2265
The Journal of Experimental Biology 204, 2265–2275 (2001)
Printed in Great Britain © The Company of Biologists Limited 2001
JEB3559
PHYSIOLOGICAL CHARACTERISATION OF ANTENNAL MECHANOSENSORY
DESCENDING INTERNEURONS IN AN INSECT (GRYLLUS BIMACULATUS,
GRYLLUS CAMPESTRIS) BRAIN
MICHAEL GEBHARDT* AND HANS-WILLI HONEGGER‡
Institut und Lehrstuhl für Zoologie, Technische Universität München, Lichtenbergstrasse 4,
85747 Garching, Germany
*e-mail: Michael.Gebhardt@bio.tum.de
‡Present address: Department of Biology, Vanderbilt University, Box 1812, Station B, Nashville, TN 37235, USA
Accepted 18 April 2001
Summary
We investigated five different descending brain
interneurons with dendritic arborizations in the
deutocerebrum in the crickets Gryllus bimaculatus and G.
campestris. These interneurones convey specific antennal
mechanosensory information to the ventral nerve cord
and all responded to forced antennal movements. These
interneurones coded for velocity and showed preferences
for distinct sectors of the total range of antennal
movements. Their axons descended into the posterior
connective either ipsilateral or contalateral to the cell
body. Electrical stimulation of sensory nerves indicated
that the interneurons received input from different
afferents of the two antennal base segments. One
interneuron had a particularly large axon with a
conduction velocity of 4.4 m s−1. This was the only one of
the five interneurons that also received visual input.
Its activity was reduced during voluntary antennal
movements. The reduction in activity occurred even after
de-efferentation of the antenna, indicating that it had a
central origin. Although we do not have experimental
evidence for behavioural roles for the descending antennal
mechanosensory interneurons, the properties described
here suggest an involvement in the perception of objects in
the path of the cricket.
Key words: insect, cricket, descending brain interneurone, antenna,
mechanoreception, vision, efference copy, Gryllus bimaculatus,
Gryllus campestris.
Introduction
Antennae are important multimodal sense organs in insects
(e.g. Fuldalewizc-Niemczyk and Rosciszewska, 1973;
Schaller, 1978; Stengl et al., 1990). Unlike many other sense
organs, antennae can be actively moved relative to the body.
In particular, insects with antennae longer than one body
length, such as crickets, have antennae that are precisely
targeted at objects around the animal (Honegger, 1981). During
walking, the antennae move continuously to scan the terrain
ahead of the insect (Horseman et al., 1997; Dürr, 1999) and
serve as mobile multimodal sensors of the environment around
the insect.
Antennal movements are controlled by mechanosensory
afferents located at the first two antennal segments, the scape
and the pedicel (Kammerer and Honegger, 1988). The
maintenance of antennal movements and postures, however,
requires a connection between the brain and the
suboesophageal ganglion (Horseman et al., 1997). Antennal
mechanosensory afferents also participate in flight control
(Gewecke, 1974) and gravity perception (Horn and Bischoff,
1983), and their stimulation may elicit evasive behaviour
(Burdohan and Comer, 1990; Stierle et al., 1994; Burdohan and
Comer, 1996). These various functions require a connection
between antennal mechanoreceptors and the motor centres
of the thoracic ganglia. Since the branches of antennal
mechanoreceptive afferents are confined to the deutocerebrum
and the suboesophageal ganglion (Suzuki, 1975; Bräunig et al.,
1983; Rospars, 1988; Honegger et al., 1990; Staudacher
and Schildberger, 1999), intersegmental interneurons must
necessarily relay the output of these antennal mechanosensory
afferents to the thoracic ganglia.
Our experiments were aimed at characterising the sensory
physiology of descending brain interneurons that receive
inputs from antennal mechanosensory afferents. We recorded
intracellularly in the deutocerebrum from such interneurons,
which were activated during forced antennal movements.
Single-cell staining revealed the dendritic arborizations in the
deutocerebrum and the positions of the somata in the dorsal
protocerebrum. The interneurons belong to a population of
approximately 200 descending brain interneurons that have
been characterised morphologically (Staudacher, 1998).
Some of the data presented in this study have been published
in abstract form (Gebhardt and Honegger, 1997).
2266 M. GEBHARDT AND H.-W. HONEGGER
Materials and methods
Experimental animals
Experiments were performed on adult Gryllus bimaculatus
De Geer of either sex obtained from our laboratory culture and
on Gryllus campestris L. caught near Munich, Bavaria,
Germany.
Preparation and electrophysiology
The electrophysiological methods used in this study followed
standard protocols for intracellular recording and staining with
Lucifer Yellow or hexammine cobaltic chloride (Stewart, 1978;
Brogan and Pitman, 1981). Electrode resistance ranged from
40 to 80 MΩ (borosilicate capillaries, Clark Biomedical
Instruments). Briefly, the cricket was fixed dorsal side up on a
cork holder, and the brain was exposed by removing the frontal
cuticle of the head together with the underlying adipose tissue.
A silver platform was used to stabilise the brain and served as
a reference electrode. Penetration of the ventral sheath of the
brain by the microcapillaries was facilitated by the application
of collagenase (one crystal, type IV, Sigma) for 45–60 s. In all
experiments, the interneurons were impaled with the
microelectrode in their deutocerebral dendrites. The activity of
antennal motoneurons was recorded with a pair of hook
electrodes implanted under nerve N4B, which contains the
axons of one adductor motoneuron and of three abductor
motoneurons, or under N4, which contains the axons of nine
antennal motoneurons (Honegger et al., 1990). In total,
60 recordings were made from descending antennal
mechanosensory interneurons. All experiments were carried out
at an ambient temperature of 20–22 °C.
