Naturwissenschaften (2001) 88:159-170
DOI 10.1007/s001140100223
R E V I E W A RT I C L E
A. Stumpner · D. von Helversen
Evolution and function of auditory systems in insects
Published online: 8 May 2001
© Springer-Verlag 2001
Abstract While the sensing of substrate vibrations is
common among arthropods, the reception of sound pressure waves is an adaptation restricted to insects, which
has arisen independently several times in different orders. Wherever studied, tympanal organs were shown to
derive from chordotonal precursors, which were modified such that mechanosensitive scolopidia became attached to thin cuticular membranes backed by air-filled
tracheal cavities (except in lacewings). The behavioural
context in which hearing has evolved has strongly determined the design and properties of the auditory system.
Hearing organs which have evolved in the context of
predator avoidance are highly sensitive, preferentially in
a broad range of ultrasound frequencies, which release
rapid escape manoeuvres. Hearing in the context of communication does not only require recognition and discrimination of highly specific song patterns but also their
localisation. Typically, the spectrum of the conspecific
signals matches the best sensitivity of the receiver. Directionality is achieved by means of sophisticated peripheral structures and is further enhanced by neuronal
processing. Side-specific gain control typically allows
the insect to encode the loudest signal on each side. The
filtered information is transmitted to the brain, where the
final steps of pattern recognition and localisation occur.
The outputs of such filter networks, modulated or gated
by further processes (subsumed by the term motivation),
trigger command neurones for specific behaviours. Altogether, the many improvements opportunistically
evolved at any stage of acoustic information-processing
ultimately allow insects to come up with astonishing
acoustic performances similar to those achieved by vertebrates.
A. Stumpner (✉)
Institut für Zoologie und Anthropologie, Universität Göttingen,
Berliner Strasse 28, 37073 Göttingen, Germany
e-mail: [email protected]
Tel.: +49-551-395574, Fax: +49-551-395438
D. von Helversen
Max-Planck-Institut für Verhaltensphysiologie,
82319 Seewiesen/Starnberg, Germany
Introduction
Not only in most vertebrates, but also in many invertebrates, sound is of paramount importance for communication, for orientation and for recognition of potential dangers. Most of those invertebrates that can hear are insects.
Hearing in insects has evolved independently several
times and has led to an enormous biodiversity of auditory
systems (see e.g. Fullard and Yack 1993; Hoy and Robert
1996; Yager 1999). From head to abdomen, from legs to
wings, there is almost no part of the insect body which
does not bear an ear in at least one group. This is astonishing if one considers how appendages such as legs and
wings move and vibrate during locomotion.
Hearing has evolved in several different behavioural
contexts. Firstly, hearing may have evolved as an adaptation for detecting the approach of predators, as is most
likely the case in grasshoppers, mantises, moths, lacewings and beetles. Secondly, hearing and signalling may
also have evolved in a coevolutionary process for mate
finding and mate recognition, as has been suggested for
crickets, bushcrickets, cicadas, and possibly water bugs.
For the Ensifera and cicadas it is likely that acoustic signalling and hearing developed from vibratory communication – maybe in combination with enhancing pheromone signals – and this may be true for other taxa as
well (e.g. Pringle 1957; Roth and Hartmann 1967; Otte
1977; Kalmring and Kühne 1980; Kalmring et al. 1990a;
Bailey 1991; Hoy and Robert 1996; Robert and Hoy
1998; Lakes-Harlan et al. 1999).
Of course, the initial selection pressure for the evolution of hearing may be different from the selection pressure for its persistence today. Additional functions of
hearing may have supplemented or even replaced the
original one when selection pressures changed or were
added over the course of time. In many groups it is quite
obvious that the ability to hear was developed first and
acoustic signalling evolved later (several taxa of grasshoppers, Riede et al. 1990; several moths, Fullard 1998).
On the other hand, a secondary loss of hearing has also
occurred several times, probably in those cases when the
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costs of acoustic signalling surpassed its benefits (e.g. in
several cricket species, Otte 1990; and some bushcrickets, Lakes-Harlan et al. 1991). In any case, hearing
seems to be a very ancient invention at least among
Orthoptera (Sharov 1971), and some recently discovered
specimen of bushcricket fossils from the Tertiary reveal
very modern tympanic structures (Rust et al. 1999).
