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AMER. ZOOL., 30:609-627 (1990)
Nerve Cells and Insect Behavior—Studies on Crickets1
FRANZ HUBER
Max-Planck-Institute fur Verhaltensphysiologie, D 8130 Seewiesen,
Federal Republic of Germany
SYNOPSIS. Intraspecific acoustic communication during pair formation in crickets provides excellent material for neuroethological research. It permits analysis of a distinct
behavior at its neuronal level. This top-down approach considers first the behavior in
quantitative terms, then searches for its computational rules (algorithms), and finally for
neuronal implementations.
The research described involves high resolution behavioral measurements, extra- and
intracellular recordings, and marking and photoinactivation of single nerve cells. The
research focuses on sound production in male and phonotactic behavior in female crickets
and its underlying neuronal basis. Segmental and plurisegmental organization within the
nervous system are examined as well as the validity of the single identified neuron approach.
Neuroethological concepts such as central pattern generation, feedback control, command
neuron, and in particular, cellular correlates for sign stimuli used in conspecific song
recognition and sound source localization are discussed. Crickets are ideal insects for
analyzing behavioral plasticity and the contributing nerve cells. This research continues
and extends the pioneering studies of the late Kenneth David Roeder on nerve cells and
insect behavior by developing new techniques in behavioral and single cell analysis.
INTRODUCTION
This report on nerve cells and insect
behavior is dedicated to the memory of the
late Kenneth D. Roeder, a founding father
of neuroethology, the field of interdisciplinary research which aims to bridge the
gap between behavioral strategies and the
underlying neural substrates and mechanisms.
Zoologists have the opportunity to select
among the manifold behaviors formed by
evolution, and to choose those where they
think an answer is within reach when
applying current technological know-how.
Their approach is a comparative one and
should be evolution-oriented. Zoologists
are interested in individual, population and
species solutions, in common principles as
well as in differences. One should never
forget that a cricket differs from a frog,
and a crayfish differs from a bird in its
demands.
Neuroethologists working comparatively have to consider two equally important sets of questions which were formulated by T. H. Bullock (1984) (Table 1).
1
From the Symposium on Science as a Way of Knowing—Neurobiology and Behavior organized by Edward
S. Hodgson and presented at the Centennial Meeting
of the American Society of Zoologists, 27-30 December 1989, at Boston, Massachusetts.
THE KIND OF APPROACH IN
NEUROETHOLOGY
Neuroethology as the study of the neural
basis of behavior favors what I call the topdown approach: a distinct behavioral strategy has to be observed and analyzed first
in the field under environmental constraints, then quantitatively studied in the
laboratory, and finally explored at its neuronal and, if possible, molecular levels. This
top-down approach is chosen because we
strongly believe that it is the behavior,
shaped and adapted by nature's abiotic and
biotic forces, which leads us to pose the
right questions to the nervous system. Thus,
neuroethologists should become familiar
with the concepts, methods, and data the
study of behavior has to offer, as well as
with the whole scenario of modern neurosciences, including approaches at the system, cellular and molecular levels (Huber,
1988, 1989).
ACOUSTIC COMMUNICATION IN CRICKETS:
A FAVORABLE STRATEGY
Orthopteran and homopteran insects
were among the first within the animal
kingdom to have evolved hearing and
sound production for intraspecific and
interspecific interactions. For pair formation and reproduction, the main topics
here, the information encoded in the send-
609
610
FRANZ HUBER
TABLE 1. Aims of comparative and evolution-orientedbe considered
veuroethology.
the subsequent
as a releasing stimulus for
one (for literature see Loher
1. What are the neural correlates and causal rela- and Dambach, 1989).
tionships to known behaviors and behavioral dif2. How to improve effective calling
ferences among animals?
and sound radiation
2. What are the behavioral correlates and causal relationships to known neural differences among anMole crickets have developed tactics to
imals?
make calling songs more efficient. They
(Statements made by T. H. Bullock, 1984.)
produce them in a burrow which they modify to an exponential horn which amplifies
sounds of the correct carrier frequency.
er's acoustic signals must be decoded by Flying conspecifics hear such signals already
the receiver. The nervous system of the at distances of several hundred meters
sender (usually the male) generates sound which guide their orientation (for literasignals which are species-specific in their ture see Bennet-Clark, 1989).
frequency spectra and their temporal orgaMale tree crickets (Oecanthus burmeisteri)
nization (Fig. 1) (for literature see Bennet- improve sound intensity and radiation by
Clark, 1989). The nervous system of the a baffle. They cut a hole into a leaf, into
receiver (usually the female) has to fulfill which they place themselves and sing (Protwo equally important tasks: it must be able zesky-Schulze et al., 1975).
to discriminate conspecific songs from
abiotic and biotic noises in order to rec- 3. Satellite behaviors
ognize them (song-recognition), and it must
In Gryllus integer only some males call
localize the sender's position in space (song- and attract female crickets (also females of
localization) (for literature see Schildber- the parasitoid flies, Euphasioptery ohracea
ger et al., 1989).
[Cade, 1975]), whereas other males are
In insects, these distinct sender-receiver silent, surround the caller and are named
interactions have evolved during the course satellites. If on her way to the singing male
of phylogeny; they are formed during the female meets a satellite male, he is able
ontogeny and based mainly on genetically to court and to mate with her (Cade, 1980).
fixed patterns of behavior. In my report I The physiological conditions responsible
will concentrate on crickets and consider for calling or noncalling are still unknown.
Advantages and disadvantages for callers
the topics listed in Table 2.
and noncallers have been discussed, but will
SOME BEHAVIORAL STRATEGIES IN
not be mentioned here.
CRICKETS
Although crickets are best known and
famous for their songs and acoustically
mediated behavior, they have evolved other
strategies which should interest us because
they point to multisensory and multimodal
conditions demonstrating that the cricket's
world is not solely acoustic (Huber, 1988,
1989). Here are a few examples.
