Auditory Systems in Insects - Cold Spring Harbor Monograph Archive

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Auditory Systems in Insects
Daniel Robert
School of Biological Sciences
University of Bristol
Bristol BS8 1UG, United Kingdom
Ronald R. Hoy
Department of Neurobiology & Behavior
Cornell University
Ithaca, New York 14853
E
capacity
for miniaturization. Virtually all aspects of insect biology convey the
sense of successfully uniting form and function in exquisitely small,
diverse, and sophisticated motor, sensory, and metabolic systems
(Grimaldi and Engel 2005). The ability of insects to fly in an efficient and
controlled manner well illustrates how, through evolution by natural
selection, they adapted to solve what we consider serious problems of
engineering. Insects are little marvels of “evolutionary engineering.” The
seemingly boundless ingenuity and creativity of the process of evolutionary adaptation are also reflected in the sensory systems of insects. As
we try to make clear in this chapter, hearing in insects is a sophisticated
process; understanding its fundamental mechanisms and trying to understand its evolution present many challenges but are likely to be very
rewarding.
Perhaps because insects are so small, their ears have generally been
considered to be simple compared to those of vertebrates. Anatomically,
they may be simpler, but their capacity for sound reception and processing
turns out to be remarkably elaborate (for reviews, see Fullard and Yack
1993; Hoy 1998; Robert and Göpfert 2002; Robert 2005; Hedwig 2006;
Göpfert and Robert 2007). The ears of insects can be as sensitive and acute
VOLUTION HAS ENDOWED INSECTS WITH AN EXTRAORDINARY
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D. Robert and R.R. Hoy
as their vertebrate counterparts (Webster et al. 1992; Hoy 1998). Indeed,
in some cases their feats of detection surpass the capabilities of vertebrates
(Robert and Göpfert 2002). For example, the ultrafast ears of the parasitoid fly Ormia ochracea can distinguish time differences in the arrival of
incident sound waves below one microsecond (Mason et al 2001).
It is commonly thought that insects cannot evolve large bodies, and
this has been a key constraint in the evolution of insect audition, one that
has likely fostered innovation. The laws of physical acoustics also apply
to tiny insects, of course: For them, the time it takes for a sound wave to
pass by is extremely short. Similarly, capturing sound energy with small
structures has been thought to be an inefficient process, which challenges
the coding capacity of the insect nervous system (Michelsen 1998; Robert
and Hoy 1998). Research on insect hearing has shown that insects can
hear very well and that to do this, they have unconventional yet highly
effective mechanisms (Michelsen 1998; Robert and Göpfert 2002).
The general constraints inherent to small body size were recognized
by D’Arcy Wentworth Thompson, a pioneer of quantitative and predictive life sciences who advanced the analysis of biological form and
function in mathematical and physical terms. In his seminal book, On
Growth and Form, first published in 1917, D’Arcy Thompson astutely
points out that identical structures differing by size only display vastly
different resonant behaviors, in inverse proportion to the square of
their length scale. In his words: “Structure apart, mere size is enough to
give the lesser birds and beasts a music quite different to our own [...].
A minute insect may utter and receive vibrations of prodigious rapidity;
even its little wings may beat hundreds of time a second” (D’Arcy
Thompson 1961).
Size alone constitutes a severe constraint; for insects only several
millimeters in size, sound passes by in a few microseconds or less. As
the temporal resolution of insect nervous systems is usually on the scale
of the millisecond (sometimes hundreds of microseconds; Rheinländer
and Mörchen 1979; Robert et al. 1996; Mason et al. 2001), additional
processing is required to resolve such rapid events. As has become
increasingly apparent, this processing may rely, not only on better neuronal performance, but also on innovative auditory mechanics (Robert
and Göpfert 2002). For insects, life goes fast, and so does the process of
sensory perception. In the passage of his works on hearing and size,
D’Arcy Thompson commented: “Far more things happen to [the insect]
in a second than to us; a thousandth part of second is no longer negligible, and time itself seems to run a different course to ours” (D’Arcy
Thompson 1961).
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Herein we discuss the capacity of insects to detect sound. The general
issues associated with the detection of sound are briefly presented. We
discuss directional hearing and active audition, and we consider how
active processes facilitate acoustic detection by insects.
FORM AND FUNCTION IN INSECT HEARING
In insects, hearing is used for tasks such as finding mates and hosts, and
avoiding predators (Hoy and Robert 1996; Yager 1999; Hedwig 2006). The
literature is plentiful on the structure (Field and Matheson 1998; Yack
2004), neurobiology (Hennig et al. 2004), and molecular genetics of
insect hearing (Kernan and Zuker 1995; Jarman 2002; Todi et al. 2004),
but our understanding of the mechanical characterization of the hearing
process is still sketchy (Robert and Göpfert 2002). To date, no auditory
system, insect or other, has been fully characterized in its mechanical
details. The gap in knowledge is significant, because hearing involves a
chain of events in which mechanical and neural responses work together
intimately. This chain of events encompasses the coupling of external
sound energy, via a sound receiver—a tympanum or an antenna—to
internal mechanosensitive neurons, which respond to the energy input
(Göpfert and Robert 2003). We need to have an integrated understanding of the mechanical behavior of the sound receiver and associated
vibration-conducting structures, and how these structures interact with
the force generating mechanosensory cells.
For any animal, hearing is a sophisticated process, relying on the
delicate interplay between sound-sensitive morphological structures
and mechanically sensitive and mechanically active neurons (insects)
or hair cells (vertebrates). Little is known about the mechanical behavior of auditory neurons in insects, in contrast to vertebrate systems, for
which both in vivo and in situ studies have generated a more detailed
understanding of vibration detection by hair cells, its molecular substrate, and its genetic basis (Kernan and Zucker 1995; Ashmore and
Mammano 2001; Manley 2001; Steel and Kros 2001; Fettiplace and
Hackney 2006).
A DELICATE BUSINESS
The process of hearing is delicate because it involves mechanoreception
at very low energy levels (Thurm 1982; Bialek 1987; Hudspeth 1997).