There is strong evidence that most tympanal ears
evolved from chordotonal organs (e.g. Yack 1992;
Boyan 1993; Fullard and Yack 1993; Hoy and Robert
1996; Lakes-Harlan et al. 1999; Hasenfuss 2000) and the
investigation of serially homologous chordotonal organs
has proved especially helpful in this respect (Meier and
Reichert 1990; Yager 1996; van Staaden and Römer
1998; Prier and Boyan 2000).
Functional aspects of hearing in different contexts
The initial selection pressure for the evolution of hearing
has probably strongly influenced the design and capabilities of the respective organ. Thus, investigating the initial functions may help us to better understand recent
constraints or differences between groups. In this section, we will first focus on the detection of predators and
then on intraspecific communication and host detection
by parasitoids, since these tasks place different demands
on the hearing organs. The following section will cover
the relevance of carrier frequencies, which are of paramount importance for directionality of hearing systems
and for signal transmission in the habitat, and communication distances.
The strongest selection pressure on predator detection
will be for maximal sensitivity. Especially where bat
avoidance is concerned, this offers a chance for the prey
to detect the predator before being detected, since the intensity of echoes is considerably reduced compared to
the emitted call, particularly when the structures of the
insect body have sound-absorbing properties (Dijkgraaf
1957). The summation of inputs from the left and right
ear (with a special situation in mantises, which have unpaired ears, but nevertheless bilateral sensory organs)
would improve the signal-to-noise ratio incurring, however, a loss of directional cues. In fact, many escape
manoeuvres elicited by echo-location calls involve nondirectional, erratic zig-zag flight and dropping to the
ground (Roeder 1967; Yager et al. 1990; Yager and
Spangler 1997). Correspondingly, many auditory interneurones sum the inputs from both ears at low intensities, while at higher intensities – given that peripheral directionality exists at all – contralateral inhibition predominates, thus restoring directionality (e.g. in some
grasshopper, cricket and bushcricket neurones; Kalmring
1975; Römer and Marquart 1984; Stumpner 1999a;
A. Stumpner, unpublished). The observation of different
behavioural responses at different intensities of the predatory signals (e.g. in lacewings and moths; Miller 1983)
may be a consequence of this non-linearity of interneuronal function. The strong selection pressure on a rapid escape response is also reflected in its short latency. Typical latencies of startle responses are in the range
<30–100 ms (Faure and Hoy 2000).
Intraspecific communication
Detection of predators
Early detection of an approaching predator and short latency escape manoeuvres are highly adaptive. Therefore,
usually all sensory modalities available (acoustic, vibratory, optical) are used alone or together in the context of
startle and escape behaviour. Grasshoppers, for example,
evolved their ears some 200 or more million years ago,
probably to detect the noise generated by the movements
of predators such as lizards and other terrestrial reptiles
while approaching a potential prey. Depending on the
substrate, these movements may produce a large range of
frequencies including ultrasound.
A great impetus for developing ears in the context of
predator avoidance arose some 60 millions years ago
when bats invaded the night niche of aerial hunters using
ultrasound clicks to detect their prey by echo-location
(Hoy 1992; Stucky and McKenna 1993; Fullard 1998).
In response, tympanal ears evolved in several taxa of
nocturnal flying insects (several times independently in
Lepidoptera, lacewings, beetles, mantises). In groups
that already possessed ears, such as crickets and bushcrickets (e.g. Rust et al. 1999), the hearing range was
most probably widened to effectively perceive the ultrasonic clicks of bats (Hoy 1992; Yager 1999).
