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Neural analysis of sound
frequency in insects
Gerald S. Pollack* and Kazuo Imaizumi
Summary
Insects, like other hearing animals, must extract information from the sounds they
hear so that they may respond appropriately. One parameter of sound that carries
information is its frequency content. Insects analyze sound frequency to identify
mates, to judge the distance to potential competitors, and to detect predators and
prey. We review how frequency is analyzed in the insect nervous system, focusing
on two taxa in which this problem has been studied most intensively, katydids and
crickets. BioEssays 21:295–303, 1999. r 1999 John Wiley & Sons, Inc.
Introduction
An important function of nervous systems is sensory processing, that is, the extraction of behaviorally relevant information
from the environment. Insects provide favorable model systems for studying sensory processing, for a number of
reasons. First, they offer the usual advantage of invertebrate
model systems: relatively few neurons, many of which are
‘‘identifiable.’’ An insect nervous system may contain a few
hundred thousand neurons (and a single segmental ganglion,
which is often the appropriate level of analysis, may have only
a few thousand), whereas a mammalian brain contains
billions of neurons. Moreover, many of the neurons of insects
can be identified by their physiology and anatomy as unique
cells that can be recognized and studied in specimen after
specimen. Second, many behaviors of insects are tightly
related to specific sensory inputs in a robust manner, allowing
one to formulate clear hypotheses about the sorts of information processing that might be taking place. Third, insects are a
highly diverse group in which sensory capabilities have
evolved repeatedly; hearing, for example, has arisen independently at least 14 times.(1) This diversity provides a rich
source of material for a comparative approach that can help
demonstrate how neural circuits are shaped by natural
selection.
In this review we examine the neural processing of one
important feature of auditory stimuli, sound frequency. Al-
Department of Biology, McGill University, Montreal, Canada. Funding
agency: NSERC; Funding agency: Whitehall Foundation.
*Correspondence to: Gerald S. Pollack, Department of Biology, McGill
University, 1205 Doctor Penfield Avenue, Montreal QC H3A B1,
Canada. E-mail: [email protected]
BioEssays 21:295–303, r 1999 John Wiley & Sons, Inc.
though analysis of sound frequency is important in many
insect groups, this problem, and in particular its relationship
to behavior, has been studied most thoroughly in Ensifera, a
suborder of Orthoptera that includes katydids (Tettigoniidae)
and crickets (Gryllidae). These insects will form the focus of
this review.
Ensiferan auditory systems
The ears of ensiferans are situated on the front pair of legs.
(Insect ears occur in a variety of locations that seem strange
from a vertebrate perspective, e.g., wings, mouths, abdomens(2).) Externally, the ear consists of a pair of tympanal
membranes, which serve as the animal’s physical interface
with its auditory world. Sound causes the thin membranes to
vibrate, and these vibrations are passed on to a population of
sense organs, called scolopoid sensilla, which are the basic
units of hearing. Each scolopoid sensillum consists of a
receptor neuron and several accessory cells, and the ear
includes a few dozen sensilla arrayed along the length of the
leg (Fig. 1A).
A single receptor is most sensitive, or ‘‘tuned,’’ to a
particular sound frequency (see Fig. 2B, for examples).
Different receptors may be tuned to different sound frequencies, and there is a systematic relationship between the
position of the receptor within the ear and the frequency to
which it is most sensitive,(3–6) similar to the tonotopic organization of frequency sensitivity along the basilar membrane of
the vertebrate cochlea.(7)
What determines the frequency sensitivities of different
receptors? In some insects, notably mole crickets (which are
also ensiferans) and locusts, the underlying mechanism
resides in the tympanal membrane itself.(8–10) The mechanical
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Figure 1. Ensiferan auditory systems. A: Auditory receptors
are arrayed along the surface of a tracheal branch in the
prothoracic tibia.(16) The ear of a katydid is illustrated, but
cricket ears are similar in overall structure. The receptor
neurons project to the prothoracic ganglion, where they
interact with several interneurons, some of which are shown in
B–E. B,C: Ascending neurons from a cricket(65) (B) and a
katydid(31) (C). Both neurons are named ascending neuron 1
(AN1). D,E: Local interneurons of a cricket(65) (D) and a
katydid(30) (E). Both neurons are designated omega neuron 1
(ON1).
properties of the tympanal membrane and associated structures are such that different sound frequencies cause different regions of the membrane to vibrate most strongly.