The threshold of hearing is considered to be near the level of thermal
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noise (4 zeptojoules). Hearing and mechanosensory thresholds are at
energy levels about 100 times lower than that of a single green photon
(Thurm 1982; Hudspeth 1997). This extreme mechanical sensitivity has
made the study of audition experimentally challenging. One key question is how auditory neurons, or hair cells, can be sensitive to mechanical perturbations of such low energy. Neural thresholds for both
mechanoreception and hearing in insects were first suggested (Autrum
1948) and then measured (Adam 1972) to be reached with mechanical
displacements on the order of a tenth of a nanometer. Recent studies
suggest that mechanical perturbations of one nanometer and below are
of relevant magnitude (mosquito: Göpfert and Robert 2000; locusts:
Windmill et al. 2005).
These amplitudes are the levels of mechanical vibration of the external, peripheral auditory structures. The actual amplitude and geometry
of the mechanical deflections that insect auditory neurons experience are
not yet known, but we need to know them in order to understand cellular mechanics and, eventually, the molecular mechanisms of nanoscale
detection. These activation amplitudes and sensory thresholds are
expected to vary from one insect species to another, depending on the anatomical construction of their auditory systems and the species-specific
requirement for acoustic sensitivity. Although measurement technologies
and analytical methods have much improved in the past years, such
low levels of vibration remain challenging to measure, especially in intact
preparations.
Yet, such in situ or in vivo measurements are key to understand
fully the mechanisms of hearing and their pathologies, from the physics
of the sound receiver to the biophysics of the molecular machinery constitutive of the cellular sensors and actuators. Much uncertainty still
remains in our knowledge of the chain of neuromechanical events
underlying hearing; outstanding research challenges include the characterization of the flow of vibration through an ear, identifying the molecular machineries sensing and generating vibrations, and, ultimately,
understanding the relation between form and function in hearing, at the
microscale and nanoscale levels. A synthetic explanation of hearing will
encompass an understanding of the systemic, cellular, and molecular
organizations and dynamics of the auditory organ (Ashmore and
Mammano 2001; Gillespie and Walker 2001; Gillespie et al. 2005). One
specific key challenge is the dissection of the neuromechanical machinery
that underpins sensitivity and frequency selectivity. What are the dynamic
mechanisms that allow a cell, buffeted by thermal noise and metabolic
activities such as respiration or locomotion, to be sensitive to mechanical
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perturbations that can be about five or six orders of magnitude smaller
than itself?
STRUCTURAL DIVERSITY OF INSECT EARS
Morphologically, the ears of insects come in two basic forms: the tympanal ears, and the flagellar ears. Tympanal ears are defined by a thin,
external membrane, a tracheal air sac behind this membrane, and a
mechanosensory organ transducing the membrane’s vibrations. The
flagellar ears rely on a fundamentally different anatomy. They are antennae or hair shafts that can sway from side to side under the action of an
incident sound wave. The mechanosensory organ is at the base of the
antenna or hair.
One immediately obvious difference between the auditory systems of
vertebrates and insects is the location of the sound receivers: Vertebrate
ears are invariably located on the head, a legacy of the evolution of hearing in fish (Webster et al. 1992); in insects, tympanal ears can be found
anywhere on the body (Fullard and Yack 1993). Tympanal hearing organs
have been found on any of the thoracic segments (moths, scarab beetles,
mantises, and parasitoid flies), on the prothoracic legs (in bush and field
crickets), at the base of the wings (hedylid butterflies, lacewings), on the
first abdominal segments (grasshoppers, tiger beetles), or on any (except
the last) of the abdominal segments (van Staaden and Römer 1998; for
reviews, see Yack and Fullard 1993; Hoy and Robert 1996; Yager 1999;
Yack 2004).
It is thought that ears may have evolved independently at least
15 times in insects (Hoy and Robert 1996; Yager 1999). Interestingly, tympanal ears have not been found so far in some ecologically important
insect orders, such as hymenoptera and odonata. In some insects, tympanal
ears can be relatively simple anatomically: For example, those of noctuid
moths (Fig. 1A) comprise only two auditory neurons, yet they are capable of sophisticated sound detection, adapting to local circumstances to
enhance sensitivity (Windmill et al. 2006).
The less well-known flagellar ears rely on an antenna-like or hair
structure to capture sound (Fig. 1B–D) (Johnston 1855; Fletcher 1978;
Tautz 1979). In ears of this kind, sound-induced vibrations—air movements—are detected by mechanosensory cells situated at the base of the
antenna or the hair borne on the cuticle. In Drosophila, for example,
the mechanoreceptive organ, Johnston’s organ (Johnston 1855), resides
in the pedicel of the antenna (Fig. 1B) (Eberl 1999). In culicid mosquitoes (Fig. 1C,D), Johnston’s organ is situated at the base of the
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Figure 1. The two basic types of ears in insects: The tympanal ears present a thin
membrane backed by an air-filled cavity and a mechanoreceptive organ. Nontympanal ears use a hair or an antennal shaft to capture sound energy. (A) Internal
view of one of the “simplest” ears known, that of the noctuid moth, comprising only
two mechanosensory cells. Arrow points to the sensory cells connecting to the
tympanal membrane. Modified from an original scanning electron micrograph
(SEM) by H. Ghiradella. (B) The antennal hearing apparatus of Drosophila
melanogaster. The pedicel (arrow) is the site of the mechanoreceptive Johnston’s
organ, containing 150 – 200 scolopidia (Sivan-Loukianova and Eberl 2005) (Ar)
Arista. The red dot indicates the site of the laser interferometric mechanical measurement reported in Fig. 3 (SEM: D. Robert and R. Porter). (C) Close-up of the
pedicel (arrow) containing Johnston’s organ in mosquitoes. (SEM: H. Kohler and
D. Robert). (D) The auditory antenna of T. brevipalpis. Arrow shows the pedicel. The
red dot at the tip of the antenna is the site of laser Doppler vibrometric measurement.
(Scanning light micrograph by D. Huber and D. Robert). Bars, 200 µm.