While hearing systems which evolved in the context of
predator avoidance are optimised with respect to high
sensitivity and short latency, the major selection pressures for those evolving in the context of communication
were song recognition and sound localisation (as the necessary prerequisites for successful mate finding), or song
recognition alone in the case of male spacing, chorusing
etc. These tasks require a more sophisticated neuronal
network and complex signal processing, compared with
the short latency escape responses involving only few
synapses (see above). Signal recognition involves a neuronal filter mechanism that responds only to a limited
range of the crucial signal parameters. Both subsystems,
the sender signal and the receiver recognition mechanism, become matched in a process of coevolution with
different and partly independent pressures on both subsystems. Signal evolution is mainly driven by the properties of the receiver recognition mechanism which, in
turn, is selected to minimise confusion of “wrong” signals with the correct ones (Heller and von Helversen
1986; von Helversen and von Helversen 1994).
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Song recognition
The parameters used for recognition may be the amplitude modulation of the signal or its spectral composition.
In insects, recognition of a conspecific signal is mainly
based on temporal pattern, i.e. the amplitude modulation,
while the spectrum of the signals normally only plays a
minor role. This is reflected in the enormous diversity of
species-specific and stereotype song patterns found in
acoustically communicating insects, whereas the spectra,
especially of related species, usually differ much less
from each other, as the sound producing systems are
usually very similar (Heller 1988; Otte 1992; Meyer and
Elsner 1996).
Song localisation
A relevant signal of a conspecific has not only to be recognised but also has to be localised. The cues for localisation are the interaural differences in ear drum vibration (which may be caused by interaural differences in
pressure amplitude and/or phase) which are provided by
the directional characteristics of the auditory system (e.g.
Michelsen 1992). A general mechanism to improve localisation is contralateral inhibition, which is a widely
observed phenomenon among auditory neurones (Rheinlaender and Mörchen 1979; Rheinlaender and Römer
1980; Römer and Dronse 1982; Moiseff and Hoy 1983;
Wiese and Eilts 1985; Pollack 1998 for a review). However, strong contralateral inhibition at the first level of
auditory processing may counteract the precise detection
of temporal patterns. Therefore, it is not surprising that
most auditory systems host both types of neurones, those
that sum inputs and those that extract directional information: both over a large range of intensities.
Relatively little is known about how the neuronal processes responsible for recognition and localisation interact in the nervous system. Most of the information available comes from the Orthoptera, exemplifying two different ways of information processing. In grasshoppers
recognition and localisation are processed in parallel; for
pattern recognition the inputs from both ears are pooled,
while for localisation the more strongly excited side determines the response (von Helversen and von Helversen
1995). In agreement with these behavioural findings,
most ascending neurones pool acoustic information from
the two sides and show poor directionality, while only a
few ascending neurones appear to transmit directional
information (Kalmring 1975; Römer and Marquart 1984;
Stumpner and Ronacher 1994; von Helversen and von
Helversen 1995). In crickets and bushcrickets, the information from the two ears remains separated and song
recognition takes place in two neuronal networks, one on
each side, the outputs of which are subsequently compared for directional analysis. Thus the resulting phonotactic movement is not only determined by the intensity
difference but also by quality differences between the
signals on the two sides, which allows a cricket to effec-
tively locate and choose a conspecific mate in the presence of others (Pollack 1988, 1998; Stabel et al 1989;
Sobel and Tank 1994; Schul et al 1998; Römer and
Krusch 2000). In addition, each side selects for the most
intense signal, allowing a clear representation of the
loudest signal out of a chorus of many singing conspecifics. This gain control is established by a slow ipsilateral
inhibition of tonically firing interneurones (Pollack
1988; Sobel and Tank 1994; Römer and Krusch 2000).
Temporal integration
An important aspect in the context of song recognition
and localisation is the time over which a nervous system
integrates in order to arrive at a decision. Song patterns
are often highly repetitive and a minimum duration is
necessary to recognise a signal (Hennig and Weber 1997;
Ronacher and Krahe 1998). This minimum duration may
be well below 200 ms and may involve only one presentation of the elementary pattern unit. This is shorter than
one might intuitively expect, considering that spike patterns of neurones usually change considerably during the
first several hundred milliseconds due to adaptation or
habituation (e.g. Boyan 1985; Stumpner et al. 1991;
Ocker and Hedwig 1993; Stumpner 1999b; Ronacher
and Krahe 2000).