1. Behaviors involved in pair formation,
reproduction and aggression
During the reproductive season adult
male and female crickets display sequences
of distinct behavioral patterns which serve
pair formation and mating as well as individual spacing, aggression and territorial
defence. Each single behavioral event can
4. Prey-predator strategies
Many cricket species are nocturnally
active. Sound traps broadcasting the conspecific song attract flying males and
females from far away (Ulagaraj and
Walker, 1973; Walker, 1982). During their
nocturnal flights these animals can be
preyed upon by echolocating and hunting
bats. Teleogryllus has evolved avoidance
strategies (Moiseff et al., 1978). The animals hear ultrasonic sounds and process
them in distinct neurons (Moiseffand Hoy,
1983) which control their turning away
from the sound source (for literature see
Pollack and Hoy, 1989).
Acheta domestica in southern France is
known as prey for a parasitic digger wasp
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NERVE CELLS AND INSECT BEHAVIOR
Calling songs
Frequency spectra
IHHtlHH*
Gryllus campestns
2
4
6
8
1 0 1 2
4
6
8
10
12
14 k H z
1
6
6
10
12
14 kHz
1 4 1 6
kHz 2 0
Teleogryllvs oceanicus
Melanogryftus desertus
Oecanthus pellucens
2
2
4
FIG. 1. Calling song patterns and frequency spectra in different species of crickets (modified from Huber,
1990).
of the genus Liris. The flying wasp patrols
the cricket area then lands and approaches
a cricket on foot. In the case of no escape,
the wasp stings and paralyzes the cricket.
The prey is then carried as food to the
wasp's nest. But crickets have developed a
warning system, consisting of an arrangement of filiform hair sensilla on their cerci.
A flying and fast walking wasp creates air
currents strong enough to stimulate the
filiform hair sensilla and to elicit activity
which is then transmitted to different
ascending interneurons within the ventral
nerve cord. Their activity controls quick
defensive and escape responses, such as
head stand, kicking with the hindlegs, and
running away (Gnatzy and Heusslein, 1986;
for literature see Gnatzy and Hustert,
1989).
5. Combined visual and acoustical
cues for orientation
Many crickets have well developed compound eyes and ocelli. Some Nemobius
species use dark contours as landmarks to
find their home territories. If they are prevented from seeing these landmarks,
celestical cues suffice for orientation (for
literature see Honegger and Campan,
1989).
By using a closed loop walking compensator (Fig. 2), which allows the unrestrained animal to chose direction and
speed of walking on the surface of a tread-
mill while being kept in place by the counterrotating treadmill, we recently found
that female Acheta domestica track optical
targets such as black squares (Atkins et al.,
1987). When given a choice between a black
square and a conspecific calling song (Fig.
3), the female previously tracking a visual
target switches to track the calling song,
but only if its temporal pattern lies within
the attractive range (Stout et al, 1987).
During orientation to the sound source she
performs a zig-zag walking course which is
characteristic for phonotaxis and expressed
as a pattern of several steps interrupted by
short pauses. During orientation to the
visual target she lacks that kind of walking
mode (Weber et al, 1987). Thus, there
seems to be a different interfacing between
the visual and the acoustical recognition
system and the walking generator. The shift
in walking modes indicates the change in
the cricket's attention and in the modality
being processed.
TABLE 2. TOPICS.
A.
B.
C.
D.
E.
Some behavioral strategies in crickets.
The cricket's nervous system.
Behavioral analysis of song recognition.
Cellular correlates for song recognition.
Behavioral and neuronal aspects of song localization.
F. Song orientation in one-eared crickets.
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FRANZ HUBER
IR-Camera
B
o c n°-.Walking
direction (°)
—- L1
180°-
n°30
60
90
120
Time (s)
— L2
e-vector detection, receptors sensitive to
blue light are required arranged in the dorsal rim area of the compound eyes. Orientation to e-vector apparently works
already at illuminations as low as moon light
(Labhart, 1988; Labhart et ai, 1984; Weber
et ai, unpublished results).
6. Hormones and phonotactic behavior
Hormonal effects have long been
neglected in cricket acoustic behavior.
Quite recently it was reported that adult
female Acheta domestica lose phonotaxis and
mating after removal of the corpora allata,
i.e., glands that produce the juvenile hormone (JH). Both behaviors are restored
after reimplantation of the glands or after
application of JH (Stout et al., 1976; Koudele et al., 1987). However, subsequent
work with female Gryllus bimaculatus
showed that allatectomy in the last larval
instar did not abolish phonotaxis in the
adult (Fig. 5), although no JH was present
in the hemolymph (Loher et al., unpublished results).
7. Aggression and phonotaxis
Male crickets perform phonotaxis (Fig.
6A) (Weber, 1989; Weber and Hissmann,
unpublished results). This strategy allows
FIG. 2. Design and analysis for studying cricket unsuccessful calling males in the field to
phonotaxis on the treadmill under closed-loop conditions. A. Experimental arrangement with the tread- leave their burrows and search for females
mill (center), the infrared sensing and detecting device in the neighbourhood of other calling
(IR camera), the electronics to control treadmill males. Moreover, males of many cricket
movements (Comp. Electr.), and the broadcast of species are famous for their fights (Alexmodel calling song (L, Comput.). B. Section of a tracking record of a female to loudspeaker 1 (LI) with a ander, 1961). To our surprise we found
switch to loudspeaker 2 (L2). Note the zig-zag course that a male which had won a fight displayed
during tracking. C. x, y plots of tracking to LI or L2 phonotaxis (Fig. 6B), whereas in the loser
respectively. Each trace represents walking for 20 sec. phonotaxis disappeared for several days
(A, B, adapted from Kleindienst, 1987; C, adapted
(Fig. 6C). Thus, aggression and pair forfrom Huber, 1987.)
mation may be linked by a common neuronal and/or hormonal mechanism which
has to be investigated. This finding invites
Recently orientation to polarized light neuropharmacological studies to explore
(e-vector) has been studied in the genus the physiological basis of winners and losGryllus (Fig. 4) (Brunner and Labhart, 1987; ers.