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antennal shaft and contains some 15,000 scolopidial cells, about as
many as there are hair cells in the human cochlea, but in a volume
~100,000 times smaller. Mosquito ears may be the most complex found
in insects.
Specialization for hearing seems to be extreme in culicidae, toxorhynchinae, and chironomidae Diptera, but actually, more than 95% of
insect species are endowed with Johnston’s organ at the base of their
antennae (Kristensen 1981). Not all of these species can necessarily hear
using their antennae, but certainly, many have the potential to do so. The
evolutionary emergence of the sense of hearing in a group that otherwise
does not possess this sensory modality is possible, if not expected. It has
been previously shown for tympanal ears in tachinid and sarcophagid
parasitoid flies (Robert et al. 1992; Robert and Hoy 1998). Antennal hearing, based on the prior presence of Johnston’s organ, may have evolved
in insect orders yet to be examined. Interestingly, recent evidence confirms the long-held suspicion (McKeever 1977) that another group of
culicid mosquitoes, the Corethrellidae midges, feeding on frogs, phonotactically find their hosts using their antennae as sound detectors (Bernal
et al. 2006; Borkent and Belton 2006).
Hairs borne on the animal’s body surface that are articulated at the
base and equipped with one or several mechanoreceptive neurons can also
act as sound or wind receivers (Fletcher 1978; Tautz 1979; Shimozawa and
Kanou 1984; Kämper and Kleindienst 1990; Barth 2000, 2004). This type
of sound receiver is very widespread among arthropods, so many more
species than previously thought, in particular spiders and crustaceans,
might have a sense of hearing, of a rather unconventional kind. A
remarkable example is that of spiders, which have extremely sensitive
mechanosensory hairs all over their bodies (Barth 2004). These hairs can
be exquisitely sensitive to small wind inputs (non-harmonic variations of
air velocity) and near-field sound (harmonic variations of air velocity),
providing information about the presence or approach of prey, mates, or
predators.
The antennal and hair-like sound receivers are sensitive to the particle velocity component of the propagating sound energy (see Box), rather
than the pressure component (Fletcher 1978). The particle velocity component is easier to detect in the vicinity of a sound source, in the so-called
near-field. Such antennal and hair receivers have thus been coined nearfield receivers, recognizing their better performance near the source of
sound. This is not to say, however, that they cannot work in the far-field
of a sound source, nor that they are not sensitive sensory organs, as
shown below.
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Acoustical Cues for Directional Hearing and Sound in the Near-field
(A) A propagating sound wave can be represented, in the case of a pure tone,
by a sinusoidal wave; for instance, representing the variation in pressure in time.
This sinusoid is characterized by an amplitude (i.e., peak to peak), a frequency
(the inverse of the period T), and a direction of propagation. In air, sound waves
propagate at ~343 m/s for normal temperature (20°C) and humidity (20% RH)
conditions. Owing to this speed of propagation, the auditory receiver nearer to
the sound source, the ipsilateral ear, detects the sound wave earlier than the
ear farther from the sound source, the contralateral ear. This interaural time difference (ITD), shown here as the time (or phase) delay between two sinusoid
waves (∂t), amounts to ~1.5 10-6 s for an interaural distance (ID) of 5 10-4 m,
such as that of the fly Ormia. Passing by and around a solid body, a sound wave
also undergoes diffraction if the ratio between the acoustic wavelength and the
size of the solid is about 10:1 or smaller. In diffractive conditions, the sound
input to the contralateral ear is attenuated, yielding a reduction in the amplitude of the wave (∂A). This is the other cue for directional hearing, the interaural intensity difference, IID.
(B) The interaural time difference as a function of the azimuthal angle of incidence. For a sound source reaching the subject at 90° off the midline, the difference in the time of arrival at the ears is 500 µs and 1.5 µs, for humans and
flies, respectively. This time decreases as the sine of the angle of incidence.
For the fly Ormia, azimuthal angles below ~45° result in submicrosecond ITDs.
Such sinusoidal relationship between azimuthal angle and ITD is an approximation; in diffractive condition, the geometry of the auditory organs, as well
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as the size and density of the body part on which they are borne, influences
the actual ITD.
(C) Attenuation of sound as a function of distance from a flying female mosquito (data from Jackson and Robert 2006). Fitted attenuation function is f(x)
= 1/x3. A large proportion of the sound intensity, measured as particle velocity, is lost already some 15 mm away from a flying female. In a sound wave,
acoustic energy is embedded in the pressure (p) and the particle velocity (v) such
that p = Zv, where Z is the acoustic impedance of the medium (413N•s/m3).
Such relation is the acoustic equivalent of Ohm’s law in electricity. The overall intensity (Watt/m2) of sound is I = pv (I = Zv2 = p2/Z). In the close vicinity of a sound source, particle velocity dominates the overall sound intensity,
whereas farther away, typically several wavelengths from the source, pressure
dominates (Olson 1942). Particle velocity decays as a function of the inverse
cube of the distance x from the source (x–3), whereas pressure does so as the
inverse square (x–2). As a consequence, particle velocity receivers, such as antennae and hairs, are best suited to detect sounds close to the source.
THE HOW AND WHY OF HEARING IN INSECTS
Like vertebrates, many insects use their hearing organs to explore and
exploit their environment in space and time. Insect ears have to accomplish the same task as vertebrate ears: to detect and encode at least one
or a combination of the three fundamental physical parameters of
sound (see Box): its frequency, intensity, and direction of propagation
(Rayleigh 1876). Although these parameters were identified early
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on, the mechanisms subtending their detection are still not fully
understood.
First, an animal’s ears must be responsive to behaviorally and ecologically salient signals in the acoustic frequency spectrum. The range of
detectable frequencies can greatly vary; for human ears, it is from about
20 Hz to 15 kHz, but for certain Meconematinae neotropical bush crickets, it goes up to 129 kHz (Montealegre-Z et al. 2006). The frequency
selectivity of an ear is determined by a combination of physical and physiological mechanisms working in concert. In vertebrate ears, the tuning
is partly determined by the passive mechanical response of the cochlea
(von Békésy 1960), but the usual exquisite sensitivity and frequency selectivity require supplementary active work by hair cells (Hudspeth 1989,
1997; Dallos 1992; Manley 2001; Robles and Ruggero 2001). The interplay between passive and active mechanisms in insects and their behavioral relevance are just beginning to be unveiled; the current knowledge
is presented below in this chapter.
