
calling songs during which the interneuron exhibits a spike frequency
of ⬃30 spikes/s. During sustained calling songs, the command neuron
activity is necessary to maintain the stridulatory behavior. Inhibition
of the interneuron stops stridulation. A transient increase in the spike
frequency of the interneuron speeds up the chirp rate and thereby
resets the timing of the chirp pattern generator. The interneuron also
is excited by cercal wind stimulation. Cercal wind stimulation can
impair the pattern of chirp and syllable generation, but these changes
are not reflected in the discharge pattern of the command neuron.
During wind-evoked silencing reactions, the activity of the callingsong command neuron remains unchanged, but under these conditions, its activity is no longer sufficient to maintain stridulation.
Therefore stridulation can be suppressed by cercal inputs from the
terminal ganglia without directly inhibiting the descending command
activity.
CONTROL OF CRICKET STRIDULATION
(Dambach and Rausche 1985). By stimulating stridulating
crickets with cercal wind stimuli I tested how any changes in
the performance of stridulation are reflected in the activity
patterns of the brain interneurons controlling the behavior.
These experiments were designed to analyze whether the central commands are altered during sensory conditions that modify or suppress stridulatory behavior.
METHODS
Animals and dissection
Intracellular recordings
Microcapillaries were pulled from capillary glass (Clark, Hilgenberg, 1 mm OD) with a David Kopf puller (type 700C). The tip of the
microcapillaries was filled with 5% Lucifer yellow Ch (Sigma) in
double-distilled water and the shaft with 0.1 M LiCl. Microelectrodes
were positioned with a micromanipulator (Leica). A digital gauge
(Mitutoyo, Digimatic Indicator 543; resolution, 1 ␮m) attached to the
manipulator measured the vertical progress of the electrode. Intracellular recordings were made in the bridge mode (npi SEC10 amplifier)
from the medial anterior region of the protocerebrum. Recordings of
the command neurons were obtained at a depth of ⬃200 ␮m. Intracellular current injection was used to modulate the spike rate of the
neurons or to inject dye iontophoretically into the cells. Because of
vigorous ventilatory movements, some of the recordings were made in
AC-coupled mode.
Sensory stimulation and recordings of behavior
Air puffs were delivered to the cerci and posterior area of the
abdomen from a small tube with 1.5 mm ID positioned at a distance
of 20 mm behind the animal. The strength and duration of the air puffs
were controlled by a pressure regulator and an electronic valve. For
acoustic stimulation, a piezoelectric speaker was positioned 31 cm
above the dorsal midline of the animal. Sound pulses (4.5 kHz, 80 dB
SPL amplitude, 25-ms duration; rising and falling ramp, 2 ms) were
delivered by a custom made stimulator.
To monitor the stridulatory movements, a 1.5-mm-diam round
piece of reflecting foil (3 M, Scotchlite type 7610) was stuck to the
lateral part of the right forewing. The animal was illuminated by a DC
light source, and the light reflected by the foil was picked up by a
linear position sensitive diode (Laser Components, Type 1L30-UV)
built into the film plane of a reflex camera. The up-down movements
of the wing, which were recorded by the measuring system, mirror the
opening-closing movements during sound production because the
wings perform an inward-outward rotation during stridulation (Kutsch
1969). In some experiments, sound was recorded simultaneously with
the movements by a microphone (Audio-Technica, AT853Rx) positioned lateral to the animal. Experiments were done at an ambient
temperature of 20 –23°C.
Data analysis
All data were sampled on-line to the hard disk of a PC with
Turbolab 4.3 software (Stemmer Technology, Gröbenzell, Germany)
and a Data Translation A/D board (DT2821 G8DI). The sampling rate
was 10 kHz per channel. Data evaluation was carried out with NEUROLAB software (Hedwig and Knepper 1992; Knepper and Hedwig
1997). Data for correlation and regression analysis were calculated
with NEUROLAB and then exported to a spreadsheet program (MS
Excel 97).
Histology
After recording, the brain was dissected for histological analysis.
The tissue was fixed in 4% paraformaldehyde, dehydrated in ethanol,
and cleared in methylsalicylate. Drawings and photographs of the
stained neurons were made with an epifluorescent microscope (Leica
Dialux 20 or Zeiss Axiophot). After embedding in polyesterwax,
sagittal sections (20 ␮m) of the tissue were cut with a microtome
(Reichert Jung Model 1130/Biocut).
RESULTS
Intracellular recordings and stainings were obtained in the
anterior protocerebrum in an area where electrical stimulation
has been shown to elicit singing behavior (Huber 1960). Several hundred neurons were tested for their behavioral effects by
intracellular stimulation. Some neurons evoked episodic or
rhythmic movements of the abdomen, legs or wings. One type
of descending interneuron that elicited stridulatory behavior
was identified from a total of 15 recordings and nine stainings.