Weber et ai, unpublished results). In comTo sum up: The world of crickets is not
petition with conspecific calling songs, entirely an acoustical world. This should
phonotactic orientation dominates over guide studies concentrating on multisene-vector orientation, and again the walking sory and multimodal information processmode changes when switching from the ing, which is corroborated by the finding
e-vector to the sound source occurs. For that many identified brain neurons encode
613
NERVE CELLS AND INSECT BEHAVIOR
cm/s
1 O
] WlWWrfcrWllWl^^
360°
optical target
1 min
Square
FIG. 3. Visual and acoustical orientation of female Acheta domestica. A. Arrangement of the treadmill with a
horizontal platform leaving an area of ca. 20 cm in diameter of the sphere open (dashed circle) for the cricket's
movement. The pulsed-infrared scanning system is shown above this area. The vertical cylindrical curtain
provides homogenous illumination by a ring lamp on top of the scanning system. The curtain is acoustically
transparent. The direction of acoustical stimulation (L) and the visual target (square) are shown for 90°
separation. B. Tracking an optical target (position indicated by arrow head on the left). C. Tracking a model
calling in the attractive range (60 ms syllable period SP) with a zig-zag course. The upper traces in B and C
show the compensatory sphere velocity, and the different walking modes, i.e., more steps and longer pauses
during tracking the square, and a spiky walking with fewer steps and shorter pauses during tracking the calling
song. The lower traces show the direction of the sphere motion caused by the female's walking. In C the
horizontal line denotes the direction of the loudspeaker (modified from Weber et al., 1987).
multimodal stimuli (Schildberger, 1981,
1984a).
THE CRICKET'S NERVOUS SYSTEM
Crickets became suitable model systems
for neuroethological research not only
because of their clear cut and measurable
acoustic behavior but also because of the
organization of their nervous system which
favors analysis of sound production, pair
formation as expressed by phonotaxis, and
avoidance behavior down to the single neuron level (for literature see Kutsch and
Huber, 1989; Schildberger et al., 1989;
Pollack and Hoy, 1989).
As shown in Figure 7 the nervous system
is divided into discrete ganglia. Moreover,
each ganglion (and even nerve cells) has a
bilateral and a mirror image arrangement
(Huber, 1989). This facilitates studies of
segmental motoneuronal (Bentley, 1969;
Hennig, 1989) and neuromuscular interactions responsible for driving and controlling the forewings during stridulation.
It enabled us to analyse plurisegmental
interactions, especially the influence of the
brain upon the thoracic song generator,
and the effects of wing sensory systems on
adapting wing handedness and tooth impact
(for literature see Kutsch and Huber, 1989).
In this respect one should never forget
that large parts of the body are employed
in a single behavioral act. When a male
cricket calls it not only moves the forewings
periodically, but also suppresses fast walking, lifts the antennae to a position characteristic of calling and raises the body from
the ground. In addition, abdominal ventilation is synchronized with the chirp
rhythm (Huber, 1960; Koch, 1983). These
two rhythmically produced motor patterns
are probably under the control of two sets
of alternatively active plurisegmental nerve
cells which feed information from the subesophageal ganglion down to the respective motor generators (Otto and Campan,
1978; Otto and Weber, 1982; Otto and
Amon, 1986).
Furthermore, cricket song is another case
of a growing number of rhythmic behaviors organized by a central pattern generator (for definition see Selverston, 1980),
which is efficiently controlled by sensory
feedback from the wings (see Kutsch and
FRANZ HUBER
614
homogeneous
light
-i- sound
intact (control)
11,
SO d8
L2. 50 dB
4
90°
B
f=T
1
180° L 1
270°
=fO
L2
polarized light
+ sound
/////////////////?
M/////////////!!'/////////J
//////
lU^'
50 dB
allatectomized
FIG. 5. Phonotaxis of intact female Gryllus bimaculatus (control) and of adult females after allatectomy
in the penultimate larval instar (allatectomized). For
explanation see Figure 4 (courtesy of Loher et al.,
unpublished).
Huber, 1989) and the cerci (see Dambach,
1989).
BEHAVIORAL ANALYSIS OF
SONG RECOGNITION
In the past, my laboratory has concentrated mainly on high-resolution behavioral experiments developed to elucidate
the acoustical constraints of female phonotaxis, a behavior, which expresses both song
recognition and localization of the caller
(for literature see Weber and Thorson,
/////////f/l///!_
lm
1989). That behavior was combined with
///////////////Fiirrp
a search for single nerve cell correlates and
causal relationships (for literature see
////////////////7////777T7
FIG.
4. Relative frequency of tracking angles of
female Gryllus bimaculatus to model calling songs and Schildberger et al, 1989).
homogenous light (A), to model calling songs and
polarized light of different e-vector orientations (B),
and to polarized light of different e-vector orientations alone (C). The position of the sound source is
marked by LI and L2. The experiments were carried
out with changing loudspeaker positions from LI to
L2 (A, B), and by increasing sound intensit) (from 50
to 80 dB SPL). Note that neither homogenous light
nor polarized light at different e-vector orientations
abolished phonotaxis (A, B). In C orientation to polarized light is demonstrated by changing the e-vector
in steps of 45°. 1 m gi\ es a calibration for the tracking
angles (courtesy of Weber et al., unpublished).
NERVE CELLS AND INSECT BEHAVIOR
615
///////////////////////////////////
//////////'(/)itiff/fffffffflfffffiff
////////////////////////////////////
1 m
/ / / / / / / / / / / / /
loser, 20 mm after combat
FIG. 6. Male Gryllus campestris phonotaxis (A) persists in the winner of the combat (B) but is lost in loser
(C). For explanation of the details compare Figures
2 and 3 (A) and Figure 4 (A, B). (Courtesy of Weber,
1989; Weber et al, unpublished.)
1. Phonotaxis in the field and in a
closed-loop arrangement
Crickets perform phonotaxis by means
of walking or flying in the field (Klopffleisch, 1973; Walker, 1982). In order to
evaluate the important calling song parameters for phonotaxis, a closed-loop setup
was developed, as already described (Fig.
2). Using this experimental tool we found
a threshold for phonotaxis to model calling
songs usually around 50 dB SPL. By changing loudspeaker positions the female
changed her orientation often within seconds and she performed a zig-zag course
while tracking the sound source by meandering ca. 40° around the loudspeaker
direction (Wendler et al., 1980; Weber et
al., 1981). This phenomenon will be treated
later.
2. Carrier frequency and walking angle
Calling songs of the correct temporal
pattern but with a wrong and higher than
natural carrier frequency did elicit anom-
FIG. 7. Aspects of the cricket's nervous system. A.