Second, an animal’s ears must be sufficiently sensitive to impinging
sound waves with vanishingly small energies. High sensitivity is made
possible by the active participation of mechanosensitive cells, a process
that is thought to counteract viscous damping and/or to modulate the
effective stiffness of the sound receiver. The mechanisms boosting the
ear’s sensitivity, generally referred to as active hearing, have been the subject of much attention in vertebrates (Hudspeth 1997; Nobili et al 1998;
Manley 2001; Robles and Ruggero 2001). In insects, the evidence for
active mechanisms in mechanoreception (Moran et al. 1977) and hearing (Kössl and Boyan 1998a,b; Göpfert and Robert 2001, 2003) has been
rare, and only recently have remarkable similarities to vertebrates been
reported.
Third, for most insects, the ability to localize a sound source is
behaviorally important. In insects, directional hearing can be achieved
in several ways by detecting timing and intensity differences between
the auditory receptors (Robert 2005). Vertebrates derive directional
information from diffractive effects on the spectral composition of
sound (Wightman and Kistler 1997). This has not yet been reported
in insects, but the possibility for it exists because, for an insect with a
1-cm body size, frequencies larger than 10 kHz are sufficient to generate diffraction (Olson 1943) and the interaural differences needed
for directional hearing (Michelsen 1998; Robert et al. 1999). Sensing
the direction of a sound source is particularly challenging for small
animals because the cues involved—the time and intensity differences
at the two ears—decrease dramatically with decreasing body size (see
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Box). What solutions have insects evolved to solve the problem of
directional hearing?
Insects have been particularly creative, evolutionarily speaking, in
generating a rich diversity of auditory morphologies, each with distinct
processing mechanisms solving the problem of directional hearing with
a small body size (Michelsen 1998; Robert 2005). The apparent evolutionary constraint on insect body size has fostered the development of
unique auditory mechanisms, such as acoustically or mechanically coupled receivers. As shown in the following section, these mechanisms allow
very small ears to function like large ones.
CHALLENGES OF DIRECTIONAL HEARING
Detecting the direction of incoming sound waves presents particular
challenges for small animals (Michelsen 1998; Robert 2005). We consider
two insect species, field crickets and parasitoid flies, which have evolved
very distinct biomechanical solutions to the problem of directional hearing (Robert et al. 1996). Field crickets are conspicuous singing insects
(Hedwig 2006): To attract females for mating, males produce chirping
and trilling calling songs, which the females hear, locate, and home in on.
The calling signals of males are essential to their reproductive success,
and call conspicuousness, achieved by high sound intensity, enhances
mating opportunities (Farris et al. 1997). But the males are acoustic beacons, and are detectable not only by conspecific females, but also by parasitic flies, such as the tachinid Ormia ochracea, which rears its larvae
within the body of their obligatory cricket host, Gryllus bimaculatus
(Cade 1975). Female crickets and female Ormia flies thus face the same
auditory task: that of detecting the mating call with high sensitivity and
localizing it precisely (Robert et al. 1992).
The mating call of G. bimaculatus is a series of brief (25 ms), tonal
amplitude-modulated sound pulses (4.8 – 5 kHz dominant frequency),
delivered as continuous trills (repeated at 35–40 Hz) lasting from 0.5 second
to several seconds (Cade 1976). Such an acoustic signal is easily detectable
by the human ear, yet personal fieldwork experience shows that even for
humans, determining its direction in the grassy vegetation is no trivial
feat; neither is it for female crickets or parasitoid flies. Biomechanical
studies on sound localization in crickets and Ormia flies have revealed
critical differences in the mechanisms employed. Crickets localize sounds
by using pressure difference acoustic receivers and by comparing binaurally
the outputs of each of the acoustically coupled hearing organs (Michelsen
1998). Ormia flies take a different approach, based on mechanical coupling
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Figure 2. SEMs comparing the prosternal anatomy of the tympanate Ormia ochracea
(Tachinidae) (A) with that of the atympanate Musca domestica (Muscidae) (B). The
prosternal membranes are conspicuously more developed in the tympanate fly and
are connected by the presternum, an unpaired sclerite endowed with some rigidity.
This structure is responsible for the mechanical coupling between the ears and hence
the fly’s capacity for directional hearing. Notably, the presternum is present in both
species; in Ormia it extends laterally. The apodemes linking the chordotonal organs
to the prosternal membranes attach at the lateral flanges of the presternum (arrows
in A and B). Abbreviations: (CvS) cervical sclerites; (N) neck; (PM) prosternal
membrane; (Pr) presternum; (Pb) probasisternum; (Cx) prothoracic coxa. Bars,
200 µm. (SEMs courtesy of E. Tuck and R. Porter.)
between the tympanal membranes of two adjacent hearing organs (Fig. 2)
(Robert 2005). Such intertympanal mechanical coupling has not been
reported to date in organisms other than flies. As an evolutionary innovation (Edgecomb et al. 1995), intertympanal coupling is considered to
be a consequence of the very small size of the flies compared to the wavelength of the sound they have to detect (Miles et al. 1995; Robert et al.
1996; Robert and Hoy 1998; Robert 2001).
In crickets, the first stage of tympanal hearing—bringing a membrane into vibration under the action of sound pressure—is achieved
using a sophisticated modified tracheal system to conduct sound across
the body. As sound travels into the animal’s respiratory system, the two
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sides of each tympanal membrane are exposed to sound pressure. These
ears are called pressure-difference receivers, and the tympanal membrane
is the first site of processing, where the difference of pressure, the net
force across it, is “computed.” This computation is possible because the
acoustic pressure field acting on the opposite sides of the tympanal membrane, the external and internal surface areas, generates a harmonic force
of opposite sign. These forces can greatly differ in magnitude and phase.