Morphology of the calling-song command neuron
Stainings of this interneuron always revealed a typical structure (Fig. 1, A and B). The soma lies at the dorsal surface of the
protocerebrum ⬃100 –200 ␮m lateral to the midline. The primary neurite loops ventrally in the protocerebrum where it has
a diameter of ⬃7 ␮m. In the ventral protocerebrum, the neurite
divides into major dendritic branches that project bilaterally
toward the pedunculi and especially arborize in the neuropil
between the ␣-lobe and pedunculus (Fig. 1B, left and middle).
The descending axon runs anterior to the central body (Fig. 1B,
right). Collaterals arising from the axon project parallel to the
axon and arborize on both sides of the anterior protocerebrum.
The axon crosses the midline and enters the connective in a
dorsal medial position. In the connectives, the axon has a
diameter of 3– 4 ␮m, and in the subesophageal ganglion, it runs
in a very medial dorsal position. Stained axons could be traced
as far as the prothoracic ganglion, but the terminal arborizations within the thoracic ganglia have not been identified. The
neuron is bilaterally paired and so far the stainings provide no
evidence for sibling command neurons as in the grasshopper O.
viridulus (Hedwig 1994).
Stimulation of calling-song stridulation in resting crickets
Crickets stridulate by rhythmical movement of their forewings. The wings are lifted into singing position and sonorous
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Mature male Gryllus bimaculatus (de Geer) were taken from
cricket colonies at the Departments of Zoology in Göttingen, Germany and Cambridge, United Kingdom. The animals were kept on
sawdust in plastic containers at 25–28°C with a 12-h light:dark cycle.
They were fed a protein-rich diet and water.
Before dissection the animals were cooled to 4°C and immobilized.
They then were positioned upright on a block of Plasticine, and all
legs were restrained by small metal clamps. Care was taken not to
damage the auditory organs in the front legs. The head was rigidly
waxed into a U-shaped holder. The whole preparation then was
positioned so that the head faced upward. The anterior head capsule
was opened, the antennae and the median ocellar nerve were cut, and
the brain was exposed. A platform attached to a micromanipulator was
positioned below the brain, and a second ring-like platform applied
gentle pressure to the anterior surface of the brain to stabilize it for
intracellular recordings. One of the platforms also was used as a
reference electrode. The brain was rinsed constantly with saline (Fielden 1960). Experiments were performed on 85 crickets.
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B. HEDWIG
syllables are produced by opening-closing movements of the
wings. During calling songs, three to five syllables are grouped
within a chirp. Chirp cycles are ⬃350 – 400 ms in duration, and
the syllables last 16 –20 ms each (Fig. 2C) (Huber 1960).
In some experiments, crickets started stridulating when the
microelectrode probed the protocerebrum. This suggested the
close proximity of the crucial descending interneuron. If the
interneuron was impaled and a transiently enhanced spike
frequency was caused, the cricket immediately started to stridulate with a calling song. With a stable recording, calling-song
stridulation could be released by depolarizing current injection
that elicited spike frequencies of 60 – 80 spikes/s (Fig. 2A).
About 500 ms after current injection, the cricket began to raise
its forewings into the singing position, and stridulation started
with low movement amplitude and soft incomplete chirps
sometimes consisting of only one syllable. After a few seconds,
the wings had reached the singing position, and fully developed chirps with three to four syllables were generated. Strid-
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FIG. 1. A: arborization pattern of the descending calling-song command
neuron in the brain of Gryllus bimaculatus in dorsal view. Soma position is
dorsal, the primary neurite loops to ventral areas of the protocerebrum. Axon
and dendrites project anterior to the central body. Lateral dendrites extend
toward the pedunculus of the mushroom body. Axon crosses the midline and
enters the contralateral connective in a median dorsal position. B: 3 compositions of parasagittal sections indicate the arborization pattern of the interneuron
in the median protocerebrum. MB, mushroom body; Ped, pedunculus; CB,
central body; ␣-L, ␣-lobe; PB, protocerebral bridge; DC, deutocerebrum.
ulation continued as long as the enhanced spike frequency was
maintained by current injection. After the end of the applied
depolarization, a few further chirps occurred; however, the
chirp interval distinctly increased and stridulation came to a
stop within the next few seconds. When the stridulatory movements had ceased, the wings remained in the elevated stridulatory posture for many seconds or even minutes before being
lowered gradually into the resting position (Fig. 2B).
During stridulation, the activity of the interneuron showed a
rhythmical modulation in phase with the chirp cycle (Fig. 2, A
and D). The phase relationship between the wing movements
(Fig. 2D, top) and the neuron spikes shows a broad distribution
of the neuron activity within the chirp cycle (Fig. 2D, bottom).