CNS of Gryllus campestris with the ganglia, connectives
and lateral nerves. B, brain; SEG, subesophageal ganglion; T l - 3 , thoracic ganglia; A3-7, free abdominal
ganglia. In crickets Al and A2 are fused with T3. B.
Prothoracic ganglion with the bilateral arrangement
of the auditory nerve bundles (dotted areas) within
the leg nerve (LN) and the left and right auditory
neuropiles (LAN, RAN). C. Structure of the mirror
image Omega cells (ONI L—black) (ONI R—
hatched). Arrows indicate the excitatory auditory input
to the left and right cell respectively. D. Scheme of a
transversal section through the mesothoracic ganglion to demonstrate the bilateral arrangement of
main neuropile areas (hatched vertically and horizontally) and several of the mirror image fiber tracts
(hatched densely and oblique). DIT, dorsal intermedia! tract; DLT, dorsal lateral tract; DMT, dorsal
medial tract; LVT, lateral ventral tract; VIT, ventral
intermedial tract; VT, ventral tract. (Modified from
Huber, 1990.)
alous phonotaxis. The female tracked the
sound source with an erroneous angle and
this angle was carrier frequency dependent
(Thorson et al., 1982). She behaved as if
the sound source had changed in space.
The mechanism for anomalous phonotaxis
is not completely understood. However,
anomalous phonotaxis clearly demonstrates that songs with wrong carrier frequencies but correct patterns do not abolish recognition but influence sound
localization.
616
FRANZ HUBER
song recognition, as discussed in the next
section.
CELLULAR CORRELATES FOR
SONG RECOGNITION
1. Functional properties of cricket ears
and prothoracic auditory interneurons
The auditory pathway in crickets begins
with the ears (tympanal organs) located
within the proximal parts of the foretibiae.
FIG. 8. Behavioral tuning (bandpass-property) to a
specific range of syllable repetition rates (SRR) during Each auditory organ consists of about 50phonotaxis of female Cryllus campestris presented in 60 auditory sense cells arranged in rows
a "to and fro" sequence. The dotted areas indicate and attached to the upper wall of the inner
the degree of variation in the response of all females trachea (Eibl, 1978). This arrangement of
tested with a preference near 30 Hz, and the black auditory sense cells reflects tonotopicity,
dots denote the extreme values. (Modified from
i.e., auditory receptors according to their
Thorson etai, 1982.)
location are tuned to different sound frequencies: proximal receptors respond
3. Bandpass-property for song recognition
preferably to lower, distal receptors to
By changing one of several temporal higher frequencies (Oldfield et al, 1986).
parameters of the calling song, we found Thus, the ear analyzes frequencies, an abilone parameter especially important for ity required, for instance, to encode calling
song recognition: the syllable repetition rate and courtship songs having different car(SRR) (Fig. 8) (Thorson et al., 1982), rier frequencies as well as ultrasonic sounds
whereas even considerable changes in other (for literature see Bennet-Clark, 1989; Polparameters were much less critical. This lack and Hoy, 1989).
indicates that at least Gryllus campestris and Sound intensity is encoded in the spike
Gryllus bimaculatus have developed a win- frequency of the auditory sense cell. Moredow for attractive SRRs in phonotaxis, a over, auditory receptors at their best frebandpass, ranging from about 19-43 Hz, quency copy the temporal structure of the
and peaking around 25-35 Hz. The prob- song, but, with an important restriction:
lem of a trade-off strategy in song pattern they are not specifically tuned to the timing
recognition, i.e., the evaluation and of the conspecific pattern (Esch et al., 1980).
weighting of several parameters, is still This indicates that the ears of crickets cover
unsolved and will not be discussed here a much wider range of sound frequencies
(Stouts al., 1983, Doherty, 19856, c).
and copy a broader range of patterns than
used for intraspecific communication. From
4. Temperature: Sound production and
a biological point of view, this is not at all
phonotaxis
surprising because the ears have also
Crickets are poikilothermic animals. evolved as sensory devices for predator
They have to match acoustic communica- avoidance where different sound frequention patterns with changes in ambient tem- cies and temporal patterns are used (Huber,
peratures. "Hot" males produce faster 1989).
Auditory nerve fibers project to the proSRRs than "colder" males, and equally
acclimatized females are tuned to them, thoracic ganglion and terminate within a
i.e., they shift their bandpass, respectively part of the ring tract, an area called the
acoustic neuropile. Each ear is represented
(Doherty, 1985a).
To sum up: Our finding that the SRR is by fiber terminals only in the correspondthe most important recognition parameter ing hemiganglion (for literature see Schildencouraged us to search for neuronal cor- berger et al., 1989). Within the prothoracic
relates and to propose a mechanism for ganglion auditory information is transmitS P [ms]
S R R [Hz]
23
43
28
36
35
29
43
23
53
19
67
15
81
12
100
10
NERVE CELLS AND INSECT BEHAVIOR
617
ted to a family of neurons which exist as
mirror image pairs, and some of them have
been identified by intracellular recording
and staining in several genera of crickets.
We can distinguish local prothoracic interneurons such as the Omega neurons (ON)
with arborizations restricted to both halves
of the ganglion, ascending (AN) and
descending (DN) plurisegmental neurons,
projecting to the brain or to lower parts of
the ventral nerve cord, and neurons with
T-shaped structures (TN).
Only for Teleogryllus commodus has monosynaptic transmission between auditory
afferents and AN1 and AN2 neurons been
substantiated (Fig. 9) (Hennig, 1988). But
there is no indication of specific tuning in
any of these prothoracic interneurons to
SRRs necessary for the female to exhibit
phonotaxis. This led us to search for cellular correlates of song recognition in the
next station of the auditory pathway, the
brain (Schildberger, 19846).
2. Song recognition by local brain neurons
Based on behavioral studies, conspecific
song recognition requires neurons sensitive to phonotactically effective SRRs.