Stimulation
The interneurons were stimulated by forced deflections of
the antenna. One antenna was cut at the tenth flagellar segment,
and a minuten pin was inserted a few segments deep into the
remaining stump. The first antennal joint was immobilised by
gluing the scape to the head capsule. We focused on the second
antennal joint between the scape and the pedicel because
horizontal antennal movements are naturally executed at this
joint and its organisation is simpler than that of the head–scape
joint. The latter includes five muscles and 10 motoneurons
compared with two muscles and seven motoneurons
controlling the scape–pedicel joint. The minuten pin with
the attached flagellum was deflected using a magnet
(0.5 mm×0.5 mm×1.0 mm) fixed to a servo-motor (Megatron
type 26-2) controlled by a custom-built feedback waveform
generator. ‘Ramp-and-hold’ stimuli were delivered with
different ramp velocities, angular amplitudes and holding times
that were within the range of natural antennal movements.
Controlled visual stimuli (looming disks, moving grids and
dots) were generated on a PC and displayed on a computer
monitor (refresh rate 72 Hz) centred in front of one compound
eye of the cricket. The monitor screen subtended 45 °×59 ° at
the eye. Care was taken to align the screen parallel to the eye
to avoid distortions in the angular size and velocity of the
patterns displayed. To characterise the gradient of visual
sensitivity of interneuron DBNi1-2, stationary black dots
subtending 8 ° were displayed on a white background. Dots
were displayed at the centre and at the four corners of the
screen for 400 ms in random sequences for each trial.
In experiments on antennal–mechanosensory inputs to the
interneurons, both optic nerves were cut to prevent unwanted
visual stimulation by the moving magnet. Other stimuli tested
were puffs of odour to the antenna (e.g. acetic acid, sage
extract, lavender extract, tobacco smoke), hissing and other
sounds and touching different parts of the body of the cricket.
Antennal sensory nerves were electrically stimulated by pairs
of hook electrodes insulated with petroleum jelly. Stimulation
pulses were 0.5 ms in length and ranged between 1 and 6 V.
Data analysis
Recordings together with stimulus monitors were taped
(Racal Store D7) and later digitised (CED 1401, Cambridge
Electronic Design Ltd) and analysed off-line on a PC using
Spike2 software (Cambridge Electronic Design Ltd). The
responses of the interneurons to antennal stimulation were
evaluated only if no antennal motor activity occurred.
The strength of synaptic activity in interneuron DBNi1-2
was quantified by calculating the integrals of the membrane
potential over a period of 200 ms. Antennal motoneuron spikes
were counted over the same intervals to quantify antennal
motor activity. The intervals were chosen either from the
onsets of motoneuron bursts or from episodes without any
motor activity. An interval of 200 ms was chosen because it
corresponded to the minimum duration of spontaneous bursts
of antennal motor activity. Before calculating integrals, the
recordings were digitally low-pass-filtered using default
Spike2 digital filter functions to remove action potentials
(−3 dB at 281 Hz). Data from different animals were separately
normalised to maximum spike counts or to maximum integrals
of synaptic potentials for each experiment and then pooled.
Non-parametric statistical tests were performed using WinStat
software (Kalmia Co. Inc.).
Results
We describe the morphology and sensory physiology of the
descending interneurons DBNi1-2, DBNi2-1, DBNc1-2,
DBNc2-2 and DBNc2-3 (Fig. 1) identified morphologically by
Staudacher (Staudacher, 1998) according to the location of
their cell bodies in distinct soma clusters in the rind of the
protocerebrum. The terminology for these interneurons was
coined by Staudacher (Staudacher, 1998). For instance,
DBNi1-2 is the second descending brain neuron of soma
cluster 1 with an axon descending ipsilateral to the soma. All
neurons with their axons in the contralateral connective carry
the label ‘DBNc’. A similar terminology for descending
cephalic interneurons in grasshoppers, active during
stridulation, was used by Hedwig (Hedwig, 1986). All the
interneurons described in this study have a characteristic
dendrite in the non-glomerular deutocerebrum, thus
differentiating them from other descending interneurons. We
Descending brain interneurones in crickets 2267
A
B
DBNi1-2 (brain)
C
DBNi1-2 (sog)
ant.
DBNi1-2 (dendrite)
N1
AL
lat.
*
ant.
lat.
100 µm
100 µm
D
DBNi2-1
E
F
DBNc1-2/c2-2
DBNc2-3
Optic
nerve
Protocerebrum
Antennal
nerve
Deutocerebrum
Circumoesophageal
connective
Fig. 1. (A–F) Morphology of the descending interneurons that receive antennal mechanosensory input. (A) DBNi1-2 is characterised by its
large dendrite (arrow), which ramifies extensively in the ventral antennal mechanosensory part of the deutocerebrum. Another dendrite extends
anteriorly into the lateral protocerebrum (arrowhead). The axon (asterisk) projects into the ipsilateral connective. ant., anterior; lat., lateral.
(B) Sparse projections of DBNi1-2 in the suboesophageal ganglion (sog). (C) Fan-like projections of DBNi1-2 in a typical intracellular fill
(Lucifer Yellow). AL, antennal lobe; N1, flagellar nerve 1. (D) DBNi2-1 ramifies extensively in the deutocerebrum (arrow) dorsal to DBNi1-2.