The maximum mean spike frequency of 81spikes/s occurs at
phase ␸ ⫽ 0.1 and coincides with the first and the second
syllable (see Fig. 2D, middle). However, there is no obvious
modulation of the spike activity in the syllable rhythm. The
mean spike frequency gradually decreases to 61 spikes/s toward the end of the chirp cycle at ␸ ⫽ 0.9. It increases again
in phase with the opening movement of the first syllable at ␸ ⫽
0.9 – 0.1. Thus there is a modulation of the spike rate within the
chirp cycle with the major spike activity occurring in phase
with the generation of the chirps. The phase histograms, however, demonstrate that the maximum spike frequency does not
precede the generation of chirps, indicating that the timing of
the chirps is not directly triggered by the rhythmic command
activity. Even after current stimulation, the interneuron remained rhythmically active in the chirp rhythm when stridulation gradually waned (Fig. 2A, see also following text).
Repeated depolarizations of the interneuron, each for several
seconds in duration, reliably elicited repeated bouts of callingsong stridulation (Fig. 3A). During the first current application,
the wings were raised into the singing position and stridulation
started. If the wings were held in the singing position until the
next stimulus, stridulation started with a larger movement
amplitude (e.g., Fig. 3A, beginning of 2nd current pulse). On
the basis of the criteria used for the characterization of command neurons (Kupferman and Weiss 1978), this descending
brain neuron clearly is sufficient to release calling-song behavior in the cricket G. bimaculatus.
The effectiveness of interneuron stimulation in eliciting
stridulation depended on the history of any preceding stridulation. A series of 1-s-long current pulses at intervals of 1.5–2
s, each of which always elicited a spike frequency of 140 –150
spikes/s, were used in resting crickets, which— besides a short
test to identify the interneuron— had not stridulated before in
the experiment (Fig. 3B). The first of the pulses elicited only a
slight elevation of the forewings and some rapid wing movements vaguely resembling chirps. During the second and third
current pulse, the wings were elevated further, and incomplete
chirps were generated at the end of the third pulse. With the
next four current pulses, wing position and stridulation improved, and finally complete chirps with four syllables were
generated by the end of the stimulation series. This suggests
that the sensitivity of the stridulatory pattern generator to
command input is enhanced by maintained stridulation. The
effectiveness of the interneuron activity therefore depends on
the preceding activity of the thoracic pattern-generating network. This becomes particularly clear in crickets that performed long-lasting stridulatory sequences.
CONTROL OF CRICKET STRIDULATION
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Release and inhibition of calling-song stridulation in
“aroused” crickets
Electrical stimulation experiments within the brain and of
the cervical connectives previously have indicated that the
threshold for the release of stridulation decreases once a cricket
has generated a few song sequences. In crickets that had
performed continuous stridulatory activity, for example, a short
sequence of electrical pulses is sufficient to trigger prolonged
stridulation (Huber 1960, 1964; Otto 1971). This change in
threshold could be demonstrated in three crickets at the level of
the descending brain neurons.
The cricket in Fig. 4, A and B, had performed sequences of
prolonged stridulation elicited by maintained intracellular injection of current into the interneuron. A subsequent 1,500-ms
pulse of current caused a burst of action potentials at 130
spikes/s followed 500 ms later by incomplete calling-song
chirps consisting of single syllables. At the end of the depolarization, stridulation was not abolished. Moreover the interneuron activity triggered a sequence of calling-song chirps
with three to four syllables at an average chirp interval of 440
ms. During this “self-maintained” stridulation, the spikes of the
interneuron were modulated in the chirp rhythm (Fig. 4C) even
though their frequency was now much lower than during
stridulation maintained by current injection (see Fig. 2). The
highest average spike rate of 27 spikes/s occurred in phase with
the syllables at ␸ ⫽ 0.2, and this frequency gradually decreased
to an average of 18 spikes/s at ␸ ⫽ 0.85 close to the end of the
chirp cycle. Thus during this self-maintained stridulation, a
much lower discharge rate of the interneuron was sufficient to
maintain stridulatory activity. Before stridulation (Fig. 4A, left)
the spike frequency of the interneuron was as high as the
maximum discharge rate during self-maintained stridulation
but was not sufficient to start stridulation.
Interneuron activity was necessary for self-maintained stridulation to continue. When the interneuron spikes were abolished by hyperpolarizing current injection (Fig. 4B), stridulation stopped immediately, and no additional chirps were
produced. Thus under the circumstances of self-maintained
stridulation the interneuron also fulfilled the necessity criterion
for the characterization of command neurons (Kupferman and
Weiss 1978).
