pollack imaizumi bio essays 99

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N e ural a nalysis of soundfre que ncy in inse c tsGerald S. Pollack * and Kazuo Imaizumi

Su mmary

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 p redators 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. BioEssays21:295303, 1999. 1999 John Wiley & Sons, Inc.

IntroductionAn important function of nervous systems is sensory process-

ing, that is, the extraction of behaviorally relevant information

from the environment. Insects provide favorable model sys-

tems 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 afterspecimen. 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 informa-

tion 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 indepen-

dently 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-

though analysis of sound frequency is important in manyinsect 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 a uditory system s

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, abdo-

mens(2).) Externally, the ear consists of a pair of tympanal

membranes, which serve as the animals physical interfacewith 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 frequen-

cies, and there is a systematic relationship between the

position of the receptor within the ear and the frequency to

which it is most sensitive,(36) similar to the tonotopic organiza-

tion 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.(810) The mechanical

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]

Re v ie w a r tic le s

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properties of the tympanal membrane and associated struc-

tures are such that different sound frequencies cause differ-

ent regions of the membrane to vibrate most strongly.

Auditory sensilla attach at different sites on the membrane,

and thus receptor neurons acquire different frequency sensi-

tivity. In crickets and katydids, however, the tympanum

responds in a spatially uniform way with respect to sound

frequency.(1114) 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 evi-

dence. 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 efficientlystimulated 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

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 struc-

tures 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 ofthis brief review. However, several more thorough discus-

sions 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 similari-

ties 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. 1BE). 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

frequencies.(1)

The remainder of this review presents a few

examples that illustrate how sound frequency affects behav-

ior, and how it is analyzed in the nervous system.

Frequency analysis in ka tydids

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 frequen-

cies.(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. 830 kHz) close to its

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 theyinteract with several interneurons, some of which are shown in

BE. 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).


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source, but the higher-frequency components become in-

creasingly faint with distance. At a distance of 20 m, frequen-

cies 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 inthe central nervous system and on circuitry among interneu-

rons. 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 neurons 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 anterodor-

sal) positions(5,6,2830) (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 consideredtogether 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 recep-

tor 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 particu-

lar interneurons 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 interneu-

ron only responds to songs arising within 1015 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

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 dis-

tances (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 cells optimum distance.(31)

Another role of frequency analysis is to sharpen selectivity

for conspecific signals. The males 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 sensi-

tive 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 neverthe-

less specialized to detect and analyze frequencies in the

narrower band used for intraspecific communication.A particu-

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)


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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, AN1s 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 cricket s

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 localiza-

tion 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 wave-length of the dominant frequency in their songs (510 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 gener-

ate 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 fre-

quency.(35) They are also highly sensitive to frequencies

within the range 2550 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 to100 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

sensitivity to one or both of these frequency ranges.(4043) 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 com-

pound action potentials (CAPs), which represent the summed

extracellular potentials produced by synchronously firing

receptor neurons. CAPs evoked by cricket-like frequenciesare 45 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 ex-

pected to conduct action potentials more rapidly.(46) However,

conduction velocity does not differ between low- and high-

frequency 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 individualpotentials. 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 record-

ings. In a sample of 86 individual receptor neurons (recorded

in as many crickets), 55 were tuned within the range 45.5

kHz, whereas only 14 were tuned to 20 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 recep-

tors, and (2) how can only a few ultrasound-tuned receptors

drive behavior as strongly as a much larger number ofneurons tuned to low-frequencies?

Why are so few receptors tuned to ultrasound?

There are no obvious functionaladvantages to detecting bat

sounds with only a few receptors while devoting many more


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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 species-

specific temporal structures of the signals, whereas the

escape response elicited by ultrasound is less selective for

temporal pattern.(48)

Responses to intraspecific signals mayalso 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 andsound-producing structures were present in the very earliest

crickets, which appeared some 250300 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) andprovides inhibitory input to a number of contralateral targets,

including its mirror-image partner. ON1 enhances bilateral

auditory contrast, thereby facilitating the crickets determina-

tion of the direction of the sound source.(5456) ON1s fre-

quency 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 excita-

tory 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

Figure 3. Unequal representation of cricket-like and bat-like

soundsin 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-likefrequency (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 contrib-

uting receptor neurons.(44)


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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 actionpotential 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

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 interneu-

ron, 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 timingof the EPSPs. If the same small population of receptors is

responsible for the responses of both interneurons to ultra-

sound, 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 neurons den-dritic 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 attenu-

ation by the passive electrical properties of the postsynaptic

cell and would thus have a greater influence on ON1s

behavior. Recent anatomical studies have begun to address

this possibility.

Unlike katydids, in which receptor neurons form a continu-

ous 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 monosyn-

aptic connections with the interneurons.(58,59)(Fig. 4C). Prelimi-

nary 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 ana-

tomical type terminate in essentially the same region, making

differential passive filtering of their inputs unlikely (Fig. 5A).

The second anatomical type, comprising the remaining low-

frequency receptor neurons, has a characteristic bifurcating

projection that has little or no overlap with the dendrites of thebest 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

Figure 4. Difference in excitatory postsynaptic potentials

(EPSPs) evoked by cricket-like and bat-like sounds. A: EP-

SPs evoked in omega neuron 1 (ON1) by cricket-like stimuli

arerelatively smooth andare gradedin 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 actionpotentials in the auditory nerve

(bottom trace). This figure was prepared by aligning succes-

sive segments of the recording according to the timing of theEPSPs, 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 record-

ings 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 traceshows 23 superim-

posed 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, revealingtemporal coupling of spikesin the twoneurons.


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low-frequency receptors may lie in differences in the design ofthe afferent circuitry.(61)

Another part of the explanation may reside in the cellular

properties of the receptors. Sensory terminals are character-

ized by numerous swellings, or varicosities, which are be-

lieved to be sites of transmitter release. Preliminary data

indicate that receptors that are tuned to ultrasound have more

varicosities than those tuned to low-frequencies, (60) suggest-

ing 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 2030% higher for

ultrasound receptors.(47) This too might enhance their influ-

ence 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. Al-

though 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. Naturalselection 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.

Ackn o wled g men ts

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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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, ifany, branches that overlap with the dendrites of the well-described

auditory interneurons. C: Confocal reconstruction of a low-

frequency receptor of the type shown in B (green) and of

processes of omega neuron 1 (ON1) (red), shown in horizon-

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