Auditory sensilla attach at different sites on the membrane,
and thus receptor neurons acquire different frequency sensitivity. In crickets and katydids, however, the tympanum
responds in a spatially uniform way with respect to sound
frequency.(11–14) Moreover, the scolopoid sensilla do not
attach directly to the tympanal membrane. Instead, sound
energy is transmitted to them through internal membranes
and air cavities,(15,16) the mechanical properties of which are
unknown. There are two main views about how individual
receptors become tuned, each with some supporting evidence. One is that the mechanics of the inner ear as a whole
(i.e., the membranes, air cavities, etc.) respond in a spatially
nonuniform way to sounds of different frequencies, so that, for
example, one end of the structure would be most efficiently
stimulated by high sound frequencies, and the other by lower
frequencies.(17) This sort of mechanism is similar to what
occurs in the inner ears of higher vertebrates, where the
mechanics of the basilar membrane results in a spatial
separation of sound frequencies along its length.(7) The
alternative view is that the tuning of each receptor neuron is
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determined by factors intrinsic to the scolopoid sensillum in
which it resides, rather than by the structures that deliver
sound energy to the sensillum.(18) Resolution of this issue will
require detailed measurements of the movements of structures within the inner ear as they respond to sound; such
measurements are not yet available. An extensive treatment
of the biomechanics of insect hearing is beyond the scope of
this brief review. However, several more thorough discussions of this topic are available.(8,19,20)
Although many of the acoustical details of katydid and
cricket ears are still somewhat murky, the structural similarities suggest that the ears are similar in overall operation. The
similarities extend into the central nervous system, where the
‘‘same’’ identified auditory interneurons can be recognized in
both taxa (Fig. 1B–E). It is unclear whether these similarities
of cricket and katydid auditory systems represent an instance
of homology(21) or of duplicate, but independent, evolution of
similar auditory systems from the same exaptations.(22)
Auditory behaviors of ensifera
Foremost among the sounds that ensiferans listen to are the
songs of their own species. Their songs are of course
conspicuous to humans as well, the words ‘‘cricket’’ and
‘‘katydid’’ being onomatopoeic descriptions of the songs of
particular species. Songs are used to attract mates, to induce
copulation, and to declare and defend territories.(20,23) A
second type of behaviorally relevant sound is produced by
echolocating bats, which hunt insects by emitting ultrasonic
cries and detecting the echoes that are reflected from the
bodies of their prey. Many insects, including ensiferans,
exhibit escape responses when stimulated with bat-like
sounds, which they recognize in part by their ultrasonic
(1)
frequencies. The remainder of this review presents a few
examples that illustrate how sound frequency affects behavior, and how it is analyzed in the nervous system.
Frequency analysis in katydids
One probable role of frequency analysis is estimation of
distance to the sound source. As sound propagates through
the environment, its spectrum changes. The attenuation of
sound with distance increases with sound frequency, both
because high frequencies are better blocked by small objects
between the source and target, such as twigs and leaves, and
because frictional loss of energy is greater for higher frequencies.(24,25) In the katydid species Mygalopsis marki, males
situate their territories according to their acoustical judgments
of the distances to other singing males,(26,27) and it is likely
that they make this assessment by analyzing song spectrum.