Interneuron impact on chirp rate and syllable rate
Crickets use two different pattern generators to produce the
motor patterns for the chirp rhythm and the syllable rhythm.
The timing of both generators is set independently (Bentley
1969; Kutsch 1969). To characterize more precisely the relationship between the interneuron activity and the chirp and
syllable generators, the correlations between the interneuron
activity and the chirp and syllable rates were analyzed quan-
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FIG. 2. Release of calling-song stridulation in G. bimaculatus by intracellular current injection into a single descending brain
neuron. A: after an initial activity peak, the current pulse (top) elicits a spike rate of 60 – 80 spikes/s (2nd and 5th traces). Cricket
raises its wings into singing position (3rd trace) and starts sonorous stridulation (4th trace). Singing stops after the end of
stimulation. During stridulation, the neuron activity is modulated rhythmically in the chirp rhythm. B: gradual repositioning of the
wing after the sequence of calling-song stridulation takes 50 s. Slow movements of the wing are due to ventilatory contractions of
the abdomen. C: chirp and syllable pattern during calling song. The calculation of phase values for syllables and spikes was done
corresponding to phase ⫽ t/chirp cycle. D: average wing movement during the chirp cycles. Prior to averaging, all chirp cycles were
normalized to a unit length of 1.0 (top). Phase histogram of the syllables, the maximum of the opening movement, is taken as
indicator of a syllable (middle). Bottom: phase histogram of the neuron activity together with the average instantaneous spike
frequency (left ordinate for peristimulus time (PST) histogram and right ordinate for average spike frequency). All averages are
calculated corresponding to the phase of the chirp cycle. In phase with the chirps, the neuron activity reaches 81 spikes/s where
it is 61 spikes/s in the chirp interval. The number of evaluated chirps, and the number of syllables and spikes that occur during these
chirps, is indicated by n in each histogram. Number of bins, 100; binwidth corresponds to 3.65 ms. All chirps from a single animal.
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B. HEDWIG
FIG. 3. A: reliable stimulation of calling-song stridulation in a resting
cricket. Interneuron was depolarized by 3 consecutive current pulses of 7- or
8-s duration that elicited a spike frequency of 120 –130 spikes/s. During the
first current pulse, the wings were raised into singing position and stridulation
started with wing movements of low amplitude. Wings remained raised, and at
the beginning of the following current pulse, stridulatory movements started
with greater amplitude. B: repeated stimulation with 1-s depolarizing current
pulses increases the intensity of calling-song stridulation. Each current pulse
elicits a rate of 140 –150 spikes/s in the interneuron. During the 1st stimulus,
the wings were raised and several incomplete chirps were generated. During
the following current pulses, the wings were more raised and more complete
chirps with 4 syllables were produced.
titatively. The instantaneous spike frequency was calculated at
the onset of chirps and at the time of maximum syllable rate of
each chirp (Fig. 5, A and B, insets). Calling-song sequences
either were evoked by intracellular current injection or were
self-maintained so that a wide range of interneuron spike
frequencies could be pooled for the analysis. The chirp repetition rate and the maximum syllable repetition rate within each
chirp were determined for stable parts of stridulatory sequences
only. Chirps immediately after the onset or offset of current
injection were not considered.
The correlation analysis between the interneuron’s spike
frequency and the chirp repetition rate (Fig. 5A) shows a high
positive correlation coefficient (r ⫽ 0.83, significant at 0.001%
niveau) and a linear regression function with y ⫽ 0.0237x ⫹
1.69. This demonstrates a tight coupling between the interneuron activity and the chirp repetition rate. The chirp rate increases linearly from 2.4 chirps/s at 30 spikes/s to 4.5 chirps/s
at 120 spikes/s. Only a very weak correlation was revealed
between the interneuron’s activity and the maximum syllable
rate of the song (r ⫽ 0.1, significant at 0.01% niveau) with the
linear regression function y ⫽ 0.0042x ⫹ 26.44 (Fig. 5B).
Independent of the neuron activity, the maximum syllable rate
stays between 26.6 syllables/s at 30 spikes/s and 26.9 sylla-
Sensory feedback to the calling-song command neuron
To identify possible sources of the rhythmical modulation of
the interneuron spike frequency during stridulation, the effect
of different sensory modalities was tested. Changes in light
intensity and auditory stimulation (80 dB SPL, 4.5-kHz pulses
with 25-ms duration; Fig. 6A) did not evoke any synaptic input
in the interneuron in resting or stridulating crickets. A sensory
stimulus so-far identified that evoked activity of the neuron
was puffs of air blown across the cerci (Fig. 6B). The air puffs
increased the spike activity of the interneuron and also elicited
abdominal contractions similar to ventilatory contractions,
which slightly lifted the wings (see Fig. 2B). The enhanced
interneuron activity therefore also might have been caused by
any proprioceptive feedback from the abdomen and wings.