Auditory information is conducted to the
brain via ascending interneurons (AN1,
AN2 and probably others) and processed
there by at least two classes of local brain
neurons (BNC1, BNC2). According to anatomical arrangements and latency measurements, Schildberger (19846) proposed
a cascade of events in each brain hemisphere: Ascending neurons feed song
information into members of BNC 1 cells,
and they and BNC2 cells are targets for
further information processing. Within the
classes of BNC 1 and BNC2 cells three functional types were discovered (Fig. 10A), (i)
Neurons acting as highpass filters (HP-F)
by responding to faster SRRs and (ii) neurons acting as lowpass filters (LP-F) by
responding to slower SRRs, both covering
a range inside and outside the phonotactic
attractiveness, (iii) Within the class of BNC2
cells, a subclass was identified with a bandpass-property (BP-F), i.e., cells that
responded only to those SRRs to which the
female on the treadmill exhibited phono-
FIG. 9. Indications for monosynaptic connections in
Teleogryllus oceankus between auditory afferent fibers
(HNF) and two ascending auditory interneurons (AN 1,
AN2) located within the prothoracic ganglion, studied with electrical stimulation of the auditory nerve.
A. Prothoracic ganglion with the structure of AN1
(left) and AN2 (right). Arrows indicate the position
of the intracellular electrodes (for the auditory afferent fibers only shown left). B. Superimposed traces of
spike potentials at expanded scale to demonstrate the
time relationships between afferent auditory fiber
spikes and postsynaptic responses in AN1 and AN2.
Top to bottom: HNF, auditory afferent fiber; AN1,
received excitatory input mediated by a low frequency
(4 kHz) receptor fiber; AN2, received excitatory input
from a high frequency receptor fiber. In each trace
the initial deflection indicates the stimulus artefact.
AN1 and AN2 exhibit short and constant latencies
to the stimulus of 3.5 ms, and latencies to the onset
of the receptor spike of ca. 1 ms (AN1) and 0.6 ms
(AN2). (Modified from Henning, 1988.)
taxis. But these cells showed no pattern
copying of the syllable rhythm and they
lost encoding of sound intensity at moderate and higher SPLs.
Schildberger (see Huber and Thorson,
1985) proposed a model (Fig. 10B) about
a cellular and network mechanism for song
recognition in the brain, based on the ANDgate property. However, the remaining gap
618
FRANZ HUBER
75-
75
_
3?
x
as
O
O
c
o
0)
CD
Q.
CO 2 5
25
26
50
Thorax
B
74
98
Syllable interval [ms]
Brain
BP-F
Chirp
• •••
SI
Auditory
Pathway
ANDGate
-Phonotaxis
LP-F
FIG. 10. Neuronal correlates for song recognition in the brain of Gryllus bimaculatus. A. Correlation of the
phonotactic response (hatched area indicating a band-pass property, peaking around 30 Hz SSR) with the
activity of bandpass neurons BP-F (marked by open circles for different females and by closed circles connected
by lines in one female). Other local brain neurons of the same classes exhibit either highpass properties (HPF, triangles) or lowpass properties (LP-F, squares) responding preferably to faster or slower syllable repetition
rates, respectively. Note that HP-F and LP-F form the boundaries of BP-F. B. Model to explain how the bandpass property for attractive SRRs could arise from AND-gating highpass and lowpass neurons. (A, modified
from Schildberger, 19846; B, modified from Huber and Thorson, 1985.)
involves our ignorance of the detailed neuronal implementation, especially with
respect to synaptic mechanisms and connectivities among the cells.
1981). It allows sound to travel to the tympanum from outside and via the acoustic
trachea from inside. Thus, vibrations of
the tympanum, necessary for hearing
(Kleindienst etal, 1983), are based on presBEHAVIORAL AND NEURONAL ASPECTS
sure and phase differences of the sound
OF SONG LOCALIZATION
waves impinging on the tympana.
1. Cricket ears as pressure gradient
Pressure gradient receivers have cardoid
receivers
directional characteristics, i.e., the sense
The cricket ear is a pressure gradient cells are excited with different strengths
receiver (Fig. 11 A) (for literature see Lar- depending on the angle of sound incidence
sen et at, 1989). The tracheal system to (Fig. 11B) (Boyd and Lewis, 1983). Both
which the tympana are connected acts as ears exhibit nearly mirror image direcan internal sound conducting pathway tional characteristics with a frontal and
(Kleindienst, 1980, 1987; KleindienstWaZ., caudal intersection point. During phono-
619
NERVE CELLS AND INSECT BEHAVIOR
cavity 2
step
attenuator -
stimulus
generator
inhibitory stimulus (dB)
65
75
85
95
FIG. 11. Cricket ears as pressure gradient receivers.
A. Prothoracic segment opened and seen from a frontal view with the two ear bearing forelegs. ATY, anterior tympanum; PTY, posterior tympanum; AT,
acoustic trachea connecting both ears; PTG, prothoracic ganglion; SR, SL, right and left stigma (lateral opening for sound entrance). B. Cardoid and
mirror image directional characteristics of Gryllus
campestris ears, obtained by recordings from whole
auditory nerves of left (L) and right (R) ear. Polar
plots show evoked responses to single sound pulses of
20 ms duration and 5 ms rise/fall time, averaged over
128 presentations and delivered at constant sound
intensities (70 dB SPL) and of 4.8 kHz from different
angles. The two directional curves cross frontal and
caudal, and exhibit greatest left-right differences to
lateral stimulation (adapted and modified from Boyd
and Lewis, 1983). C. Diagram to explain binaural
directional hearing based on the algorithm "turn to
the side more strongly stimulated." According to the
directional responses of the left and the right ear their
information is fed into left and right central prothoracic ascending neurons (NL and NR), respectively.
Their activity is compared by a central comparator
(possibly located within the brain) which evaluates
left/right excitation differences (AIR/L) for correcting
the course, indicated by zig-zagging of the female
during phonotaxis (adapted from Huber, 1987).
tactic tracking crickets follow the algorithm "turn to the side more strongly stimu-
lated." Their zig-zag course allows them to
pursue the frontal crossover point where
the left and right intensity and excitation
differences are minimized (Fig. 11C) (for
literature see Huber, 1987).
E
4
1
45
'
55
'
r—constant stimulus 65 dB
*\ ' 0
65
excitatory stimulus (dB)
FIG. 12. Quantitative analysis of contralateral inhibition in the Omega cell type 1 in response to 5 kHz
sound signals. A. Closed sound field arrangement (leg
phones = miniature sound chambers) for external and
internal isolation of excitatory and inhibitory inputs
to the ONI (fi). Ml, M2 microphones 1 and 2 acting
as miniature loudspeakers. B. Response characteristic
( • — • ) and latency (O
O) of the Omega cell for
various excitatory and inhibitory stimulus settings.