The song has a broad spectrum (ca. 8–30 kHz) close to its
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source, but the higher-frequency components become increasingly faint with distance. At a distance of 20 m, frequencies above 12 kHz are barely distinguishable from ambient
noise, even though the lower frequency components of the
song are still prominent.(28)
Neural analysis of song spectrum depends both on the
anatomical organization of the receptor neuron terminals in
the central nervous system and on circuitry among interneurons. As in most sensory systems, the central target regions
of receptor neurons are related to their positions at the
periphery. Auditory receptors form a tonotopic ‘‘map’’ in the
central nervous system, mirroring the systematic relationship
in the ear between a receptor neuron’s location and its
frequency sensitivity. The receptors terminate in a region of
the prothoracic ganglion called the auditory neuropil, where
their branches form a curved band that starts at the anterior
edge of the neuropil and proceeds posteriorly along its ventral
border, eventually wrapping dorsally around the posterior
edge and continuing anteriorly. Receptors that respond best
to low sound frequencies terminate at the anterior end of the
band and receptors tuned to progressively higher frequencies
terminate at progressively posterior (and eventually anterodorsal) positions(5,6,28–30) (Fig. 2A). This anatomical organization
provides the framework within which receptors make synaptic
connections with interneurons. Different interneurons sample
different regions of the array of receptor terminals with their
dendrites, and thus receive input from receptors tuned to
different sound frequencies.(30)
Auditory receptors differ not only in frequency tuning but
also in absolute sensitivity. Minimum thresholds of receptors
tuned to different frequencies can vary by as much as 40 dB
(Fig. 2B). When these sensitivity differences are considered
together with the distance-dependent spectrum of the song, it
becomes apparent that the tonotopic organization of receptor
terminals can also be interpreted as an odotopic map: there is
a systematic relationship between the distance from which a
song arises and the region of auditory neuropil where receptor activity is most intense (Fig. 2C). Similarly, the frequency
selectivity of interneurons can also be seen as selectivity for
songs arising from different distances. For example, a particular interneuron’s dendrites are restricted to the low-frequency
portion of the tonotopic map, and the neuron is accordingly
tuned to low frequencies. The intensity of low frequency
components in the song is low, and receptors tuned to low
frequencies are rather insensitive. Consequently, this interneuron only responds to songs arising within 10–15 m. By
contrast, another interneuron with dendrites throughout most
of the tonotopic array responds well to songs 30 m away.(31)
Perhaps the most interesting interneurons, from the point
of view of distance selectivity, are a group (of undetermined
Figure 2. Tonotopic and odotopic organization of katydid
receptor neurons. A: Drawings of parasagittal sections of the
auditory neuropil, showing the terminal branches of receptors
tuned to different frequencies, shown at right.(30) B: Threshold
tuning curves of different receptors in M. markii. Each curve
plots, for a single receptor neuron, the minumum sound
intensity (threshold) needed to excite the receptor as a
function of sound frequency. Each receptor is ‘‘tuned’’ to that
frequency at which threshold is lowest.(31) C: The effect of
distance to the source on the activation of receptors. Each
curve in the graph corresponds to a different receptor. The
sketches below illustrate the extent to which different regions
of the auditory neuropil (shown in sagittal view) are activated
by songs arising from different distances; darker areas are
more heavily activated.(31) D: Distance selectivity of three
different interneurons.(31)
size) of morphologically indistinguishable neurons similar to
that shown in Figure 1C. Even though their dendrites invade
most of the auditory neuropil, different neurons within the
group are maximally sensitive to sounds from different distances (Fig. 2D). This selectivity thus comes about not
through selective sampling of the receptor array, but instead
is ‘‘sculpted’’ by inhibitory inputs from other interneurons (as
yet unidentified) that are ‘‘tuned’’ to distances above and
below a particular cell’s optimum distance.(31)
Another role of frequency analysis is to sharpen selectivity
for conspecific signals. The male’s calling song in another
species of katydid, Ancistrura nigrovittata, has a fairly narrow
spectrum, with energy concentrated between 10 and 17 kHz.
Behavioral measurements show that females are most sensitive to frequencies in this range.(32) Thus, although a female
can hear sounds over a wider range (perhaps allowing her to
hear bats or other predators), her nervous system is nevertheless specialized to detect and analyze frequencies in the
narrower band used for intraspecific communication. A particu-
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lar interneuron, designated AN1 (Fig. 1C), is sharply tuned to
the conspecific frequency range and may play a role in tuning
the behavioral responses of females. AN1 is morphologically
similar to the distance-selective interneurons of M. marki, and
one is tempted to speculate that it may be a homologue of
these. In both species, AN1’s dendrites overlap with the
terminals of most receptor neurons and frequency selectivity
results mainly from inhibition by neurons tuned to higher and
lower frequencies.(31,33,34) It thus appears likely that similar (or
identical?) neural circuitry is used for different tasks in the two
species; distance estimation in M. markii, and selectivity for
conspecific song spectrum in A. nigrovittata.