Dense arborizations are present in the medial protocerebrum (arrowhead). (E) The DBNc1-2/c2-2 interneuron descends into the connective
contralateral to the soma. The single main dendrite is in the ispilateral deutocerebrum. (F) The contralaterally descending DBNc2-3 interneuron
is characterised by a primary neurite devoid of any branchings and a fan-like dendrite in the deutocerebrum. All diagrams are in ventral view.
could reliably identify interneurons DBNi1-2, DBNi2-1 and
DBNc2-3 on the basis of their morphology. We do not,
however, distinguish between DBNc1-2 and DBNc2-2, both of
which showed very similar morphologies and physiological
responses. In addition, they do not meet the identification
criteria of Staudacher (Staudacher, 1998) in our preparations.
They will therefore be referred to as ‘DBNc1-2/c2-2’.
Morphology
The axons of the interneurons under consideration project
into the circumoesophageal connectives either ipsilateral
(DBNi1-2, DBNi2-1) or contralateral (DBNc1-2/c2-2,
DBNc2-3) to the cell bodies (Fig. 1A,D–F). All interneurons
have their major dendrite in the lateral deutocerebrum. They
differ, however, in the shape and in the ventro-dorsal extent of
their branchings in this neuropile. While DBNi2-1 ramifies in
the dorsalmost layers of the deutocerebrum, the branchings of
DBNc1-2/c2-2 are more medial. The dendrites of DBNi1-2 and
DBNc2-3 are positioned more ventrally.
DBNi1-2 projects with regularly spaced fan-like branches
(Fig. 1C) running close to the ventral surface of the brain into
a mechanosensory neuropile of the deutocerebrum, where
flagellar afferents project (vfa; Staudacher and Schildberger,
1999). This regular branching pattern of the dendrite suggests
2268 M. GEBHARDT AND H.-W. HONEGGER
A
23°
Antennal
deflection
10 mV
DBNi1-2
2s
Abduction
Adduction
0°
C
B
Spikes per ramp, normalised
Fig. 2. (A–D) Response characteristics of
DBNi1-2 evoked by forced deflections of
the second antennal joint between the scape
and pedicel. (A) Compound excitatory
postsynaptic potentials (EPSPs) elicited by
imposed movements with ramps of amplitude
23 ° at an angular velocity of 300 ° s−1 during
both adduction and abduction of the antenna.
The positions of the antenna at the extreme
positions of the deflection are indicated as
insets. (B) Correlation between the increase in
spike frequency and movement velocity up to
900 ° s−1 during abduction and adduction
between 0 and 100 °. Values are means ±
S.E.M. of normalised data for 3–7 stimulus
periods in five animals. (C) Directional
sensitivity to imposed deflections of the
scape–pedicel joint (range 0–80 °; four steps of
20 ° each; 300 ° s−1 as in A). Curves indicate
relative mean spike counts (± S.E.M.) per ramp
(N=7 animals). The curves are discontinuous
every 20 °, corresponding to the pauses
between two ramps at a constant angular
position. Arrows indicate the direction of
movement (the outer curves are for
movements towards the back of the insect;
abduction); the solid line at 30 ° indicates the
antennal resting position. The radius of circles
represents the percentage of the maximum
response (outer circle, 100 %). The shaded
sector indicates the range of naturally
occurring movements of the scape–pedicel
joint. (D) Electrical stimulation of afferent
antennal nerves during intracellular recording
from DBNi1-2. The shortest latencies (2 ms)
resulted from stimulation of N1 in the scape
(the arrow indicates spikes). Electrical
stimulation of the flagellar N1 resulted only in
EPSPs of small amplitude and long latency
(7 ms). Stimulation of N2B failed to elicit any
responses. The downward shift in the
intracellular trace after stimulation is due to the
microelectrode capacitance and was also seen
when the electrode tip was extracellular. sc,
scape; pd, pedicel; fl1, first flagellar segment;
fl6, sixth flagellar segment. Asterisks indicate
transient stimulation artefacts. Each recording
consists of five superimposed sweeps.
0.8
90°
0.4
0
100
300
900
Angular velocity (degrees s-1)
D
Stimulation of N1 (flagellum)
fl6
*
*
a topological ordering of the surrounding sensory neuropile.
An additional dendrite emerges from the primary neurite and
extends anteriorly into the dorsolateral protocerebrum
(Fig. 1A). The axon of DBNi1-2 is 16–20 µm in diameter and
descends dorsally in the ipsilateral connective. The axon gives
rise to a small region of branches in the maxillar segment of
the suboesophageal ganglion (Fig. 1B) before extending at
least as far as the mesothoracic ganglion (one successful
staining). The branching pattern of DBNi1-2 in the thoracic
ganglia is not known.