Symbols represent means of 30 consecutive sound
presentations with standard deviations. Sound pulse
duration: 50 ms, rise and fall times: 2 ms (adapted
from Kleindienst el al., 1981).
2. Processing of monaural and binaural
auditory input by prothoracic
interneurons, and network analysis
With the invention of the legphones (Fig.
12A) {i.e., miniature sound chambers
around the ear) (Kleindienst et al., 1981),
each ear could be stimulated separately
after severing the acoustic trachea connecting both ears while recording simultaneously from different types of prothoracic interneurons. Thus, binaural and
monaural inputs to these neurons and some
network properties could be studied (Wohlersand Huber, 1982).
620
FRANZ HUBER
pattern copying in these cells (for literature
seeSchildberger^a/., 1989; Huber, 1989).
3. A direct approach to song
localization by hyperpolarizing
single ascending interneurons
Network studies of prothoracic neurons
and effects of cell killing (see also Atkins et
al., 1984) led to the assumption that some
of these neurons are involved in song localization. To test this hypothesis, an openloop arrangement was used to study
phonotactic behavior and single cell
responses simultaneously in female Gryllus
60 0
100 200 300 0
100 200 300
Time (s)
Tims (ms)
Time (mi)
bimaculatus (Fig. 13) (Schildberger and
Horner, 1988).
FIG. 13. Correlation and causal relationship between
phonotactic course and the activity of an ascending
To obtain a causal relationship between
auditory interneuron in the cricket, Gryllus bimacu- the phonotactic course and neuronal activlatus. A. Open-loop experimental arrangement for
intracellular recordings from walking animals. The ities one needs reversible manipulation of
animal is fixed on a holder and can only walk straight single neurons during the behavioral perforward, but the legs can turn an airsupported sty- formance which cell killing does not offer.
rofoam ball. A special camera (IR) senses two com- The female cricket was mounted as shown
ponents of the ball's (animal's) movement—rotation
and translation—and thus its turning tendency. Call- in Figure 13A; it could only walk straight
ing song is delivered by one of two loudspeakers (L, forward but turned an airsuspended ball
R) 50° on either side of the longitudinal axis of the with its legs, and ball rotation was mearestrained animal. The computer controls model call- sured. One loudspeaker positioned 50° to
ing song broadcast, and later evaluates tape recorded the left or to the right in azimuth to the
movements of the animal and neuronal activities. B.
Graph with rotation of the animal by sound delivered body axis of the female broadcast the callfrom the left speaker (a), from the right speaker (b), ing song while either AN1, ONI, or AN2
and to the right (c) after the left AN1 neuron had neurons were recorded intracellularly and
been hyperpolarized, despite sound stimulation from later on manipulated electrically. With a
the left. C. Outlines of the prothoracic ganglion with
the mirror image AN1 cells (LAN], dendritic field model calling song presented via the left
and axon on the left and RANI, dendritic field and loudspeaker, the left AN1 neuron (with the
axon on the right). In both neurons the axon courses dendritic field on the left side) (Fig. 13C),
to the brain. D. Response patterns of AN1 cells to a was more strongly excited and copied the
four syllabic calling chirp (bottom trace). Further pattern (a, in Fig. 13D). The animal folexplanations are given in the text (adapted from
lowed the algorithm "turn to side more
Huber, 1989).
strongly excited" and turned to the left
sound source (a, in Fig. 13B). By considering
the directional characteristic of the
Between the mirror image ONI type
right
ear,
under this condition the right
neurons reciprocal inhibitory connections
AN1
neuron
must have been less excited
were discovered which serve to increase
(a',
in
Fig.
13D).
When the calling song was
the binaural contrast (Fig. 12B). This was
broadcast via the right loudspeaker, the
further established by selective cell killing animal turned to the right (b, in Fig. 13B).
with photoinactivation (Selverston et al., While still recording from the left AN1
1985), which removed inhibition from one neuron it was now less excited than before
ON 1 neuron upon the other. When testing (b, in Fig. 13D). On the other hand, the
the animal after killing of one ON 1 neuron mirror-image partner cell on the contraon the treadmill, it tracked the sound lateral side was now more strongly excited
source with a slightly erroneous angle. (b\ in Fig. 13D).
Morever, ONI-neurons inhibit contralatThe crucial experiment for establishing
eral AN1 and AN2 neurons, which may
assist to enhance directionality as well as the hypothesis of binaural comparison was
NERVE CELLS AND INSECT BEHAVIOR
to hyperpolarize the left AN 1, i.e., to reduce
its activity even below the level of its right
mirror image cell (compare c with c' in Fig.
13D) and to broadcast the sound from the
left, its excitatory side. An animal with a
nonhyperpolarized left AN 1 cell turned to
the left (a, in Fig. 13B). As predicted by
the rule, the animal changed its course to
the right when the neuron was hyperpolarized (c, in Fig. 13B).
This indicates that the system responsible for orientation must have received
"wrong directional information" due to the
reduced activity of this single hyperpolarized cell. The effects of hyperpolarizing
single AN2 and ONI neurons caused less
dramatic changes in walking courses
(Schildberger and Horner, 1988).
3. Pattern dependence of sound
localization
621
and the activation levels of these two neurons corresponded only if pattern copying
of the neurons was considered. With calling song from above and continuous tone
from ipsilateral to the neurons recorded,
their pattern copying was masked, whereas
in the contralateral neurons pattern copying was still maintained.
These results demonstrate that the overall activity of the two mirror image ascending neurons does not directly guide orientation. It first has to pass a filter tuned
to the temporal structure of syllables and
chirps. Thus, recognition of the conspecific song and localization of the sound
source are not independent events.
SONG ORIENTATION IN
ONE-EARED CRICKETS
1. Walking courses in one-eared crickets
When Pollack et al. (1984) studied sound
The algorithm based on binaural comfrequency effects during tethered flight and parison predicts that animals with only one
compensated walking in Teleogryllus oceani- ear ought to circle to the side of the
cus, they found a larger shift in angular remaining ear. However, Huber et al.
error of tracking at the same high fre- (1984), Schmitz et al. (1988) and Schmitz
quency (15 kHz) after the sound pattern (1989) found that more than 30% of monhad changed from a four-pulsed calling aural females of Gryllus campestris and G.
song to a sound containing a single pulse bimaculatus exhibited phonotaxis even with
one ear. These females recognized the conof the chirp rhythm (2/sec).