Detection of host signals
Some species of parasitoid flies use the acoustic signals
of their hosts to detect them (Cade 1975; Soper et al.
1976). Such a parasitoid/host system is similar to conspecific communication in that a host must be both recognised and localised (Robert et al. 1996a). However,
in contrast to intraspecific communication, song pattern
recognition in parasitoids may be less specific and include the song patterns of several (host) species (Walker
1993; Wagner 1996). Among other parameters, the duty
cycle of the host signal may be especially important and,
where a choice is available, species with more repetitive
songs are more likely to be infested (Walker 1993;
Lehmann and Heller 1998).
Importance of carrier frequency
Carrier frequency may be a decisive parameter for discrimination between conspecific and predator, to detect
conspecifics in a world of noise made by other species,
to distinguish between male and female, or to discriminate calling from courtship or rivalry songs. In some
cases the entire auditory system appears to focus on only
one frequency band, indicating that the system may have
evolved just for one task (e.g. lacewings, some flies,
many species of moths, tiger beetles, mantises – at least
their ultrasound-sensitive ear; e.g. Hoy 1992; Hoy and
Robert 1996). In other cases, the auditory system has
162
two sensitivity peaks, one at a frequency tuned to the
conspecific signal and the other at a different frequency
range to detect predators (most clearly in many crickets,
e.g. Moiseff et al. 1978; Nolen and Hoy 1986).
Whereas the frequency spectrum may be the most important signal parameter for predator detection, recognition of conspecifics usually relies mainly on the temporal
pattern of a signal (see above). Correspondingly, for
intraspecific communication, a broad frequency band in
artificial stimuli may be as effective as a narrow frequency
band (e.g. Dobler et al. 1994; von Helversen and von
Helversen 1997). Nevertheless, there are clear indications
also for some closely related species of crickets and bushcrickets in which, in addition to other parameters, the frequency spectrum can be used for species discrimination,
especially in species with similar temporal patterns in
their songs (Hill 1974; Hennig and Weber 1997; Schul et
al. 1998). Some grasshopper and bushcricket species use
(in addition to temporal parameters) the spectrum of their
signals to discriminate between male and female (Dobler
et al. 1994; von Helversen and von Helversen 1997). Frequency-dependent excitation and inhibition of neurones
has also been hypothesised to contribute to a more precise coding of temporal patterns at high song intensities
(Boyan 1981; Hutchings and Lewis 1984). Another function of carrier frequency is found in some bushcrickets,
where the spectral composition of the signal might be
used to estimate the distance of a singer (Latimer and
Sippel 1987; Römer 1987; Kalmring et al. 1990a). In
some cricket species different song types, such as calling
and courtship song, may differ clearly in their frequency
spectra (e.g. Gryllus), while in others they differ only in
temporal composition (e.g. Teleogryllus). In both groups,
calling songs elicit positive phonotaxis (e.g. Popov and
Shuvalov 1977; Pollack et al. 1984) and courtship songs
increase mating frequency (e.g. Libersat et al. 1994). The
meaning or evolution of these species differences and the
corresponding differences in the neuronal basis, however,
are not understood so far.
We are not aware of an example in which more than
two frequency bands are used to encode different meanings, although the physiological basis for a fine frequency
resolution is present in many taxa which have hearing
organs with numerous receptor cells tuned to different
frequencies (e.g. Oldfield 1988; Lin et al. 1993; Fonseca
et al 2000 for crickets, bushcrickets and cicadas, respectively). However, the sharp tuning of sensory cells is not
reflected in most auditory interneurones (e.g. Stumpner
1997, 1999b), the broad tuning of which results from
summation of inputs from many receptors and is most
likely used to gain a larger dynamic range of processing
sound intensity (Römer et al. 1998). Central mechanisms
to sharpen frequency tuning i.e. frequency-specific inhibitions, are found in many interneurones. The resultant
tuning, however, usually is no sharper than the tuning of
receptors (Huber et al. 1989; Stumpner 1997, 1998,
1999b).