Stimulation of N1 (scape)
fl1
Stimulation of N2B
pd
*
sc
20 mV
3 ms
Physiology of DBNi1-2
Antennal mechanosensory inputs to DBNi1-2
Intracellular recordings were made from the deutocerebral
dendrite of DBNi1-2 in all experiments. They revealed
summed excitatory postsynaptic potentials (EPSPs) in
response to imposed deflections of the ipsilateral scape–pedicel
joint (Fig. 2A). Deflections of the contralateral joint had no
effect on the activity of the interneurons. In all specimens,
EPSPs were reliably elicited by each deflection and could reach
amplitudes of up to 40 mV. Spiking responses consisted of
Descending brain interneurones in crickets 2269
Responses of DBNi1-2 to electrical stimulation of antennal
sensory nerves
Three pairs of stimulating electrodes were placed under
different antennal nerves to identify the origin of the
postsynaptic potentials following antennal stimulation (for
nerve terminology, see Honegger et al., 1990). First, one pair
of electrodes was attached to both branches of nerve 1 (N1) in
the third/fourth flagellar segment to stimulate flagellar
afferents. Second, the afferents of the scapal chordotonal organ
and a scapal hair plate in nerve 2B (N2B; H.-W. Honegger,
unpublished data) were stimulated. Third, hook electrodes
under both branches of N1 in the distal scape allowed
pedicellar and flagellar afferents to be stimulated. One
experiment on DBNi1-2 (Fig. 2D) clearly demonstrates that
two sources of antennal sensory input to DBNi1-2 existed.
Stimulation of flagellar N1 elicited EPSPs with an amplitude
of approximately 23–26 mV in DBNi1-2 with a latency of
7 ms, whereas stimulation of the scapal N1 evoked EPSPs with
an amplitude of approximately 30 mV and a latency of 2 ms.
Each of the latter EPSPs gave rise reliably to one spike (arrow
in Fig. 2D). Stimulation of N2B had no effect on DBNi1-2.
The mechanoreceptive organ most effectively exciting DBNi12 was, therefore, located in the pedicel, with inputs from the
flagellum being weaker and possibly polysynaptic.
Visual inputs to DBNi1-2
Of the five interneurons investigated, only DBNi1-2 was
activated by visual stimulation of the ipsilateral compound eye.
There is no evidence for inputs from the ocelli and the
contralateral compound eye. All visual responses of DBNi1-2
consisted either of spikes and EPSPs smaller than the EPSPs
A
Computer
monitor
White
Black
10 mV
DBNi1-2
0.2 s
B
Spike count (%)
phasic bursts and followed the onsets of deflections with a
latency of 7.7–8.8 ms.
One variable influencing the strength of spiking responses
was the angular velocity of antennal deflections, which was
tested in the range 30–900 ° s−1. Deflections with velocities of
30 ° s−1 were already above threshold for the generation of
EPSPs. In five experiments, spiking responses increased at
approximately 2 spikes 100 ° s−1 between 90 and 300 ° s−1 and
decreased above 300 ° s−1 (Fig. 2B). A second variable
influencing spike production was the antennal position before
a single deflection step. The range of antennal positions tested
was 0 ° (antenna in the forward-pointing position) to 80 °
lateral. DBNi1-2 responded best to deflections of the antenna
at angles between 40 and 60 °. This is slightly lateral to the
antennal resting position of approximately 30 ° (Fig. 2C; twotailed Friedman test, P=0.018, N=7). At a given angle,
however, the response of DBNi1-2 did not depend on the
direction of movement (arrowheads in Fig. 2C); adductions
and abductions were equally efficient (two-tailed Wilcoxon
test, P=0.12, N=7).
The spike conduction velocity of DBNi1-2 was 4.4 m s−1 as
measured by intracellular recordings close to the axon origin
combined with extracellular recordings from the ipsilateral
neck connective.
100
Dorsal
50
0
Anterior
Fig. 3. (A,B) Response of DBNi1-2 to visual stimuli. (A) Light-off
stimuli elicited bursts of spikes. Upper trace, stimulus monitor; lower
trace, five superimposed sweeps of the intracellular recording.
(B) Mapping of responsiveness to visual input. Sensitivity to the
presentation of stationary black dots subtending a visual angle of 8 °
changes over the receptive field of DBNi1-2. Columns represent
relative means of the spike counts (± S.E.M., standardised for each
experiment, N=5). DBNi1-2 responded best to dots in the dorsoanterior corner of the computer screen. Note that the the size of the
screen did not allow the full size of the receptive field of this neuron
to be probed (see Materials and methods).
evoked by antennal mechanosensory stimuli or of spikes alone
(see Discussion). Severance of the ipsilateral optic stalk
between the medulla and lobula abolished all visual responses
in DBNi1-2. Toggling a computer monitor between black and
white elicited bursts of spikes (Fig. 3A). In general, ‘Light-off’
responses were more effective in triggering spikes than ‘Lighton’ responses (N=4 crickets, two-tailed Wilcoxon test,
P=0.033). In addition, small moving, high-contrast stimuli
such as a black dot (subtending a visual angle of 8 °) moving
on a white background and looming black disks on a white
background increasing at 7 ° s−1 were effective in triggering
spikes. The visual responses of DBNi1-2 were subject to fast
habituation in all experiments. To reveal the spatial
organisation of the visual input to DBNi1-2, stationary black
dots were presented for 400 ms on a white background in the
centre and at the corners of the computer screen, which was
centred at the eye. The strongest spike responses per dot
displayed occurred when dots were presented at the outer
corner of the dorso-anterior quadrant of the computer screen,
2270 M. GEBHARDT AND H.-W. HONEGGER
i.e. approximately 37 ° dorso-anterior of the centre of the eye
(see Materials and methods for more details). Minimum
responses were elicited by dots in the centre of the screen
(Friedman test, P=0.031, Fig. 3B).