Stabel (1988) and Stabel et al. (1989) ana- specific song by input from one ear, and,
lyzed phonotaxis of female Gryllus bimacu- even more surprising, they succeeded in
latus with an open-loop device. They tracking the sound source.
recorded the turning tendency of a tethIn adult female crickets, one foreleg
ered female Gryllus bimaculatus on paired bearing an ear in the tibia was amputated
tread wheels in a complex acoustic stimulus between coxa and femur. When the ampuparadigm. When calling song at the correct tation occurred before the 6th instar (4-5
carrier frequency was broadcast horizon- instars before imaginal molt) the leg regentally the female turned to its side as erated often to its full length and size, but
expected. However, as soon as the same without an auditory organ. Several extercalling pattern was broadcast from above nal sensory systems reappeared and leg
{i.e., without directional cues), and a con- muscle innervation was completed, as inditinuous tone of a slightly different carrier cated by the coordinated walking of the
frequency was presented horizontally, the regenerated leg (Huber, 1987; Schildberfemale changed its direction and turned ger and Huber, 1988).
away from the horizontal sound source.
When a calling song was broadcast from
This sign reversal in turning was then stud- a horizontal direction, some females kept
ied at the level of two ascending auditory course, although with an error angle usuinterneurons, AN1 and AN2, recorded ally below 90°, which in nature would guide
extracellularly from the cervical connec- them through an arc to the singing male
tives while the animal walked. Both the (Fig. 14A, C). Phonotactic tracking was
characteristic curves in turning tendency most commonly elicited in a smaller sound
(toward the sound source or away from it) intensity range, preferably at lower inten-
622
FRANZ HUBER
with the central neurons of the deprived
side. Or, crickets can switch from the
mechanism of binaural comparison to one
with consecutive measurements of monaural input, that is, to a scanning mechanism, since auditory excitation varies
according to the directional characteristics
of the remaining ear. Here I only discuss
results that favor the first alternative; for
the second, refer to Schildberger and
Kleindienst (1989).
-1.2
FIG. 14. Phonotactic tracking in one-eared Gryllus
bimaculatus females to model calling song. A. x, y plots
of sound source dependent walking courses of an intact
female. C. Change in walking angle of the same female
after amputation of the right foreleg. Note the deviation from the sound source by about 70° toward the
left ear. B. Precise phonotactic tracking of an adult
female which lost the right foreleg in an earlier larval
instar and regenerated it to its normal length, but
without a functional auditory organ. D. No change
in walking courses in the same female after amputation of the previously regenerated right foreleg. L 1,
2, loudspeakers 1 and 2, respectively, positioned 135°
apart. Sound intensity was 70 dB SPL. Each trace
represents a 20 sec walking (adapted from Huber,
1987).
sides, and it could be observed in some
adults already within 24 hr after ear loss.
Course accuracy in some adults improved
when the foreleg had been amputated in
earlier larval instars (Fig. 14B, D), or in
adults, after a week or two had elapsed
between amputation and test (Schmitz et
ai, 1988; Schmitz, 1989). Some females
tracked the sound source as accurately as
binaural animals. This led to the question,
what kind of localization mechanism is
involved in monoaural crickets.
There are, in principle, two mechanisms
which could account for tracking the sound
source with only one ear. Either the cricket
reorganizes the auditory pathway so that
the remaining ear drives a central bilateral
system which would allow central comparison. Such a mechanism would imply that
the existing ear makes new connections
2. Bilateral central comparison due to
changes in structure and function of
central prothoracic auditory neurons
In adults which had lost one foreleg in
a larval instar and regenerated it, or in
adults with enough time elapsed between
amputation, bilateral comparison could
result from two different mechanisms: (i)
primary auditory fibers, known to terminate preferably within the ipsilateral auditory neuropile, could grow processes across
the ganglionic midline to meet neurons
with dendritic fields in the contralateral
hemiganglion. Many cobalt backfills of
auditory nerves in monaural crickets
revealed that only very few primary auditory fibers crossed the ganglion midline,
and perhaps not more than already seen
in binaural animals (Schmitz, 1989). It is
still unknown whether these fibers carry
auditory information from the remaining
ear to the contralateral central neurons
deprived from their previous auditory
inputs.
A second alternative is that central auditory neurons, the target cells of primary
auditory fibers, change their morphology
and function after monaural deprivation.
This was found in several of the identified
local and ascending interneurons in different cricket species (for literature see
Schildberger et ah, 1989). The previously
deafferented neurons grew dendrites from
their former input area which crossed the
ganglion midline to invade the auditory
neuropile of the intact side (cf, Fig. 15 A,
B). These cross-grown dendrites made
functional connections, very probably with
primary auditory fiber terminations, which
were manifested by their responses to stimulation of the remaining intact ear. Thus,
NERVE CELLS AND INSECT BEHAVIOR
they were rewired with the "wrong ear."
According to their threshold curves (Fig.
15C) and intensity-response functions (Fig.
15D), the rewiring created functional
properties very similar to intact cells,
including the cell specific pattern copying
(inset in Fig. 15C). Thus, one can state that
the cross-grown dendrites must have
"found" terminals of auditory sense cells
of the wrong ear comparable to those with
which these neurons were previously connected on their intact side, and even the
synaptic organization must have been
restored. This plasticity was unexpected in
crickets and calls for future research in
developmental and postembryonic neurobiology.
3. Constraints for phonotaxis with one ear
and experimental proofs
Despite this time dependent and unexpected reorganization within the prothoracic auditory pathway, the mechanism
underlying monaural tracking is not yet
explained. If localization in monaural animals is the result of a central bilateral comparison, then one should propose different
thresholds, based on synaptic efficacies
and/or combinations of excitation and
inhibition. Furthermore different slopes of
the intensity-response functions should be
expected, resulting in different directional
characteristics between neurons connected
to the remaining ear, and those rewired to
the wrong ear. For tracking, monaural animals need an intersection point of the intensity-response functions of a neuronal pair
(similar to the frontal intersection point of
binaural animals), which would enable them
to set an equilibrium between the excitation of both auditory pathways necessary
to perform phonotaxis, by following the
rule similar to that used by intact binaural
crickets (Fig. 16A).