If the driving forces have opposite sign but equal amplitude and phase,
there is no difference force, so the membrane does not enter harmonic
motion. Forces that are out of phase efficiently drive the membrane; the
characteristics of tracheal sound transmission are thus crucial in determining the driving force to the auditory system (Michelsen and Rorhseitz
1995; Michelsen 1998; Robert 2005).
Pressure-difference receivers are usually bilaterally acoustically coupled,
rather than mechanically coupled, and these are most notably found in
crickets, bush crickets, and locusts (Miller 1977; Michelsen and Rohrseitz
1995; Michelsen 1998; Schul et al. 1999). A well-balanced pressure-difference
auditory receiver system needs to maximize constructive interference on
the side of the animal closer to the sound source, and to minimize it on
the other, contralateral side. This process is quite likely to be frequency
dependent, as transmission through small tracheal tubes affects the velocity
of wave propagation and frequency bandwidth (see also Bangert et al. 1998;
Schul et al. 1999). In crickets, the tympanal membrane does not directly
connect to the chordotonal organ containing the mechanosensory cells.
However, the role played by the tympanal membrane in generating the
actual mechanical drive to the mechanosensory organ remains unclear.
Ormia flies possess a pair of hearing organs that, because the fly is
so small, are set close together (Fig. 2): The distance between them is just
0.5 mm, compared to ~15 mm in crickets and ~180 mm in humans. The
ears are so close together in Ormia that, even in the best scenario—when
the sound comes from one side of the animal, at 90° angle from the
midline—the time it takes for a sound wave to pass from one ear to the
other is a mere 1.5 x 10–6 seconds (see Box). For humans, the maximal
interaural time difference is ~500 x 10–6 seconds, whereas the shortest
times that can be resolved binaurally are in the range 4 x 10–6 to 8 x 10–6
seconds, representing a deviation by the sound source of 1–2° from the
midline (Middlebrooks and Green 1991; Wightman and Kistler 1993).
How short is the smallest resolvable interaural time difference in flies,
where the interaural distance is about 360 times smaller than that of
humans? Behavioral experiments have shown that Ormia can detect and
accurately orient toward a sound source deviating only by 2° in azimuth
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(Mason et al. 2001). Such deviation has been calculated to correspond to
time differences between the tympanal membranes of the fly of a mere
50 nanoseconds (this value may not be strictly accurate because the
acoustic interaural time differences have not been directly measured).
Thus, are flies indeed capable of detection with a temporal resolution that
would be considered fast even for electronics? Nature tends to have ways
of making things work, not necessarily the same ways used by human
engineering (Bleckmann et al. 2004). Finding its own way, the acoustic
detection system of the little Ormia fly seems to have taken the problem
apart by assigning a different task to each step in the auditory chain of
events (Robert et al. 1996).
The first and crucial step involves the mechanisms of conversion of
acoustic energy into mechanical energy. Sound energy results in the motion
of the tympanal membrane, which in turn channels mechanical energy to
the sensory neurons. For directional hearing, the essential physical quantities reaching the neurons are the phase (or timing) of the impinging sound
wave, and its amplitude. In Ormia, as mentioned above, the tympana are
anatomically linked; a flexible cuticular lever connects them across the midline of the animal (Fig. 2A). Most remarkably, when the sound of a singing
male cricket impinges on the ears of the fly, this coupled tympanal system
undergoes asymmetrical mechanical oscillations. The side nearer to the
sound source oscillates with larger amplitude and earlier than the far side.
This results in the differential activation of the mechanosensory neurons
located in the chordotonal organs linked to each of the membranes (Robert
et al. 1996; Robert 2001). Note that, if the two membranes were acting
independently from each other, like two separate microphones, the time
difference between the two sides would be only 1.45 microseconds, and no
amplitude difference would be detectable (Robert et al. 1996).
Mechanically, this asymmetrical behavior is generated by the linear
combination of two resonant oscillators. In the mode that dominates at
the frequency of the cricket song, the two tympana move out of phase
and at different amplitudes, displaying motions that are reminiscent of
the rocking of a floppy seesaw (Miles et al. 1995; Robert et al. 1996). This
system generates, for a sound delivered at 90° to the side of the animal,
a mechanical interaural time difference of 50 – 60 microseconds and a
mechanical interaural intensity difference of 3–12 decibels. The mechanical time difference at the ears is thus about 40 times longer than the
1.45-microsecond acoustical time difference.
There is thus an amplification of the acoustic cues which converts small
acoustical cues into much larger mechanical cues (Robert et al. 1996).
These mechanical cues are conducted from the tympanal membranes
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to the auditory neurons of the chordotonal organ. The exact manner by
which tympanal vibrations are transmitted to the chordotonal has not been
investigated in detail in flies, or in any other insect. It is possible that further mechanical processing takes place along the connecting apodemes
linking tympanal membranes to the mechanosensory neurons. But the
accuracy required in the coding of temporal events may still be in the range
of microseconds, a challenge for any auditory system (Mason et al. 2001;
Robert 2005).
Does the neuronal processing in the cricket and fly auditory systems
mirror the peripheral mechanisms in exhibiting special adaptations to
deal with the consequences of small body size? For female crickets, in the
monoaural situation, the intensity of a sound stimulus is encoded in one
of two ways. The response latency of the primary afferents decreases with
increasing sound level, and the spiking activity of each afferent increases
for each sound pulse proportionally to sound intensity (Imaizumi and
Pollack 1999; see the authoritative review by Pollack 1998).
Interestingly, the coding of intensity information can also be used to
regulate the sensitivity of the hearing process. Intracellular recordings of
an identified auditory interneuron in a singing cricket have revealed some
of the neural mechanisms that contribute to modulating and preserving
auditory sensitivity (Poulet and Hedwig 2002). The process involves both
the presynaptic inhibition of primary afferents and postsynaptic inhibition of a central interneuron—the well-studied omega neuron. The two
inhibitions appear to be phase-locked, or coincidental, with the acoustic
input from the song and were later demonstrated to be genuine corollary discharges that originate from the song generation network (Poulet
and Hedwig 2006). Collectively, the work on crickets illustrates the
sophistication of the peripheral mechanical and neural processing in
insect auditory systems and their integration in the behavioral and sensory
ecology of the species (Hedwig 2006).