Antennal motor-activity-dependent modulation of synaptic
activity to DBNi1-2
DBNi1-2 clearly received strong excitation from afferents of
the second antennal joint between the scape and pedicel. How
does DBNi1-2 respond to active antennal movements that are
likely to excite these afferents ? In a tethered cricket walking
on a stationary ball (Kammerer and Honegger, 1988), bursts of
motoneuron spikes were recorded extracellularly from a pure
antennal motor nerve (N4B; Honegger et al., 1990; Fig. 4A)
that drove antennal movements with large amplitudes and
velocities. Additional short bursts of motor
activity were closely coupled to the respiratory
rhythm and did not result in visible antennal
movements. There was a clear negative
N4B
correlation between motor activity and synaptic
activity in DBNi1-2. Postsynaptic potentials had
amplitudes of less than than 5 mV during episodes
of longer-lasting motor activity and during some
of the bursts related to respiration. EPSPs with an
DBNi1-2
amplitude of 20 mV and spikes occurred during
intervals between motor activity. This decrease in
the amplitude of postsynaptic potentials during
motor activity also occurred during antennal
stimulation (Fig. 4B). Deflections of the
A
*
*
*
*
*
40 mV
3s
B
20°
Antennal
deflection
N4B
0.5 mV
DBNi1-2
10 mV
0.5 s
1.0
92
C
9
0.8
Normalised integral
Fig. 4. (A–C) Synaptic activity of DBNi1-2 during
motor activity. (A) Intracellular recording of DBNi1-2
(lower trace, hyperpolarised with −2 nA) and
extracellular recording of antennal motoneurons from
N4B (upper trace) as a measure of antennal motor
activity. Movements of the antenna were not
registered. Large excitatory synaptic potentials
(arrows) and action potentials (open arrows) are absent
during a spontaneous motor neuron burst (arrowhead)
and during respiratory-related bursts (asterisks).
(B) During forced antennal movements, excitatory
postsynaptic potential (EPSP) frequency was also
reduced in the presence of high levels of antennal
motor activity. Solid bars represent episodes of low
synaptic activity in DBNi1-2 and the dashed bar
represents episodes of high activity. (C) Box-andwhisker plot showing the median, the second and third
quartiles and the fifth and ninety-fifth percentiles of
normalised integrals of 176 spontaneous EPSPs plotted
against normalised motor spike count in motor nerve
N4B from four crickets (see Materials and methods).
Large synaptic potentials did not occur in the presence
of high motor spike counts. The integral values were
binned into classes with a width of 0.1 relative motor
spike count units. The maximum integral values
decrease with increasing spike count (Spearman rank
correlation coefficient r=−0.85, P<0.001). Numbers
indicate numbers of samples in each class.
scape–pedicel joint elicited EPSPs in DBNi1-2 and sometimes
also produced bursts in N4B, probably reflecting resistance
reflexes. During motoneuron bursts, the amplitudes of EPSPs
and the frequency of small-amplitude postsynaptic potentials
were clearly reduced compared with stimuli without
concurrent motor activity (broken bar in Fig. 4B).
To quantify the relationship between synaptic potential
amplitude and motor activity, Spearman rank correlation
analyses of DBNi1-2 membrane potential integrals (see
Materials and methods) and antennal motoneuron spike counts
were carried out in five experiments (Table 1). The correlation
coefficient (r) ranged from −0.57 to −0.69 (experiments 1–4 in
Table 1), indicating that the amplitudes of EPSPs in DBNi1-2
decreased with increasing motor activity. The motor spike
count was the only variable found to be correlated with the size
7
0.6
7
5
10
12
0.4
0.2
13
17
0.9
1.0
4
0.1
0.2
0.3 0.4 0.5 0.6 0.7 0.8
Normalised motor spike count
Descending brain interneurones in crickets 2271
Table 1. Summary of the experiments analysed for the motor-activity-dependent suppression of synaptic inputs to DBNi1-2
Experiment
Number of intervals analysed
Spearman correlation coefficient, r
Probability of error
Antennal sensory–motor loop
1
2
3
4
5
37
−0.57
<0.001
Closed
60
−0.69
<0.001
Closed
35
−0.62
<0.001
Closed
55
−0.67
<0.001
Closed
63
−0.58
<0.001
Open
of the integrals. The resting potential immediately before the
onset of EPSPs was not correlated with the size of the integrals.
The Spearman rank correlation coefficient for the pooled
data from experiments 1–4 in Table 1 is −0.64 (P<0.001,
N=176). During periods of low antennal motor activity, both
large and small synaptic inputs to DBNi1-2 were measured,
resulting in considerable variance in the data shown in Fig. 4C.
However, the gradual decline in synaptic inputs is clearly
revealed when the data are grouped into classes. The maximum
integral values decline gradually with increasing motor spike
count (Spearman r=−0.85, P<0.001).
These experiments were performed under closed loopconditions with all antennal nerves intact. In one experiment,
all the nerves that contain antennal motoneurons (N2, N3, N4)
were transected (Table 1, experiment 5), rendering the treated
antenna completely motionless and thereby preventing
peripheral sensory feedback. This open-loop condition still
results in a negative correlation coefficient for the relationship
between motoneuron activity and synaptic inputs to DBNi1-2
(r=−0.58), indicating a central origin for the motor-activitydependent modulation of synaptic inputs to DBNi1-2.