Because abdominal movements alone did not elicit any enhanced interneuron activity, it is suggested that cercal wind
stimulation is a source for sensory feedback to the descending
command neurons.
Command neuron activity and cercal wind stimulation
during stridulation
In naturally singing crickets (G. campestris), stimulation of
cercal hairs with air puffs can elicit two different behavioral
effects; single weak air puffs change the chirp rhythm (Dambach et al. 1983). Stronger air puffs elicit a silencing response
during which crickets lower their wings and stop stridulation
(Dambach and Rausche 1985). Here puffs of air disturbed the
chirp rhythm and when delivered within a chirp, also disrupted
the performance of the syllables within that chirp (Fig. 7A).
Silencing reactions could be evoked by increasing the amplitude of the air puffs.
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bles/s at 120 spikes/s. The interneuron activity, therefore drives
the thoracic chirp pattern generator but has no impact on the
repetition rate of the syllables.
To test the effect of experimentally increased neuron activity
on the performance of the ongoing behavior (Fig. 5C), intracellular current injection was used to modulate the interneuron
spike frequency during self-maintained stridulation. During
such sequences, the discharge rate was rather low, ⬃30
spikes/s, and the chirp repetition rate was 3.6 chirps/s. When
the interneuron discharge rate was transiently enhanced to 146
spikes/s, the chirp rate also transiently increased to 5.6 chirps/s.
Thus increasing the spike rate drives the chirp generator and
shifts the chirp repetition rate corresponding to the regression
function (Fig. 5A). This effect of course also led to a reset of
the chirp generator. The chirps after the onset of stimulation
occurred before moment based on the previous chirp rate. Note
that the time between the onset of the intracellular stimulus and
the consecutively following chirp is only 150 ms and well
beyond the duration of a chirp cycle. Therefore a sudden short
increase in the interneuron activity will be sufficient to reset the
thoracic chirp pattern generator.
There was no change of the maximum syllable repetition
rate during the intracellular interneuron stimulation; it was 26.2
syllables/s before and at 26.4 syllables/s during the current
injection. There was, however, a reduction in the number of
syllables generated during each chirp; this also is described by
Otto (1971).
CONTROL OF CRICKET STRIDULATION
717
The behavioral effects of air puffs applied to the cerci can be
demonstrated when self-maintained stridulation occurs during
intracellular recordings (Fig. 7B). In these experiments, calling-song stridulation occurred after intracellular current injection of the descending command neuron. Air puffs of different
strength were delivered to the cerci. When presented during
ongoing chirps, air puffs led to a slight increase in the interneuron spike rate, for example, from 20 to 29 spikes/s for the
duration of 160 ms. An increase in the interneuron activity also
should increase the singing activity, but the chirps ended
prematurely. The evoked change in the syllable pattern was not
reflected in any obvious change in the command neuron activity. This may correspond to the finding that there also was no
correlation between the syllable rate and the interneurons spike
frequency.
Higher strength of air puffs elicited a transient increase in
the interneuron activity and a silencing of the motor pattern
(Fig. 8A). The cricket remained silent for several seconds and
then began to stridulate again. During the pause in stridulatory
behavior, however, the command neuron continued to spike
with the same average spike frequency as during stridulation.
Data from five experiments in three animals show the average
wing position and spike histogram and interneuron spike rate
during the silencing reaction (Fig. 8B). The wing position
indicates a rapid lowering of the wings starting ⬃110 ms after
the beginning of the air puff. In the interneuron, the average
discharge rate increased during the air puff to ⬃58 spikes/s.
Before the air stimulus, while the cricket was still stridulating
and after the stimulus during the silencing reaction, the average
spike frequency was constant at ⬃33 spikes/s. The silencing
reaction changed the performance of the stridulatory motor
activity without an obvious modification of the descending
command neuron activity. Thus during the silencing reaction,
the command neuron activity was not effective in maintaining
calling-song stridulation. In this experimental situation, it
failed to meet the sufficiency criterion.
DISCUSSION
Within the brain of G. bimaculatus, a descending interneuron was identified as a command neuron for calling-song
stridulation. The function of this interneuron seems to be rather
complex because its discharge is modulated rhythmically during stridulation, it can modulate and reset the stridulatory
pattern generator, it may receive sensory feedback, and its
effectiveness changes depending on the behavioral state of the
animal. Together these features are beyond a simple control of
a rhythmic motor pattern by a command interneuron and indicate a high degree of plasticity within the stridulatory motor
system.