In female Ormia flies, the afferent activity shows an additional type
of response related to stimulus intensity. Over half of the afferents recorded
as single units exclusively encode sound intensity by the conventional
quasi-exponential decay relation between latency and increasing intensity.
Remarkably, some afferents in the fly auditory organ never discharge more
than a single spike per stimulus cycle (Oshinsky and Hoy 2002). Such
latency-only coding of sound level in single-spiking afferents has never
been reported in the afferent responses of crickets or other insects.
Other primary afferents recorded in the same preparation were
shown to exhibit spike recruitment and modulation of the tonic discharge
as a function of intensity. The single-spiking behavior of the primary
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mechanoreceptive afferents, and its repeatable accuracy, are especially
interesting in light of mechanisms for acute sound localization. Not only
can some primary afferents spike only once in response to harmonic
stimuli some 20 milliseconds in duration or longer, but they do so with
remarkable repeatability (Oshinsky and Hoy 2002). Presented with repeating sound stimuli mimicking a cricket song, these primary afferents
respond with a consistent delay of 3164 microseconds with, remarkably, a
variation of only 95 microseconds (Oshinsky and Hoy 2002). This very
small jitter in the temporal response is consistent with the idea that these
neurons perform some sparse coding of the temporal information contained in the arrival of the sound wave at the tympanal membranes
(Mason et al. 2001). The single-spike encoding of stimulus latency has
also been interpreted as a neuronal adaptation to sound localization at
the submillisecond timescale (Mason et al. 2001). It is important to recall
here that, because of the lack of significant acoustic diffraction in Ormia,
no measurable acoustic interaural intensity differences are available
(Robert et al. 1996, 1999).
The temporal coding observed in the fly’s auditory system is reminiscent of a type of sensory processing called hyperacuity. Under such a
scheme, neural coding at submillisecond timescales, as reported to occur
in electric fish (Rose and Heiligenberg 1985) and barn owls (Knudsen
and Konishi 1979), relies on the convergence of many sensory afferents
onto an interneuron that acts as a coincidence detector. The logic is such
that only the coherent firing of an ensemble of afferents within a narrow
time window—the coincidence—can elicit interneuronal activity. For
Ormia, the very small variation in the firing times of the afferent population seems essential to generate the sort of coincidence necessary to the
binaural discrimination of acoustic events in the microsecond range. This
type of interneuronal processing cascade may explain the hyperacute
directionality observed at the behavioral level (Mason et al. 2001).
ACTIVE MECHANISMS IN INSECT HEARING
Hearing relies on the detection of nanoscale, or even picoscale, vibrations.
The inherently weak energies conveyed by propagating sound waves are
at the root of the hearing challenge; low-level sounds may often be those
that an animal should detect rapidly and reliably. For some insects, detection challenges have been identified that relate to the particularly transient nature of sounds to be detected in the near-field (Jackson and
Robert 2006). Selection pressure is likely to have favored the evolution
of ears that can detect, and localize, mate, prey, or predators with better
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sensitivity, accuracy, rapidity, and reliability, pushing the feat of detection
to its physical limits (Bialek 1987).
In hearing, these limits involve energy levels so faint as to be comparable to that of thermal noise. One of the keys to fully understanding
hearing resides in the identification and characterization of the molecular constituents and their mechanical behavior. Crucially, this needs to be
done in the physical and physiological contexts in which mechanosensory cells operate, be that at thermal noise level or just above. The investigation of that process has proved to be a formidable challenge that
has attracted sustained scientific attention and resulted in a number of
spectacular advances (Dallos 1992; Hudspeth 1997; Gillespie and Walker
2001; Robles and Ruggero 2001; Gillespie et al. 2005).
It is now widely accepted that, for both vertebrates and invertebrates,
the exquisite sensory sensitivity and frequency selectivity achieved by
auditory organs result from an active process (vertebrates: Fettiplace and
Hackney 2006; invertebrates: Göpfert and Robert 2007). Using their own
metabolic energy, the mechanosensory cells that mediate hearing generate motions that coherently enhance, and sometimes sustain, the minute
vibrations they have to detect in the first place (Hudspeth 1989, 1997).
This cellular behavior has not yet been observed at the cellular level in
an intact auditory system. In vertebrates, both motile and sensory functions are considered to be embodied in a single cell type, the outer hair
cell. In insects, whereas active mechanisms have now been shown to contribute to hearing (Göpfert and Robert 2003, 2007; Göpfert et al. 2005),
the question of the integration or segregation of function has not been
addressed.
This question naturally arises because chordotonal (auditory) organs
are known across insects to harbor several types of scolopidial
mechanoreceptors (Field and Matheson 1998; Eberl 1999; Yack 2004;
Boekhoff-Falk 2005). The mechanically sensitive unit is a scolopidium,
an assembly of several different cell types accompanied by one or more
ciliated axonemal mechanosensory sensory neurons (Yack 2004). It is
possible that, in those insects endowed with active mechanisms, different
scolopidial or neuronal types fulfil different functions. However, the
available evidence in insects seems to point to an integrated sensorymotor function (Göpfert and Robert 2007), possibly much like that
found in the outer hair cells of mammals (Fettiplace and Hackney 2006).
Active auditory mechanics manifests itself in several characteristic
ways in vertebrate hearing. First, sensitivity and tuning are metabolically
vulnerable and, thus, depend on the animal’s physiological condition.
Second, the active process introduces a nonlinearity in the mechanical
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response to sound. This response is also metabolically vulnerable; for
instance, it can be reversibly suppressed by exposure to carbon dioxide.