Such intersection points have recently
been discovered in the intensity-response
functions of the pair of AN2 neurons by
Schildberger and Kleindienst (1989) (Fig.
16B). Only those females which exhibited
phonotaxis on the treadmill (closed-loop)
or showed a reverse in turning tendency
in the open-loop condition at a distinct
sound intensity, had an intersection point
623
FIG. 15. Structural and functional changes in prothoracic auditory neurons (Omega cells of type 1) in
one-eared Gryllus bimaculatus, after the loss of the left
auditory input in an earlier larval instar. A. Lucifer
yellow fill of a left Omega neuron in the intact animal
(horizontal view). B. Left Omega neuron with dendrites grown across the ganglion midline from the
former input area and arborizations within the contralateral neuropile (which is normally the output area
of the cell). C. Comparison of auditory thresholds in
normal and deafferented ON 1 cells shows only slight
differences within the tested frequency range. Inset:
Pattern copying of the deprived ONI cell now wired
with the wrong, intact ear. D. Intensity-response
curves of intact and deprived ONI cells listed in C.
The slopes are very similar except for a decrease in
response in the deprived ONI at higher stimulus
intensities (adapted from Huber, 1989).
in the corresponding neuronal pair correlated within this intensity range. Nonorienting females lacked such an intersection point (cf Fig. 16B, lower left with lower
right).
Thus, it seems that the structural reorganization of the central auditory pathway
in monaural crickets is accompanied by
changes in some functional properties of
the participating neurons. Both together
allow a bilateral central comparison used
for tracking. However, one should not forget that only some females tracked the
sound source within a restricted intensity
range while others, with probably a similar
structural reorganisation but a missing
functional repair did not (Schmitz et ai,
1988).
This and the fact that some females
tracked the sound source already several
hours to one day after loss of one ear, where
the described morphological changes have
624
FRANZ HUBER
not been observed (Schmitz, 1989), pose
questions regarding normal and regenerative development, functional plasticity in
single neurons, and they even point strongly
to a second sound orientation mechanism
which has recently been found: a monaural
scanning device (Schildberger and Kleindienst, 1989).
CONCLUDING REMARKS
FIG. 16. Evidences for a central bilateral comparison
in one-eared crickets with loss of the right ear in an
earlier larval instar and after subsequent regeneration
of the right foreleg without its ear. A. Left, diagram
of the situation: The intact left ear did not change its
directional characteristic. Its input reaches both left
(NL) and right (NR) prothoracic ascending neurons.
They conduct song specific directional information
to a central comparator (Com), which evaluates left/
right activity differences (AIL/R) and minimizes them
to establish the course. A. Middle, hypothetical and
rather parallel intensity—response functions of a neuronal pair with the NR newly connected. Turning
tendencies are shown, if the animal follows the algorithm "turn to the side more strongly stimulated."
A. Right, hypothetical intensity-response functions
of the same neuronal pair with different slopes now
intersecting. The intersection point would be a stable
point for tracking. Turning tendencies are indicated
below and above the intersection point. B. Experimental proof for A. Upper left, examples are shown
for one animal (Animal A) which tracked the sound
source under closed loop conditions at 60 dB SPL,
and for a second animal (Animal B) with the same
treatment but without phonotaxis. Upper right, Animal B followed the algorithm "turn to the side more
strongly stimulated" by consistently turning to the
left under open-loop conditions, whereas Animal A
showed a reversal in turning in the range between 60
to 70 dB SPL. At low sound intensities it turned to
the side of the deprived ear; at higher sound intensities it changed to the side of the intact left ear.
Lower left, intensity—response curves of the mirror
image AN2 neurons recorded extracellularly in Animal B with no phonotaxis indicate that the intact and
normally wired left A\2-cell is more sensitive to sound
within the whole intensity range tested. Thus the left
AX2 seems to determine turning toward its side.
Lower right, in Animal A, howeser, which exhibits
phonotaxis under closed-loop conditions and shows a
change in turning under open-loop conditions, an
intersection point is seen in the intensity-response
The top-down approach applied to song
recognition and song localization in crickets was successful because results of highresolution studies of phonotactic behavior
guided the questions addressed to single
nerve cells.
We first learned that the world of crickets is not solely an acoustic world which
invites studies of multisensory and multimodal inputs and their processing within
the CNS in the context of behavior.
We have identified a cellular correlate
in the brain with a bandpass-property for
SRRs similar to the one obligatory for
phonotaxis in the behaving animal. Without, however, knowing the neuronal hardware in detail, we even present a mechanism which could be responsible. Students
of animal behavior would perhaps call the
bandpass-cells in the brain an element of
the innate releasing mechanism (IRM).
For song localization the binaural algorithm "turn to the side most strongly stimulated" could be established at the level of
a single ascending neuronal pair. However,
the comparison and transfer of directional
information (possibly within the brain) is
still a matter of speculation.
Other studies have shown that localization of a calling song source needs patterned information from the ventral nerve
cord, which clearly suggests that recogni-
curves (IR-function) in the two AN2 cells, within the
corresponding sound intensity range (compare upper
right with lower right). At lower intensities the
deprived right AN2 cell is more strongly excited and
determines turning to its side: at higher intensities
the intact AN2 cell is more strongly excited which
results in turning to the left as expected by following
the algorithm (modified and adapted from Schildberger and Kleindienst, 1989).
NERVE CELLS AND INSECT BEHAVIOR
tion and localization are not based on two
completely independent neuronal circuits.
Finally, one-eared crickets with their
ability to track a sound source have elucidated an unexpected plasticity in the
behavior related to structural and functional changes of central neurons. These
findings will certainly facilitate further
studies on the development and the regeneration power of the auditory pathway,
including sensory deprivation or overstimulation in single cells. Thus, the nervous
system of the cricket is not completely
hardwired. Plasticity within nerve cells
allows adjustment of synaptic efficacies and
formation of new connections with changing conditions within the body and in the
environment.
ACKNOWLEDGMENTS
I am most grateful to my coworkers and
guests for their motivation, experimental
skills and ongoing interest in the work
which is presented here.
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