Stimulation sites and descending brain neurons in the cricket
In the cricket, electrical stimulation in the anterior protocerebrum (Huber 1960, 1964) and extracellular electrical stimulation of a dorsal medial axon within the connectives (Bentley
1977) were most effective in eliciting calling song. The arborization pattern of the calling-song command interneuron
corresponds to these stimulation sites. I therefore suggest that
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FIG. 4. A: brief increase in interneuron firing from 30 to 130 spikes/s caused by injection of depolarizing current triggered a
long-lasting sequence of stridulation in an aroused cricket. Interneuron activity was modulated rhythmically during stridulation. B:
suppression of the interneuron‘s spike activity by hyperpolarizing current injection stopped the calling song. C: average of the wing
movements during chirps (top), phase histograms of the syllables (middle), phase histogram of the action potentials (bottom left),
and average of the instantaneous spike frequency in the chirp cycle (bottom right). Maximum spike rate occurred in phase with the
generation of the chirps.
718
B. HEDWIG
FIG. 6. A: interneuron did not respond to acoustic stimulation at 4 kHz, 80
dB SPL. Interneuron was hyperpolarized with 3 nA throughout the recording.
B: stimulation of the abdomen with air puffs was followed by excitation of the
interneuron but also caused abdominal contractions which passively elevated
the wings.
Descending interneuron as a command neuron for
calling song
Wiersma and Ikeda (1964) introduced the concept of command neurons, postulating that the brain of invertebrates controls coordinated movements by tonic activity of specific sets
of interneurons. More rigid criteria for the characterization of
command neurons were established by Kupferman and Weiss
FIG. 5. Statistical analysis of the correlation between the spike frequency
and the chirp and syllable repetition rate, respectively. A: there is a high
correlation (r ⫽ 0.83) between the interneuron spike frequency and the chirp
rate. B: there is no correlation (r ⫽ 0.1) between the maximum syllable rate
and the interneuron spike rate. C: intracellular current injection into the
interneuron during self-maintained stridulation evoked a transient increase of
the spike rate that caused a transient increase in the chirp rate and reset the
chirp pattern. Dots indicate the expected continuation of the chirp pattern if no
current would have been applied. There was no change in the maximum
syllable rate.
the effects of earlier stimulation experiments were mediated by
the direct or indirect activation of the calling-song command
neuron identified in the present paper.
A survey of interneurons and soma cluster in the cricket
brain reveals ⬃200 descending brain neurons projecting into
each circumoesophageal connective (Staudacher 1998). Individual descending interneurons are involved in the processing of visual stimuli (Richard et al. 1985), acoustic
stimuli (Boyan and Williams 1981; Brodfuehrer and Hoy
1990), or exhibit multimodal response properties (Hörner
and Gras 1985). Some descending interneurons alter their
FIG. 7. A: air puffs of 50-ms duration delivered to the cerci disturbed
ongoing calling-song activity. Air puffs impair the chirp rhythm and terminated ongoing chirps. B: air puff prematurely terminates a chirp, but the change
in the stridulatory motor activity is not accompanied by any change in the
firing rate of the interneuron.
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sensory responses during walking and may even function as
command neurons for walking (Böhm and Schildberger
1992; Staudacher and Schildberger 1998). All these descending interneurons exhibit great differences in arborization patterns and none of them matches the structure of the
descending calling-song command neuron.
CONTROL OF CRICKET STRIDULATION
719
(1978): command neurons should be sufficient and necessary
for the performance of a particular motor behavior. Stimulation
of the interneuron should evoke the behavior in a resting
animal and inhibition of the interneuron should prevent occurrence of the behavior. Although only a small number of command neurons fulfill both of these criteria (e.g., Edwards et al.
1999; Fredman and Jahan-Pawar 1983; Frost and Katz 1996;
Hedwig 1994; Nolen and Hoy 1984) many higher order “command-like” interneurons have been shown to be sufficient and
not necessary to release a rhythmic motor pattern (e.g., Boyan
et al. 1986; Brodfuehrer et al. 1995; Granzow and Kater 1977;
Hedwig 1992; McCrohan 1984; Pearson et al. 1985; Weeks
and Kristan 1978). This may be due to a redundant organization of these command systems. The described interneuron in
the brain of G. bimaculatus must be regarded as a command
neuron for calling-song stridulation. In resting crickets, it is
sufficient to elicit stridulation, and stridulation stops whenever
the neuron is prevented from firing during self-maintained
calling song. The stainings so far do not indicate more than one
of these neurons in each side of the brain. If there would be
multiple copies of the neuron, the necessity criterion might not
always be fulfilled as in redundantly organized command systems (see Hedwig 1994 for discussion of this point).