Third, the mechanical response of the auditory organ or part thereof displays, most compellingly, vibrations taking place in the conspicuous
absence of external acoustic stimulation. These autonomous vibrations
are known as spontaneous otoacoustic emissions in vertebrates and can
be readily recorded, when they occasionally take place, as sounds emitted by the ear (Dallos 1992; Hudspeth 1997; Robles and Ruggero 2001).
These features have been used as operational criteria to investigate the
presence and modalities of active auditory mechanics in insects. To date,
only two species have fulfilled this list of criteria: the fruit fly Drosophila
melanogaster (Göpfert and Robert 2003) and the culicid mosquito species
Toxorhynchites brevipalpis (Göpfert and Robert 2001).
What are the manifestations of active hearing in insects? In vertebrates,
active mechanisms have been shown to contribute to both sensitivity and
frequency selectivity of hearing (Hudspeth 1997; Manley 2001). In invertebrates, active mechanisms have been suggested, unveiled, and characterized only recently (Kössl and Boyan 1998a,b; Göpfert and Robert 2001,
2003; Göpfert et al. 2005) and although their function(s) first appears to
be similar, the role it plays in the auditory behavior of the animal has not
been addressed (Jackson and Robert 2006; Göpfert and Robert 2007). The
sensory ecological relevance and the species-specific function of these
mechanisms remain to be explored. The presence of these mechanisms in
insect auditory systems has opened the door to a broad range of novel
questions and renewed experimental opportunities.
Some fundamental questions arise. Do the ultimate and proximate
functions of active auditory mechanisms differ between insect and vertebrates? Given their presence in animal lineages that diverged 600 million
years ago, are the molecular substrates supporting active mechanisms
evolutionarily convergent (Boekhoff-Kalk 2005)? Or do they display a
deep-rooted legacy of an earlier evolution of cellular motility? Or is it a
seamlessly integrated mix between both? Notably, both the hair cells of
vertebrates and the scolopidial mechanosensory neurons of insects are of
ciliary origin. The phenomenological convergence of active auditory
mechanics between insects and vertebrates seen today may well reflect the
combination of fundamental properties deeply rooted in the evolution
of fluid-coupled mechanosensory systems and, complementarily, the
unavoidable biophysical constraints linked to the sensitive, accurate, and
robust detection of weak sound energy.
Looking into auditory biodiversity may provide the background
necessary to resolve these issues. Does the diverse and independent
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evolution of insect hearing organs suggest that active auditory mechanisms, should they be found in other insect species, will be commensurately diverse in structure and function? Enticingly, both ultimate and
proximate questions are finding an increasing number of detailed
answers (Boekhoff-Falk 2005; Göpfert and Robert 2007). Such issues are
also being addressed with much success in other sensory systems of
insects, most notably, olfaction (Couto et al. 2005; Hallem and Carlson
2006; see Chapter 4).
The evidence for active mechanisms in insect hearing all comes from
a series of studies on locusts and moths (Coro and Kössl 1998; Kössl and
Boyan 1998a,b), mosquitoes (Göpfert and Robert 2001; Jackson and
Robert 2006), and flies (Göpfert and Robert 2003; Göpfert et al. 2005;
2006). The studies on the mechanical behavior of antennal hearing of
mosquitoes were first to document a series of nonlinear mechanical
responses that could be unambiguously interpreted as the result of active
processes (Göpfert and Robert 2001). The use of Drosophila as a model
system for hearing (Kernan and Zuker 1995; Eberl 1999) instigated the
necessary quantum leap; the presence of tell-tale nonlinearities in
Drosophila (Göpfert and Robert 2002) meant that active auditory mechanisms could be investigated at the systemic, cellular, molecular, and
genetic levels (Göpfert and Robert 2003; Göpfert et al. 2006).
Collectively, these studies established an important fact: The origin
of the nonlinear mechanical behavior is to be found in the activity of
auditory mechanosensory neurons. The molecules involved in insect
audition also are starting to be identified (Caldwell and Eberl 2002;
Göpfert and Robert 2003; Kim et al. 2003) and for some of these
molecules—the mechanotransduction channels—their role in audition
is being progressively unveiled (Göpfert and Robert 2003; Göpfert et al.
2006). It is also apparent that several of the key molecular components
of the insect auditory (or mechanoreceptive) machinery have homologs
in the vertebrate hair cells (Walker et al. 2000; Caldwell and Eberl 2002;
Weber et al 2003).
Enticingly, in Drosophila, the molecular substrate supporting the
mechanical sensitivity to sound is beginning to be unraveled. Recent
evidence links the neuron-based generation of motion that enhances
mechanical sensitivity to the concerted actions of “transient receptor
potential” (TRP) channels (Kim et al. 2003; Göpfert et al. 2006). A recent
genetic and mechanical study has shown that the NompC3 gene, which
encodes a mechanotransduction channel protein expressed in sensory
neurons, plays a role in augmenting the gain of the antennal system, a
measure of its sensitivity to sound (Göpfert et al. 2006).
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Remarkably, the external structures of the antennal auditory system
of Drosophila, the arista (Fig. 1B), undergo prominent autonomous
vibrations, revealing the oscillations of the mechanosensory neurons of
Johnston’s organ (Göpfert and Robert 2003). In wild-type flies, such
oscillations can reach several tens of nanometers in magnitude, exhibiting a prominent power output for frequencies below about 300 Hz
(Fig. 3A). In dead or anesthetized animals, such fluctuations are much
reduced (Göpfert and Robert 2003). This vibrational signature of active
mechanisms has been shown to be useful in assessing the effects of various
mutations on the ear’s mechanics (Göpfert et al. 2005, 2006); a powerful
way of analyzing auditory function by genetic dissection (Caldwell and
Eberl 2002).