Finally, carrier frequency plays an important role in
directional hearing. There are two types of tympanal or-
gans; pressure receivers, in which sound acts only on one
side of the tympanal membrane; and pressure gradient
receivers, in which sound acts via external and internal
pathways on both sides of the membrane. For pressure
receivers, only signals with wavelengths short enough to
be diffracted by the insect’s body produce sufficient interaural intensity differences. In pressure gradient receivers, the phase relation of internal and external pressures
varies dependent on the angle of sound incidence. Thus,
precise localisation is limited to a narrow but potentially
low frequency band. The pure tones of cricket songs may
be selected by their highly sophisticated hearing system
allowing correct localisation only in a narrow frequency
range (e.g. Thorson et al. 1982; Löhe and Kleindienst
1994; Michelsen et al. 1994; Michelsen and Löhe 1995).
Organisation of the auditory system
The auditory system of insects consists of three distinct
levels. The peripherally located hearing organ contains
the somata and dendrites of auditory receptors (Fig. 1).
The receptor’s axons enter the corresponding segmental
ganglion, where the first level of central auditory processing takes place (see Figs. 1, 2). In several groups
(grasshoppers, cicadas, moths) the axons may project into several ganglia. Plurisegmental interneurones constitute the transmission channels up to the brain for information on frequency, pattern and direction of a sound
(Fig. 2). The final filtering processes and comparison
between different channels for localisation take place in
the brain (e.g. Ronacher et al. 1986; Bauer and von
Helversen 1987) from where the commands to motor
centres descend. Most data available for the auditory
system are from Orthoptera.
Hearing organs
Two components can be used for the detection of airborne sound, either the velocity of particle movement or
the pressure component. The first is directional but most
useful at distances from the source below about one
wavelength of the sound, whereas the latter provides no
directional information but enables the transmission of
information over much longer distances. Special organs
to detect the velocity component of low sound frequencies (up to about 600 Hz) have evolved in several arthropod groups (e.g. Ewing 1978; Kämper and Dambach
1979; Barth 2000), while hearing based on the perception of sound pressure, as discussed here, has only
evolved in insects. The presence of a tracheal system allows amplification by sound guiding structures by means
of connecting the inner side of the tympanal membrane
to air sacks (which also affects the impedance of ear
drums considerably). The groundplan of the insect body
contains numerous chordotonal organs acting as sensitive proprioceptors to mechanical displacement, which
was the predisposition facilitating the evolution of tym-
163
Fig. 1 Schematic horizontal section through the portion of the
body carrying the tympanum, auditory sense organ and acoustic
trachea in various groups of insects (left in each pair) and schematic representation of central branching of auditory receptors in
the thoracic ganglia (right in each pair). The sizes of the various
groups are not to scale. In crickets, the connecting trachea between left and right is more prominent than shown here and is
very important for directional hearing, while in bushcrickets it is
tiny and probably without function for hearing. A1,2 first or second abdominal neuromere, CNS central nervous system, SO sensory organ, Ty tympanum (position of Ty indicates incidence of external sound), T1,3 pro- and metathoracic ganglion or neuromere.
Redrawn after Wohlers and Huber 1985 (cricket CNS); Stumpner
and Lakes-Harlan 1996 (fly CNS); Roeder and Treat 1957 (moth
ear); Boyan and Fullard 1986 (moth CNS); Yager and Hoy 1989
(mantis); Schwabe 1906 (grasshopper ear); Vogel 1923 (cicada
ear); Huber et al. 1990 (cicada CNS) and own data (crickets, bushcrickets, grasshoppers, hearing flies, cicadas)
panal organs (e.g. Hoy and Robert 1996; Field and
Matheson 1998; Lakes-Harlan et al. 1999; Yager 1999).
are phase-shifted relatively to each other such that the
vibration amplitude on that side is drastically attenuated.
Usually, directional characteristics provide an intensity
difference of several decibels (up to 15 dB or more)
between left and right ear and, typically, show a rapid
change in sensitivity as the sound source crosses the
midline (e.g. Nocke 1975; Hill and Boyan 1976;
Michelsen and Rohrseitz 1995; Michelsen 1998). Comparison of the excitation difference between the two
sides then allows accurate lateralisation of the sound
source at least in the frontal region (Rheinlaender and
Blätgen 1982; Rheinlaender et al. 1986; von Helversen
and Rheinlaender 1988; Schildberger and Kleindienst
1989; von Helversen and von Helversen 1997; Schul et
al. 1998). In hearing flies, a unique lever mechanism obviously has an effect similar to that of a pressure gradient
receiver (Robert et al. 1996b).