Control of calling-song chirp rate
Singing activity in crickets can be released by electrical
stimulation of the neck connectives (Otto 1971) or of axon
bundles of the cervical connectives (Bentley 1977). At stimu-
lus repetition rates of 55 and 75 stimuli/s, chirp rates of 2.9 and
3.4, respectively, were released (Bentley 1977) and at 75
stimuli/s, Otto (1971) obtained 3.3 chirps/s. A linear extrapolation based on intracellular stimulation gives chirp rates of 3.0
chirps/s for 55 spikes/s and of 3.5 chirps/s at 75 spikes/s. This
suggests that the same descending interneurons were investigated in the different studies.
There is a linear relationship between the spike frequency of
the interneurons and the chirp repetition rate. Linear relationships between the interneuron activity and the expression of a
motor pattern also have been found in other command systems,
e.g., swimmeret movement of the crayfish (Davis and Kennedy
1972). Such a relationship indicates that the driving cell has
direct control over the motor pattern. It also implies that any
sufficient increase in the tonic command neuron activity can
accelerate and even reset the motor rhythm as demonstrated in
Fig. 5C. A reset of the motor pattern also has been obtained
with command-like interneurons for swimming in the leech
(Weeks and Kristan 1978, Fig. 8), for feeding in Lymnaea
(McCrohan 1984, Fig. 2), and with command neurons for
stridulation in a grasshopper (Hedwig 1994, Fig. 7). Generally,
a neuron that can reset a motor pattern is thought to be an
element of that pattern-generating network (e.g., Ramirez
1998). The present data and data on leech neuron 204 (Weeks
1981), however, demonstrate that a pattern generator can be
reset and speeded up by a neuron that is not an element of the
pattern-generating network but that has only a suitable driving
input. This may force us to analyze critically whether or not a
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FIG. 8. A: silencing reaction caused by an air puff delivered
to the cerci of a singing cricket. Cricket lowered its wings and
stopped stridulation for 4 s. Interneuron responded to the air
puff with a slight transient increase in the spike rate but then
continued to fire with the same rate as before the silencing
reaction. B: average response of the wing (2nd trace) and the
interneuron (2 bottom traces) in 5 different silencing reactions
obtained in 3 singing crickets. Wings are lowered after 110 ms.
There is an increase in the spike activity after ⬃70 ms. During
stridulation and during the silencing reaction, the interneuron
activity remains at ⬃33 spikes/s.
720
B. HEDWIG
reset was obtained as an epiphenomenon by modulating the
driving input to a pattern generator or by modulating an element of the pattern-generating network itself.
Activity of command neurons and production other
song types
Rhythmic modulation
Command neurons are thought not to carry specific timing
information for the production of a motor program (Pearson
1993; Stein 1978). Tonic activation of a command neuron
generally is sufficient to elicit a corresponding behavior. However, command-like neurons in several systems exhibit a pronounced rhythmic modulation of their activity during the performance of the behavior, e.g., CV1 interneuron initiating
feeding motor output in Lymnea stagnalis (McCrohan 1984),
DRI during swimming in Tritonia (Frost and Katz 1996); PCN
neurons for feeding in Pleurobranchaea, (Gillette et al. 1978,
1982). In Pleurobranchaea and also in Lymnea, the modulation
is mediated by an inhibitory feedback from the motor patterngenerating network and contributes to rhythm generation. Huber (1960, 1964) postulated that the brain of crickets generates
a patterned descending activity controlling the chirp rhythm.
The calling-song command neuron exhibits a slight and gradual modulation of its spike frequency by ⬃25–30% in the chirp
cycle. The phase diagrams (Figs. 2D and 4C) indicate that the
discharge rate increases simultaneously with the generation of
the chirp. Therefore it rather seems that the modulation of the
descending command neuron activity is not properly timed to
initiate the single chirps and its functional role is not yet clear.
A central feedback from the thoracic pattern-generating net-
Command neuron activity and behavioral state
Extracellular stimulation experiments have demonstrated
previously a high degree of facilitation and threshold reduction
of the thoracic stridulatory network. After consecutive sequences of stimulation, the stridulatory sequences became
longer until the stridulatory activity could go on without any
additional stimuli (Huber 1960, 1964; Otto 1971). Because
these effects occur even when the connectives or single command neurons are stimulated, the underlying changes must
occur in the thoracic pattern-generating system rather than in
the brain. As a consequence, the impact of the calling-song
command neuron clearly depended on the activity state of the
thoracic system. Stimulation elicited premature calling-song
chirps in resting crickets or triggered continuous calling-song
sequences after considerable preceding stridulation had occurred. Data on the thoracic stridulatory pattern-generating
mechanism in crickets are still very limited (Bentley 1969;
Henning 1989, 1990). We may understand the changes in the
effectiveness of command neuron activity once the thoracic
pattern-generating interneurons postsynaptic to the command
neurons are identified and their physiological properties are
characterized.