The antennal motor activity did not seem to have an effect
on visually elicited activity. One experiment showed that the
strength of spiking responses to ‘Light-on’ and ‘Light-off’
stimuli during antennal motor activity did not differ from
the strength of responses during its absence (N=16;
Mann–Whitney U-test, P=0.45 and P=0.47, respectively).
the ipsilateral scape–pedicel joint with compound EPSPs and
spikes (Fig. 5C) in the angular range 0–100 ° at angular
velocities of 30–900 ° s−1. Adductions were significantly more
effective than were abductions in stimulating DBNc1-2/c2-2
(Fig. 5D). Electrical stimulation of N2B, which contains the
axons of the chordotonal organ in the scape and of two scapal
hairplates (H.-W. Honegger, unpublished data), elicited spikes
at a mean latency of 2.5 ms (Fig. 6A). In two experiments on
DBNc1-2/c2-2, no indications were found that the synaptic
activity was suppressed by antennal motor activity, as in
DBNi1-2.
Two DBNc2-3 interneurons resembled DBNi1-2 and
DBNc1-2/c2-2 in that forced deflections of the ipsilateral
scape–pedicel joint resulted in compound EPSPs and bursts of
spikes in one specimen (Fig. 5E) and EPSPs alone in another
specimen (not shown). The spiking response was best at lateral
positions between 80 and 100 ° for abductions; the amplitudes
of EPSPs in the second specimen were independent of angular
position and of the direction of the ramps. One experiment
identical to that shown in Fig. 2D indicated that
mechanosensory afferents located in the pedicel must excite
DBNc2-3 (Fig. 6B).
None of the four interneurons was activated by other
olfactory, acoustic or mechanical stimuli to parts of the body
other than the antennae, as tested under the conditions of our
experiments.
Physiology of DBNi2-1, DBNc1-2/c2-2 and DBNc2-3
Recording from DBNi2-1 was more difficult than recording
from DBNi1-2, probably because of the dorsal position of the
deutocerebral dendrite. The recordings from DBNi2-1 yielded
only spiking responses and no large compound EPSPs upon
forced deflections of the ipsilateral scape–pedicel joint
(Fig. 5A). One specimen responded preferentially to adductions
between 80 and 67 ° with a phasic–tonic response of an average
of 23 spikes per ramp (Fig. 5B, one experiment, N=11 stimulus
periods, 90 ° s−1). A second DBNi2-1 spiked more phasically in
response to comparable stimuli; this specimen responded to
abductions in an angular range between 23 and 90 ° (data not
shown). This indicates that a single interneuron may respond
differently to identical stimuli in different animals. Experiments
on the origin of the antennal mechanosensory input to DBNi21 and on antennal motor-activity-dependent suppression of its
synaptic activity were not performed.
Recordings from DBNc1-2/c2-2 interneurons were made in
14 animals. They responded to step-like forced deflections of
Discussion
We show that, in the cricket, large identified descending
brain interneurons compute specific antennal mechanosensory
information and convey it posteriorly. Additional visual inputs
converge onto one of the five interneurons. In crickets, only
the tritocerebral commissure giant has been shown to receive
antennal mechanosensory input (TCG; Bacon and Tyrer, 1978;
Bacon, 1980). In the locust, the descending movement detector
(DCMD) neuron receives inputs from the antenna, and it has
been been suggested that these contribute to the periodic nonresponsiveness of the DCMD (Rowell and O’Shea, 1980).
Antennal mechanosensory inputs
All interneurons responded reliably to forced deflections of
the second antennal joint, which allows horizontal movements
of the antennae. In this study, only forced deflections were
used, although we are currently investigating the response
properties of the neurons during voluntary antennal
movements. Electrical stimulation of antennal sensory nerves
2272 M. GEBHARDT AND H.-W. HONEGGER
B
A
DBNi2-1
DBNi2-1
25
12.5°
*
20 mV
10
5
0
80–67
67–54
54–41
41–28
28–15
15–2
DBNi2-1
15
2s
0–13
13–26
26–39
39–52
52–65
65–78
Antennal
deflection
Spikes per ramp
20
Angular position (degrees)
C
D
DBNc1-2/c2-2
DBNc1-2/
c2-2
20 mV
1s
E
DBNc2-3
Antennal
deflection
0.8
0.6
0.4
0.2
0
Abduction
20°
1.0
Adduction
Antennal
deflection
Spikes per ramp, normalised
DBNc1-2/c2-2
Fig. 5. (A–E) Responses of DBNi2-1 (A,B), DBNc1-2/c2-2 (C,D)
and DBNc2-3 (E) to forced deflections of the ipsilateral
scape–pedicel joint. (A) Responses of one DBNi2-1 consisted of
spikes. This DBNi2-1 responded best to adductions between 80 and
67 ° with an average of 23 spikes per ramp. The asterisk marks a
spike triggered by a small extra ramp at the medial turning point of
the deflection. (B) Average activity over 11 stimulus periods at
10 mV
90 ° s−1 for the same interneuron. (C) Recordings from DBNc12/c2-2
yielded compound excitatory postsynaptic potentials
DBNc2-3
(EPSPs) and spikes. (D) DBNc1-2/c2-2 was more responsive to
adductions than to abductions. Columns represent normalised mean
50 ms
spike counts per ramp (± S.E.M.) of all ramps during adduction
versus abduction in five animals (N=23 stimulus periods at 90 ° s−1; Wilcoxon test P=0.03). (E) Compound EPSPs and bursts of spikes were
triggered in one DBNc2-3 by abductions between 80 and 100 ° at 300 ° s−1 (five sweeps superimposed). Other angular positions were less
effective in stimulating this example of DBNc2-3.