Sensory cells
Directionality
In principle, a pressure receiver is not directional. However, sophisticated arrangements of peripheral structures,
allowing sound to act not only on the external but also
on the inner side of the tympanal membrane, caused such
organs to function as pressure gradient receivers. In such
organs, the interaural difference of ear drum vibrations
can be enhanced effectively when the internal and external sound pressures acting on the sound-contralateral ear
The number of receptors in tympanic hearing organs varies from as few as one (Notodontidae, Surlykke 1984) to
as many as several thousands (some cicadas and a
pneumorid grasshopper, Michel 1975; Young and Hill
1977; van Staaden and Römer 1998). The auditory receptors project into the respective abdominal or thoracic
ganglia. Their axons run in the ventral intermediate tract
and collaterals form arborisations in the median ventral
association centre (Pflüger et al. 1988; Boyan 1993),
where they remain strictly ipsilateral (Fig. 1). This neu-
164
Fig. 2 Examples of sound activated interneurones restricted
to one ganglion or fused ganglionic complex (‘local neurones’, left) or with an axon ascending (most likely or definitely) to the brain (right).
Most neurones are assumed to
have direct contact with afferents. The majority of local neurones are probably inhibitory
(demonstrated for crickets and
grasshoppers). The local and
some ascending neurones have
smooth dendrites (predominantly postsynaptic) on one
side and beaded terminations
(predominantly presynaptic) on
the other. Otherwise, ascending
neurones typically have beaded
terminations in the brain. The
neurones are grouped according to similarity of morphology
indicating potential homology,
for which there is some evidence in cricket and bushcricket
or grasshopper and mantis. All
neurones are assumed to be involved in song recognition or
signal localisation (positive or
negative phonotaxis). All species have many more local and
ascending cells. The species
are: Acheta domesticus (cricket: ON1, Stumpner et al. 1995;
AN1, A. Stumpner, unpublished); Magicicada septendecim (cicada A: Huber et al.
1990); Tettigetta josei (cicada
B: Münch 1999); Ancistrura
nigrovittata (bushcricket: ON1,
A. Stumpner unpublished;
AN1, Stumpner 1997); Heliothis virescens (moth: 101, 501,
505, Boyan and Fullard 1986);
Therobia leonidei (fly: AN1,
Stumpner and Lakes-Harlan
1996); Chorthippus biguttulus
(grasshopper: SN1, AN1,
AN12, Stumpner and Ronacher
1991); Mantis religiosa (mantis: MR-501-T3, Yager and
Hoy 1989). Modified after the
authors cited
ropil may be extremely enlarged in the ganglion which
houses the terminations of auditory receptors (e.g. in
bushcrickets). In crickets, bushcrickets, cicadas, mantises
and flies, the receptor projections remain restricted to
one ganglion or to the fused ganglion complex that they
enter, whereas in grasshoppers and some moths single
receptors project anteriorly into the suboesophageal ganglion, and perhaps even into the brain. The central projection of receptor organs may be tonotopically organised, which is seen more clearly in some groups (espe-
cially bushcrickets, Oldfield 1988; Stölting and Stumpner
1998) than in others (e.g. crickets: Oldfield et al. 1986;
Imaizumi and Pollack 1999; Pollack and Imaizumi 1999;
compare also inconsistent results published for grasshoppers: Römer 1985; Halex et al. 1988; Jacobs et al. 1999).
The typical receptor does give (phasic-) tonic responses
and copies the incoming signals, although adaptation
may influence signal representation (e.g. Römer 1976;
Esch et al. 1980; Coro and Perez 1984, 1993; Ronacher
and Römer 1985; Kalmring et al. 1990b). Directional re-
165
sponses of receptors are determined by the directionality
of the peripheral auditory system. The dynamic range of
single receptors covers between 15 and 30 dB; however,
differences in sensitivity may lead to intensity range
fractionation with an increased overall dynamic range
(Rheinlaender 1975; Römer 1987; Römer et al. 1998).