Stein (1978) distinguished between trigger and gating command neurons. Trigger command neurons evoke behavioral
sequences that last longer than the command neuron activity,
whereas the typical (gating) command neurons are activated
continuously to maintain motor activity. In the leech, both
types of command neurons, the trigger neuron TR1 and the
gating neurons 204, 61, and 21 (see Brodfuehrer et al. 1995 for
review) are involved in the swim-activating system. Properties
of both functional types can be assigned to the calling song
command neuron depending on the activity state of the thoracic
system. Although it is not yet clear whether or not both
properties are functional in the control of stridulation, on
balance it seems that the interneuron is acting more like a
gating than like a trigger neuron. This observation, however,
demonstrates the difficulties in categorizing command neurons.
Of course stimulation experiments of single interneurons do
not necessarily tell something definite about the function of
that particular interneuron within a network. They moreover
demonstrate how the postsynaptic network responds to the
input from that interneuron. Thus the effectiveness of the
interneuron is a function of the state of the postsynaptic network.
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During extracellular brain and connective stimulation experiments, there are often transitions between the calling song and
rivalry song or between the calling song and courtship song
(Huber 1960; Otto 1971). Transitions between song patterns
did not occur during any intracellular stimulation experiments.
Activation of the interneuron only elicited the calling song
even at experimentally induced spike rates of 160 spikes/s. It is
therefore unlikely that different song types in G. bimaculatus
are controlled by the activity of a single interneuron as proposed by Otto (1971) or Bentley (1977). Further, preliminary
data indicate that a different type of descending interneuron is
involved in the control of courtship song (B. Hedwig, unpublished data). The control of the different stridulatory motor
patterns in the cricket rather seems to be organized with labeled
lines as in the acridid grasshopper O. viridulus where three
different types of descending brain neurons specifically control
three different types of stridulatory motor patterns (Hedwig
1994; Hedwig and Heinrich 1997). A multifunctional command-like interneuron contributing to six different types of
behaviors involving head movements has been described in
Aplysia (Xin et al. 1996). So far, however, there is no experimental evidence that the calling song command neuron is
multifunctional and is involved in the control of other behaviors as well. It may have to be considered that under the
pressure of sexual selection that drives the evolution of acoustic communication systems, the emergence of a hardwired
neuronal control system for the generation of acoustic signals
may have been favored.
work could account for the rhythmic modulation of the command activity. Another source could be a sensory feedback to
the cricket calling song interneuron by the wind-sensitive system of the cerci. The ascending giant fiber system of crickets
responds to low-frequency air currents that occur during stridulation (Kämper 1984; Kämper and Dambach 1981), and the
chirp rhythm can be modified by cercal wind stimulation
(Dambach et al. 1983). Cercal wind stimulation elicits responses in a number of local (Schildberger 1984) and descending brain interneurons (Hörner and Gras 1985). Because wind
stimulation also elicits responses in the calling-song command
neuron, it may indeed contribute to the rhythmic modulation of
the command activity.
CONTROL OF CRICKET STRIDULATION
Decisions about behavior: stridulation and silencing
reaction
about wind stimulation of the cerci is carried by the cercal giant
and nongiant fiber system (Edwards and Palka 1974; KohstallSchnell and Grass 1994; Mendenhall and Murphey 1974) and
first will reach the thoracic ganglia before entering the brain. A
motor response to cercal wind stimulation can be mediated
fastest when the ascending pathway directly activates the thoracic motor networks, avoiding any loop via the brain. The
neuronal decision, allowing the silencing reaction to dominate
over stridulation, seems to be located at the level of the
thoracic ganglia. Because the stridulatory command is not
switched off, it allows stridulation to recommence when the
silencing reaction wanes. The synaptic mechanisms within the
thoracic ganglia that underlie the precedence of silencing over
singing now may be analyzed in future experiments.
I thank my Cambridge colleagues M. Burrows, T. Matheson, M. Wildman
and J. Poulet for critical and constructive comments on the manuscript and M.
Schink (Göttingen) for support with the histology.
One part of this study was conducted at the Department of Zoology,
Göttingen, and was supported by the Heisenberg Programm of the Deutsche
Forschungsgemeinschaft (He 2018/1-3). The other part was done at the Department of Zoology, Cambridge, and was supported by a Biotechnology and
Biological Sciences Research Council Grant to M. Burrows and B. Hedwig.
Address for reprint requests: Dept. of Zoology, Downing Street, Cambridge
CB2 3EJ, UK.
Received 13 July 1999; accepted in final form 9 October 1999.
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