20°
demonstrated that DBNi1-2 and DBNc2-3 were excited by
afferents from the pedicel, whereas DBNc1-2/c2-2 were
excited by afferents from the scape. This is consistent with
morphological data showing that DBNi1-2 and DBNc2-3 have
their input dendrites close to each other in the ventral
deutocerebrum, which receives projections of flagellar
afferents (vfa; Staudacher and Schildberger, 1999).
Stimulation of flagellar afferents evoked only long-latency and
small-amplitude responses in DBNi1-2, indicating several
layers of intercalated interneurons. In comparison, the latencies
of the EPSPs following electrical stimulation of N1 in the distal
scape for DBNi1-2 and DBNc2-3 ranged from 1.0 to 2.0 ms
(EPSPs) and from 1.9 to 3.6 ms (spikes), suggesting that only
a few synaptic layers exist between the afferents and the
interneurons. The deutocerebral dendrites of DBNc1-2/c2-2
branch more dorsally than those of DBNi1-2 and DBNc2-3 and
in an area where the proprioceptors of the antennal base
terminate (Bräunig et al., 1983; Honegger et al., 1990;
Descending brain interneurones in crickets 2273
Staudacher and Schildberger, 1999). It is likely that afferents
(Rowell, 1971). Both interneurons respond to novel stimuli,
of the scapal chordotonal organ excite DBNc1-2/c2-2. A
such as small, erratically moving, high-contrast objects. These
contribution from other scapal mechanosensory afferents,
stimuli cause fast habituation in the DCMD (Rowell, 1971) and
however, cannot be excluded because N2B contains the axons
of DBNi1-2. Recent results demonstrate that the DCMD
of receptors in the scapal bristles. The origin of the
functions as a detector of approaching objects (Rind and
mechanoreceptive input to DBNi2-1 remains unknown.
Simmons, 1992; Hatsopoulos et al., 1995; Gabbiani et al.,
Staudacher (Staudacher, 1998) has described seven
1999; Rind and Simmons, 1999). Since looming discs with a
descending interneurons with dendritic arborizations in the
linear rate of increase of 7 ° s−1 in radius were used in the
mechanosensory area of the deutocerebrum. We have recorded
present study, it is not known whether DBNi1-2 might
from five of the seven interneurons, which seem to represent
similarly work as an ‘approach detector’.
specific lines each coding for a set of variables of antennal
Our results showed that DBNi1-2 was not evenly responsive
movement and/or position. While DBNc1-2/c2-2 appears to
to stimuli throughout its visual receptive field, although only
code preferentially for movement direction, DBNi2-1 and
a small area of the total visual field was probed. Our
DBNc2-3 code for extreme antennal positions. Interneuron
experimental arrangement did not allow us to investigate the
DBNi1-2 is special in representing movements at more medial
limits of the receptive field. The spatial response pattern of
antennal positions. It also appears to be the only one of the
DBNi1-2 is likely to derive from a retinotopic source, as found,
descending interneurons to show motor-activitydependent suppression and to receive visual
A
input. The remaining two interneurons, whose
DBNc1-2/c2-2
physiologies are so far unknown, may complement
this information and support a finer resolution of the
whole angular range of the scape–pedicel joint.
6V
Stimulation of N2B
Although only a few recordings have been made 4 V
from the interneurons DBNi2-1 and DBNc2-3, it is
apparent that their response properties can differ
between animals. Thus, the activity of the
interneurons may be altered by modulatory effects
30 mV
as has been shown, for instance, for the direction3 ms
specific antennal response in honeybees, which is
modulated by octopamine and serotonin in an
antagonistic way, probably via the underlying
visual interneurons (Erber and Kloppenburg, 1995;
B
Kloppenburg and Erber, 1995). Morphologically
DBNc2-3
Stimulation of N1 (flagellum)
identical ‘twin’ interneurons with different response
properties might also explain this interindividual
variability. Such interneurons, however, were not
Stimulation of N1 (scape)
reported by Staudacher (Staudacher, 1998).
DBNi1-2: visual responses
The fact that DBNi1-2 is the only one of the five
antennal mechanosensory interneurons to receive
visual input coincides with its morphology. It is the
only one of the five interneurons with a dendritic
arborization in the lateral protocerebrum. In contrast
to the antennal mechanosensory responses, in
addition to spikes, only small synaptic potentials
could be recorded from DBNi1-2 during visual
stimulation. This probably reflects a long
electrotonic conduction time between the site of
the visual inputs and the recording site, leading
to attenuation of EPSPs. The geometric distance
between the electrode and the protocerebral
dendrite, the putative site of visual inputs
(arrowhead in Fig. 1A), was approximately 300 µm.
The basic properties of the visual responses of
DBNi1-2 resemble those of the locust DCMD
Stimulation of N2B
30 mV
3 ms
Fig. 6. (A,B) Electrical stimulation of afferent antennal nerves during
intracellular recordings from DBNc1-2/c2-2 (A) and DBNc2-3 (B).
(A) Stimulation of N2B (carrying the axons from the scapal chordotonal organ)
elicited spikes in DBNc1-2/c2-2 at latencies of approximately 2.5 ms. Increasing
the stimulus strength from 4 to 6 V resulted in an increase in spike count per
stimulus and better synchronisation of the first spike. (B) DBNc2-3 received
strongest inputs (spikes, marked by an arrow, and excitatory postsynaptic
potentials) upon electrical stimulation of N1 in the distal scape, suggesting input
from pedicellar proprioceptors. Stimulation of N1 in the third/fourth flagellar
segment and of N2B were not effective.