Frequency analysis in crickets
Cricket songs are dominated by a single narrow frequency
band. This spectral purity (which is responsible for the songs’
musical quality) may be an adaptation that facilitates localization of the singer by conspecific listeners. Crickets determine
sound direction by comparing sound intensity at the two
ears.(35,36) The insects are small with respect to the wavelength of the dominant frequency in their songs (5–10 cm)
and because of this a song originating on one side can readily
diffract around the body and reach the offside ear with little or
no attenuation. Interaural intensity differences are thus too
small for accurate sound localization. Crickets solve this
problem with an acoustical trick (the operation of which is
beyond the scope of this article) that works only over a very
narrow frequency range,(37) and the energy of the song is
concentrated within this range. (The localization problem is
presumably less severe for katydids, the songs of which
generally include short-wavelength components that generate larger interaural intensity differences.)
The dominant frequency in the songs of the cricket
species Teleogryllus oceanicus is about 4.5 kHz(38) and, not
surprisingly, the insects are most sensitive to this frequency.(35) They are also highly sensitive to frequencies
within the range 25–50 kHz, however, even though these are
present only at very low intensity in intraspecific signals.
These ultrasonic frequencies are used by echolocating bats,
which hunt insect prey on the wing by emitting ultrasonic cries
and analyzing the echoes reflected by the insects’ bodies.
When stimulated with ultrasound, T. oceanicus, like a number
of other insects, exhibit escape responses.(1,35) Behavioral
experiments indicate that T. oceanicus divide the entire
audible range of frequencies, which extends at least from 3 to
100 kHz, into only two frequency classes, namely low
(cricket-like) and high (bat-like) frequencies, with the border
between the two classes at around 15 kHz.(39)
The dual specialization of the auditory system to analyze
both cricket-like and bat-like sound frequencies is apparent at
the level of interneurons, most of which show enhanced
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sensitivity to one or both of these frequency ranges.(40–43) At
the level of receptor neurons, representation of the two
ranges is heavily skewed in favor of cricket-like stimuli.
Recordings from the whole auditory nerve consist of compound action potentials (CAPs), which represent the summed
extracellular potentials produced by synchronously firing
receptor neurons. CAPs evoked by cricket-like frequencies
are 4–5 times larger than those evoked by ultrasound,
suggesting that cricket-like frequencies excite more
receptors(44)(Fig. 3A). A difference in CAP amplitude could
also arise, however, if extracellular potentials were larger for
low-frequency receptors, as would be the case if they had
larger-diameter axons.(45) Larger axons would also be expected to conduct action potentials more rapidly.(46) However,
conduction velocity does not differ between low- and highfrequency CAPs (Fig. 3B), ruling out this explanation for the
difference in their amplitude. Another possible explanation is
that receptors that respond to low frequencies might be more
tightly synchronized than those responding to ultrasound,
resulting in more efficient summation of their individual
potentials. If this were the case, low-frequency CAPs would
be expected to be shorter in duration, but they are not (Fig.
3C). The difference in CAP amplitude thus arises simply
because more receptors respond to low frequencies than to
ultrasound. This conclusion is supported by single-unit recordings. In a sample of 86 individual receptor neurons (recorded
in as many crickets), 55 were tuned within the range 4–5.5
kHz, whereas only 14 were tuned to ⱖ20 kHz.(47) Thus,
although more than 80% of the neurons were tuned to one or
the other of the two behaviorally relevant ranges, four times
as many were tuned to the lower range.
The numerical imbalance in receptors tuned to cricket-like
and bat-like sounds is at odds with the equally robust
behavioral and interneuronal responses to these stimuli.