Local and thoracic auditory interneurones
Knowledge about local and thoracic neurones that synapse directly with auditory receptors is mainly based on
few large interneurones such as the omega cell (ON1) in
crickets and bushcrickets, which seem to be mainly involved in processing directional information (e.g. Wiese
and Eilts 1985; Horseman and Huber 1994; Rheinlaender and Römer 1986; Römer and Krusch 2000). It
appears at the moment that the prime task of many local
neurones is to inhibit local and intersegmental interneurones (e.g. Marquart 1985; Selverston et al. 1985),
whereas auditory receptors do excite their postsynaptic
cells, most probably through acetyl choline (Popov et al.
1974; Hildebrand 1982). In addition to contralateral inhibition, frequency-dependent inhibition is found in many
neurones, as demonstrated by two-tone experiments or
by the occurrence of IPSPs (e.g. Boyan 1981; Römer et
al. 1981; Moiseff and Hoy 1983; Römer 1987; Stumpner
1997). This frequency-dependent inhibition is probably
evoked by local or thoracic neurones (e.g. Sokoliuk et al.
1989; Stiedl et al. 1997). In bushcrickets, pharmacological blocking of frequency-dependent inhibition uncovered a broad frequency response in a neurone which is
quite frequency-selective in the intact system (Stumpner
1998). Some thoracic neurones may, however, also transfer excitation to ascending interneurones (e.g. BSN in locusts, Marquart 1985) and even to local neurones (e.g.
ON1 in crickets, which is obviously excited directly by
receptors as well as by local interneurones, Pollack
1994).
The transmitters used by local neurones (as revealed
by immunocytochemistry) vary between the different
cell types and probably include GABA-ergic (Sokoliuk
et al 1989; Thompson and Siegler 1991) and serotonergic (Hörner et al. 1995) cells.
In summary, local (and thoracic) auditory interneurones have not yet been sufficiently characterised. This is
due to the fact that these neurones are usually small and
therefore are not easily accessible for electrophysiological recordings.
Interneurones with an axon ascending to the brain
Ascending interneurones constitute the channels which
transmit the acoustic information to the brain where the
interface between sensory input and motor output is located. As the output elements of the first stage of neuronal processing they encode specific features of an acoustic signal. The number of such neurones, each with char-
acteristic morphological and physiological properties,
varies among groups between at least two (crickets) and
perhaps more than 20 (grasshoppers). Ascending neurones are similar insofar that they have dendrites (mainly
postsynaptic structures) in the ganglion or ganglionic
complex that houses the soma and an axon ascending
contralaterally to the soma up to the brain. Typically, the
axon side is also the side more sensitive to sound, if directionality exists. A prominent exception to this pattern
is found in moths, where the dendrites that seem to receive direct input from receptors lie soma-ipsilaterally
and the axon ascends contralaterally, i.e. on the side contralateral to the respective ear (Boyan and Fullard 1986).
Ascending neurones may (grasshoppers, Pearson et al.
1985; crickets, Hennig 1988; Hirtz and Wiese 1997) or
may not (grasshoppers, e.g. Römer et al. 1988) be directly
connected to receptors; in most cases this is not known
for sure, though indirect evidence e.g. from regeneration
experiments suggests direct connections in several cases
(only primary interneurones seem to show sprouting
after lesions: Pallas and Hoy 1986; Schildberger et al.
1986; Lakes et al. 1990). For one identified intersegmental neurone in the locust (“G-neurone” = "714”) which is
involved in escape behaviour (Pearson et al. 1980)
monosynaptic inputs from sensory cells and various diand trisynaptic inputs were identified and demonstrate
how complex the embedding of a sound activated neurone in the auditory network can be (Boyan 1999). The
neurotransmitters used by ascending neurones are not
known.