2274 M. GEBHARDT AND H.-W. HONEGGER
for instance, in the fly male-specific visual neurons (Strausfeld,
1991; Gilbert and Strausfeld, 1991).
DBNi2-1: antennal motor-activity-dependent modulation of
synaptic activity
During episodes of active antennal movements, DBNi1-2
shows a suppression of its antennal mechanosensory
synaptic activity (Fig. 4). This suppression does not depend
on the presence of sensory feedback and, as our results
indicate, may thus be generated centrally. The strength of
this suppression gradually increases as the strength of the
motor activity increases, i.e. large EPSPs are absent during
strong antennal motor activity. Although the graded
relationship is masked by small EPSPs occurring either
spontaneously or during weak antennal motor activity, the
decline is visible in the trend of the upper 95 % quartile
values in Fig. 4C. There are several potential mechanisms
that would result in a reduction in the amplitude of the
synaptic potentials in DBNi1-2. Hyperpolarising inhibitory
synaptic potentials could superimpose on depolarising
synaptic potentials, thus reducing the amplitude of the
latter. This mechanism can probably be excluded since
hyperpolarising potentials were never observed in DBNi1-2
and the amplitudes of EPSPs were independent of the
membrane potential before the EPSPs. Conductance changes
in the dendritic membrane of DBNi1-2 could contribute to
the reduction in EPSP amplitudes by shunting the membrane.
Currently, no experimental evidence is available to support
or reject this possibility. The terminals of neurons
presynaptic to DBNi1-2 could have been the target of
presynaptic inhibition, as demonstrated for the sensory
terminals of, for example, locust leg afferents (Burrows and
Laurent, 1993; Burrows and Matheson, 1994) or cercal hair
afferents (Boyan, 1988). Only the antennal mechanosensory
input, not the visual input, was suppressed. This suggests
that this suppression occurred in neurons presynaptic to the
deutocerebral dendrite of DBNi1-2.
Motor-activity-dependent
modulation
of
sensory
information has been observed in several systems (e.g.
Zaretsky and Rowell, 1979; Bell, 1981; Bell, 1982; Camhi and
Nolen, 1981; Guthrie, et al., 1983; Paul, 1989; Robert and
Rowell, 1992; Hjelmstad et al., 1996; Wolf and Burrows,
1995) and is generally considered to aid the central nervous
discrimination of self-induced and external sensory feedback.
Two reports (von Holst and Mittelstaedt, 1950; Sperry, 1950)
independently proposed a central nervous copy of a motor
command (‘efference copy’, von Holst and Mittelstaedt, 1950;
‘corollary discharge’, Sperry, 1950) to counterbalance selfinduced sensory feedback. If such a mechanism were effective
in DBNi1-2, external stimuli to the antenna should be
represented by the interneuron irrespective of motor-activitydependent suppression. It is not yet known, however, whether
the responsiveness to external antennal mechanosensory
stimuli is affected by motor-activity-dependent suppression.
Experiments are currently being carried out to address this
question.
Functional considerations
What conclusions concerning the behavioural function of the
descending interneuron system emerge from our results? First,
the high spike conduction velocity of DBNi1-2 is comparable
with velocities found in fibres of similar calibre, e.g. the locust
giant interneurons (Boyan and Ball, 1989). This suggests that
speed is an important variable, at least for DBNi1-2. A spike
initiated in the brain and travelling at 4 m s−1 would reach the
thoracic ganglia within 2 ms in an adult cricket. Second, all five
antennal descending interneurons seem to code for a portion of
the antennal space. DBNi1-2 appears to act as a directionindependent, but position-sensitive, detector of deflections of
the antenna slightly lateral to its resting position of 30 °. We are
currently investigating whether the maximum spatial sensitivity
of the antennal mechanosensory response may match that of the
visual response.
It is known that antennal signals are necessary for obstacle
avoidance during locomotion in the potato-beetle (Pelletier and
McLeod, 1994). Furthermore, mechanical stimulation of a
cockroach antenna can trigger escape turns (Burdohan and
Comer, 1990; Stierle et al., 1994; Burdohan and Comer, 1996;
Ye and Comer, 1996). In our experiments, motor actions were
never elicited by injections of depolarising currents into
DBNi1-2. It is likely that the descending antennal interneurons
participate in the control of the fast motor programmes of the
legs, such as obstacle-induced correctional turns during fast
walking, escape movements or flight, by priming thoracic
motor networks for subsequent activity in response to an
aversive stimulus.
In crickets, the activity of several descending neurons
correlates with the rotational or the translational velocity of
walking (Böhm and Schildberger, 1992; Staudacher and
Schildberger, 1998); one interneuron even proved to be
sufficient and necessary for the maintenance of walking (Böhm
and Schildberger, 1992). None of the interneurons investigated
in the present study represents such a type. Experiments are
currently being carried out to test whether DBNi1-2 is
activated during free walking or during encounters with
obstacles, conspecifics or predators.
We thank P. Bräunig, Aachen, and S. Ott, Cambridge, for
continuous and fruitful discussions about the descending
interneurons. M. Burrows and T. Matheson, Cambridge, made
valuable comments on an earlier version of the manuscript.
Two anonymous referees helped to improve this article.
This research was supported by the Deutsche
Forschungsgemeinschaft (Ho 463/20-2) and by Vanderbilt
University. M.G. was supported by a grant from the
‘Studienstiftung des Deutschen Volkes’.
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