Crickets perform positive phonotaxis (locomotion toward the
sound source) when stimulated with conspecific songs, and
negative phonotaxis (locomotion away from the sound source)
when stimulated with ultrasound.(35) Both responses are
strong and reliable (although the threshold for negative
phonotaxis is somewhat higher), and there is little hint of a
four- to fivefold difference in the numbers of sensory neurons
involved. Two main questions arise from this situation: (1)
why are these two ranges represented unequally by receptors, and (2) how can only a few ultrasound-tuned receptors
drive behavior as strongly as a much larger number of
neurons tuned to low-frequencies?
Why are so few receptors tuned to ultrasound?
There are no obvious functional advantages to detecting bat
sounds with only a few receptors while devoting many more
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Figure 3. Unequal representation of cricket-like and bat-like
sounds in cricket ears. A: Compound action potentials (CAPs)
recorded from the auditory nerve are larger for stimuli with a
cricket-like frequency (4.5 kHz) than for those with a bat-like
frequency (30 kHz). Numbers to the left indicate stimulus
intensity relative to threshold.(44) B: Conduction velocities of
CAPs are similar for the two frequencies, indicating that the
difference in their amplitude is not due to differences in axon
diameter.(44) C: CAPs evoked by 4.5 kHz (solid line) and 30
kHz (dashed line) are similar in duration, indicating that the
difference in amplitude (note scaling factors) is not due to a
difference in the degree of synchronization among the contributing receptor neurons.(44)
to encoding intraspecific signals. Both tasks present similar
problems, namely detecting, recognizing, and localizing the
stimulus, and one might expect that these could be better
accomplished with more rather than fewer receptors, if only
because a larger number of receptor neurons would allow
greater dynamic range and increased signal-to-noise ratio.
Analysis of intraspecific signals does appear to be more
demanding than bat detection, however, perhaps accounting
in part for the differing numbers of receptors involved. For
example, behavioral responses to cricket song, in addition to
showing frequency selectivity, are tuned to the speciesspecific temporal structures of the signals, whereas the
escape response elicited by ultrasound is less selective for
temporal pattern.(48) Responses to intraspecific signals may
also be oriented more precisely than escape responses.
Although no direct comparison of the directional accuracy of
these two responses is yet available, experiments on other
model systems suggest that escape responses may be less
precise than target-oriented behaviors.(49) Direct evidence
that the sensory requirements to detect and evade bats are
minimal is provided by some moths, which accomplish this
with only a single receptor neuron in each ear.(50) So, one
reason for the small number of ultrasound receptor neurons
in crickets may simply be that only a few receptors are
needed to get the job done.
Another reason may be the different evolutionary histories
of listening to conspecifics and listening to bats. Ears and
sound-producing structures were present in the very earliest
crickets, which appeared some 250–300 million years
ago.(21,51,52) Hearing in crickets has thus been associated with
intraspecific communication throughout the entire course of
this long evolutionary history. Bats, however, appeared only
about 50 million years ago.(53) Selective pressure to detect
and respond to bat cries thus arose relatively recently and
must have been incorporated into a system that was already
highly specialized for the analysis of intraspecific signals.
One can imagine that this was accomplished by coopting
some of the preexisting circuitry for this new task, and
perhaps only a few receptors could be ‘‘spared’’ for this.
How do only a few ultrasound receptors drive
behavior as strongly as many low-frequency
receptors?
That a small number of ultrasound-tuned receptors can
influence behavior as strongly as a much larger number that
are tuned to low frequencies implies that each ultrasound
neuron must ‘‘speak more loudly’’ to central neural circuits.
Recent studies on an identified interneuron, ON1, have
confirmed that this indeed takes place.
The ON1 neurons (Fig. 1D) exist as a bilateral pair in the
prothoracic ganglion. Each neuron receives auditory input on
one side (the side on which its cell body is located) and
provides inhibitory input to a number of contralateral targets,
including its mirror-image partner. ON1 enhances bilateral
auditory contrast, thereby facilitating the cricket’s determination of the direction of the sound source.(54–56) ON1’s frequency sensitivity mirrors that of behavioral responses,(41)
suggesting that it receives input from the entire array of
receptors.