Function of ascending neurones
Correlation between the functional characteristics of ascending neurons and acoustically evoked behaviour has
been shown in several cases and their direct influence on
behaviour has been demonstrated for positive and negative phonotaxis in crickets (Nolen and Hoy 1984; Schildberger and Hörner 1988; Atkins et al. 1992). This is certainly the most elegant way to test neuronal function, but
also the most difficult to accomplish. Crickets may be
especially suited for such experiments, since they appear
to use only few neuronal elements (only two ascending
neurones are known, whose responses are sensitive and
consistent enough to evoke positive phonotaxis or have
short enough latencies for negative phonotaxis; e.g.
Wohlers and Huber 1982; Atkins and Pollack 1987).
These elements transmit simultaneously information
about the signal pattern and its location. In most other
groups there is a number of elements, each with specific
filter properties, so that information about different aspects of a song is transmitted in parallel (e.g. Boyan and
Fullard 1986; Wolf 1986; Huber et al. 1990; Stumpner
and Ronacher 1994; Stumpner and Lakes-Harlan 1996;
Schul 1997; Fonseca et al. 2000).
166
Brain neurones
Because ascending neurones may be accessed relatively
easily (compared with brain neurones) we know a great
deal about acoustic information entering the brain but
little about processing within the brain. Only in crickets
do data about brain interneurones exist to such a degree
that a picture had been built up of the organisation of the
final filter level in the CNS: low-pass, high-pass and
band-pass neurones evaluate temporal parameters of
conspecific songs and a number of ultrasound-sensitive
neurones evaluate bat cries (Boyan 1980; Schildberger
1984; Brodfuehrer and Hoy 1990). In grasshoppers, a
body of data from extracellular recordings in the brain
exists, which may include brain neurones with specific
properties combining outputs of simple temporal filters
(Adam 1969), but there is little knowledge about identified local auditory brain neurones and their characteristics (e.g. Boyan et al. 1993). Although the filter mechanisms underlying song pattern recognition are not well
understood so far, it is postulated that their outputs drive
descending command fibres which elicit specific behaviours: in grasshoppers and crickets, specific command
neurones, when stimulated intracellularly, trigger specific stridulatory patterns which normally occur, for
example, in response to a perceived conspecific male or
female song (Hedwig 1994, 1996). Other descending
neurones in the cricket brain were suggested to be involved in phonotactic behaviour: in the presence of calling song the activity of these neurones was correlated
with the translatory and angular velocity respectively;
moreover, the auditory responsiveness of these neurones
was specifically gated by locomotion (Staudacher and
Schildberger 1998).
Conclusions
The pioneering work of people such as Autrum (e.g.
1940), Roeder (e.g. Roeder and Treat 1957) and Suga
(e.g. 1963) had a great impact on the development of
research into hearing in insects, which flourished especially in the 1970s and 1980s. Nevertheless, many new
insights have been gained during the past 10–15 years or
so about the auditory systems and acoustic information
processing in various insect groups, and new types of
ears have been discovered, for instance in the fly thorax.
Ears appear to stem from chordotonal organs and then
have diversified in the different groups with respect to
the way sound reaches the sensory cells, the number of
sensory cells and interneurones, and the central computation. The comparative approach has allowed us to discriminate between species-specific trends (e.g. frequency
processing) and general trends (e.g. organisation of the
central pathway) and to describe evolutionary developments from general chordotonal organs to specialised
ears. We have much information about the properties of
auditory receptors and thoracic neurones, although we do
not yet know the patterns of connectivity and the physio-
logical basis of specific properties. We know little about
brain neurones and processing within the brain. It is,
however, quite clear that the brain extracts temporal features that apparently cannot be discriminated by single
ascending neurones and makes the final decisions with
regard to the behaviour elicited by a signal. Therefore, a
major focus in the future will certainly be on auditory
processing in the brain. More behavioural experiments
are also needed to help us understand auditory information processing on the ethological level and to direct the
course of neurophysiological experiments.
Acknowledgements We would like to thank Rohini Balakrishnan,
Norbert Elsner, Otto von Helversen, Matthias Hennig, Reinhard
Lakes-Harlan, Axel Michelsen, Bernd Ronacher and an anonymous referee for discussions and comments on various versions of
the manuscript.
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