Although ON1 responds strongly to both cricket-like and
bat-like sounds, recordings of its membrane potential show
that the underlying physiological events differ for the two
frequency ranges.(57) Cricket-like frequencies evoke excitatory postsynaptic potentials (EPSPs) with smooth waveforms
that increase in amplitude in a graded manner with increasing
stimulus intensity (Fig. 4A). Ultrasound, by contrast, evokes
trains of large, discrete EPSPs that increase in frequency with
increasing intensity (Fig. 4B). A simple hypothesis to account
for this difference in waveform is that the EPSPs evoked by
low frequencies are compound responses, formed by the
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Figure 4. Difference in excitatory postsynaptic potentials
(EPSPs) evoked by cricket-like and bat-like sounds. A: EPSPs evoked in omega neuron 1 (ON1) by cricket-like stimuli
are relatively smooth and are graded in intensity.(57) B: Bat-like
sounds elicit summating trains of large, discrete EPSPs.(57) C:
Large, ultrasound-elicited EPSPs (top trace) are preceded,
with constant latency, by action potentials in the auditory nerve
(bottom trace). This figure was prepared by aligning successive segments of the recording according to the timing of the
EPSPs, and then averaging across these segments. A total of
770 segments of recording were averaged, derived from
responses to a series of 50-dB, 30-kHz stimuli (G. Pollack,
unpublished observations). D: Temporal coupling of spikes in
two ultrasound-sensitive interneurons. Extracellular recordings were made both from omega neuron 1 (ON1) (top two
traces) and from another identified interneuron, ascending
neuron 2 (AN2) (bottom trace), in response to both 5-kHz and
30-kHz stimuli.(57) The traces are aligned according to the
timing of the spikes in AN2. The top trace shows 23 superimposed sweeps in a response to a 5-kHz, 100-dB stimulus. The
spikes of ON1 occur nearly randomly with respect to those of
AN2. The middle trace shows 25 sweeps in a response to 30
kHz, 90 dB. Here, ON1 spikes are clustered around those of
AN2, revealing temporal coupling of spikes in the two neurons.
summation of a number of smaller EPSPs that cannot be
resolved individually, but that the discrete EPSPs observed in
response to ultrasound are unitary responses, each resulting
from a single action potential in a single receptor neuron. The
unitary nature of ultrasound-elicited EPSPs is confirmed in by
simultaneous recordings from the auditory nerve and ON1. In
Figure 4C, the large EPSPs were used as time markers to
divide a long recording into segments, each corresponding to
a single EPSP. These segments were then aligned according
to the timing of the EPSP and averaged. The clear action
potential in the nerve recording seen in the lower trace of
Figure 4C ‘‘survives’’ the averaging because it is time-locked
to the EPSP; other events in the nerve that occur randomly
with respect to the EPSP average to zero. The constant
latency between action potentials in the nerve and EPSPs in
ON1 indicates that receptors tuned to ultrasound synapse
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directly onto ON1, and the large size of the EPSPs indicates
that these connections are powerful. Another indication of
their potency comes from comparing the timing of action
potentials in ON1 and another ultrasound-sensitive interneuron, AN2. If single EPSPs are sufficiently large to bring both
interneurons to firing threshold, the timing of action potentials
in the interneurons would be determined in part by the timing
of the EPSPs. If the same small population of receptors is
responsible for the responses of both interneurons to ultrasound, it follows that action potentials in the two interneurons
would be temporally correlated. This is in fact observed, but
only when the neurons are driven by ultrasound (Fig. 4D).
These experiments show that the paucity of ultrasound
receptor neurons is compensated by their increased synaptic
potency.
The cellular mechanisms for increased synaptic efficacy
are unknown, but several possibilities present themselves.
Perhaps the most obvious of these is differential passive
filtering of inputs from low- and high-frequency receptors. The
transmission of synaptic potentials through a neuron’s dendritic arbor is affected by factors such as the diameters and
lengths of neuronal branches. If ultrasound-tuned receptors
terminated closer to the site at which action potentials are
initiated in ON1, or if they terminated on larger-diameter
processes, the EPSPs they produce would suffer less attenuation by the passive electrical properties of the postsynaptic
cell and would thus have a greater influence on ON1’s
behavior. Recent anatomical studies have begun to address
this possibility.
Unlike katydids, in which receptor neurons form a continuous map in the central nervous system, cricket auditory
receptor neurons fall into two distinct anatomical classes.
One class terminates in a cluster of branches near the
midline, in the same region where the best known auditory
interneurons arborize most extensively (Fig. 5A). These
receptor neurons are thus well positioned to make monosynaptic connections with the interneurons.(58,59)(Fig. 4C). Preliminary data indicate that all the ultrasound-tuned receptors, and
about one-third of those tuned to low frequencies, fall into this
class.(60) Both low- and high-frequency neurons of this anatomical type terminate in essentially the same region, making
differential passive filtering of their inputs unlikely (Fig. 5A).
The second anatomical type, comprising the remaining lowfrequency receptor neurons, has a characteristic bifurcating
projection that has little or no overlap with the dendrites of the
best known auditory interneurons (Fig. 5B,C). Interestingly,
this is the most frequently encountered type of receptor,
suggesting that a substantial amount of sensory input to
auditory interneurons may come not directly from sensory
neurons but rather from interposed interneurons. So, part of
the explanation for the differing potency of ultrasound and
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varicosities than those tuned to low-frequencies,(60) suggesting that each action potential may release a greater amount of
neurotransmitter. In addition, firing rates (i.e., number of
action potentials per unit time) are about 20–30% higher for
ultrasound receptors.(47) This too might enhance their influence on interneurons.
Concluding remarks
The examples summarized illustrate a few ways in which
insect auditory systems implement the specializations that
are required to analyze behaviorally important signals. Although this review has focused on only one suborder of
insects, similar work is being pursued in other groups as well,
including grasshoppers,(30,62) mantises(63) and flies.(64) And
whereas we have focused here only on frequency analysis,
these same insect models are being exploited to study other
problems of hearing, such as the analysis of sound direction
and of the temporal structure of stimuli.(23) What ties these
various insects and investigations together is the explicit
focus on the role of the auditory system in behavior. Natural
selection operates at the level of phenotype which, in the
case of the nervous system, is behavior. Insects, with their
wide array of auditory systems, each with their own special
features that can be assigned clear behavioral functions,
provide ideal material for studying the cellular mechanisms by
which nervous systems respond to selection pressure.
Figure 5. Central projections of cricket auditory receptors. A:
All ultrasound receptors (right) and some low-frequency receptors
(left) terminate in a dense cluster of branches close to the midline,
in the same region of the auditory neuropil in which well-described
auditory interneurons arborize. B: The majority of low-frequency
receptors terminate more laterally and posteriorly, and have few, if
any, branches that overlap with the dendrites of the well-described
auditory interneurons. C: Confocal reconstruction of a lowfrequency receptor of the type shown in B (green) and of
processes of omega neuron 1 (ON1) (red), shown in horizontal view. The receptor neuron was stained with Lucifer Yellow,
and ON1 was stained with neurobiotin/Texas-Red avidin. Most of
the receptor terminals are lateral and posterior of ON1 processes.
The few receptor branches that appear to overlap with ON1 are, in
fact, situated dorsal of ON1 dendrites (G. Pollack, unpublished
observations). a, anterior; p, posterior; m, medial; l, lateral.
low-frequency receptors may lie in differences in the design of
the afferent circuitry.(61)
Another part of the explanation may reside in the cellular
properties of the receptors. Sensory terminals are characterized by numerous swellings, or varicosities, which are believed to be sites of transmitter release. Preliminary data
indicate that receptors that are tuned to ultrasound have more
Acknowledgments
We thank Dr. Zen Faulkes, Dr. Adam Wilkins and two
anonymous referees for their helpful comments. Research
not previously published was supported by grants (to G.S.P.)
from NSERC and from the Whitehall Foundation.
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