In NompC mutants, for example, the fluctuations are much reduced
and yield a power spectral density notably lower than that generated by
the wild type (Fig. 3B). Remarkably, for mutations involving the TRPV,
vanilloid channels, Nan (Nanchung) and Iav (Inactive), antennal fluctuations are observed to be enhanced, exceeding those of the wild type
(Fig. 3C) (Göpfert et al. 2006). Nan and Iav mutants exhibit an enhanced
Figure 3. Active auditory mechanics in Drosophila; unveiling the role of TRP chan-
nels. In the absence of external stimulation, the external structures of the ear, the
arista mainly (see Fig. 1B, Ar), undergo significant mechanical fluctuations that can
be measured optically by laser interferometry. (A) Time course (top panel) and spectral composition (bottom panel) of the spontaneous mechanical fluctuations in wildtype flies. (B) Absence of such fluctuations in NompC3 mutants. (C) Excess of
mechanical fluctuations in Nan mutants. (Modified, with permission, from Göpfert
et al. 2006 © Macmillan Publishers Ltd.)
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gain and power generation in their autonomous vibrations (Fig. 3)
(Göpfert et al. 2006). It was concluded by Göpfert et al. that the mechanical sensitivity of the Drosophila ear is regulated by the combined actions
of the distinct NompC and Nan-Iav channels.
In the scheme suggested, NompC3 is considered responsible for the
amplificatory process, whereas the molecular dyad Nan-Iav is involved in
controlling the amount of gain produced (Göpfert et al. 2006). These
seemingly antagonistic effects—reduction and enhancement of gain—
suggest the presence of a regulatory feedback loop, the output gain of
which is controlled by the concerted action of both types of mechanotransduction channels. Knowing the exact physical localization of these
channels and their functional positions in the auditory pathway will be
important for understanding the molecular anatomy of active auditory
mechanisms. Related to this question is that of the relationship between
neuronal signaling and neuronal mechanical power generation in these
mechanoreceptive neurons, should these functions be operating concomitantly in a single neuron.
Such studies, marrying molecular genetics and auditory mechanics,
show that it is becoming possible to dissect the chain of events down to its
molecular components and to understand, perhaps molecule by molecule,
the structure and mode of operation of the entire auditory machinery.
Likewise, comparisons with vertebrate systems will be most interesting,
contrasting the respective molecular functional constituents and establishing whether or to what extent they share an evolutionary past.
In mosquitoes, the mechanical response of the external auditory structures (the flagellum, or shaft, of the antenna) displays the tell-tale signs of
active auditory mechanism (Göpfert and Robert 2001). Analysis of the
mechanical behavior of the sensory cells, or genetics-based approaches,
have hitherto not been possible. The sound-induced mechanical response
of the antenna is resonant, resembling that of a simple harmonic oscillator and displaying a maximal response and a phase transition at resonance
frequency. This response, however, changes with stimulus amplitude. In
effect, the frequency response of the antennal sound receiver gets more
sharply tuned as the amplitude of the stimulus is reduced (Göpfert and
Robert 2001).
This nonlinear effect enhances the frequency selectivity of the antennal oscillator and also affects its sensitivity to sound. Sensitivity has been
measured as the gain of the response; that is, the mechanical output normalized by the magnitude of the sound input (Göpfert and Robert 2001).
The antennal system becomes mechanically more sensitive to sound as
sound intensity decreases. For some sound intensities, the mechanical
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response of the antenna exceeds that predicted by the acoustic input
alone, a strong indication that an active process is at work in Johnston’s
organ. This effect is physiologically vulnerable; the gain of the mechanical response does not depend on input intensity in dead or anesthetized
animals (Göpfert and Robert 2001).
This nonlinear behavior was also examined in the Tanzanian mosquito
T. brevipalpis for a broad range of varying sound intensities. Because in
nature, for mosquitoes as for any other animal, incident sound stimuli
are seldom of constant amplitude, antennal mechanics was investigated
to gradually changing sound intensities (Fig. 4), an experiment that has
rarely been conducted. A gradual, linear increase in sound intensity starting with low-level background noise was presented to the mosquito (at
380 Hz carrier frequency) as the mechanical response of the antenna was
measured by laser Doppler vibrometry (Fig. 4A). For low intensities, the
response curve shows a response for which stimulus and response are first
linearly related (Fig. 4A, zone a). As stimulus intensity continuously
increases, a significant departure from linearity can be observed (Fig. 4,
zone b), yielding an amount of mechanical displacement exceeding that
imposed to the antenna by sound alone. Further up the intensity scale
(Fig. 4, zone c), the mechanical response converges back to the linear
regime, eventually entering a compressive regime.
Such experiments show that the mechanical response is not that of a
passive oscillator and that an active mechanism enhancing acoustic sensitivity may explain such response. Interestingly, the frequency selectivity
of the antennal receiver (the mechanical oscillator) is also affected by
sound intensity (Fig. 4B). The frequency spectrum of the response gain
changes with intensity: The low-intensity response displays a relatively
broad spectrum (Fig. 4B, curve a), whereas intensities in the middle of
the range generate a sharper frequency spectrum with a higher gain
(curve b); at yet higher intensities, the response broadens up, and restitutes
a diminished gain (curve c).
Altogether, such responses indicate that the sensitivity of the antennal system and its capacity to detect a single frequency are enhanced for
certain stimulus intensities, in this case at about 400 nm particle displacement. It thus becomes apparent that maximum gain does not take
place at very faint sound levels, perhaps suggesting that the active, actuating function of the neurons in Johnston’s organ takes place well above
the reported signaling thresholds, which are in the nanometer range for
the same species (Göpfert and Robert 2001).
The mechanical response of the male antenna to sound simulating
a passing female was also measured, not the least because the sound
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Figure 4. Mechanical response of the antennal receiver of the mosquito Toxorhyn-
chites brevipalpis to a stimulus of linearly increasing intensity. Carrier frequency of the
stimulus is 380 Hz. (A) Mechanical response, measured as the displacement of the
antennal tip (see Fig. 1D), as a function of sound intensity, expressed as the near-field
particle displacement. The straight line indicates response linearity, against which the
antennal response can be compared. For sound intensities in the middle and higher
ranges (b, c), the response is nonlinear. This indicates that the antenna moves more
than predicted by the energy input provided by sound alone. (B) Frequency spectra
of the mechanical response at intensity regimes a, b, and c. In the regions of nonlinearity (b, c), the frequency response reveals the sharpening, and the increase in the
gain of the response, an enhancement of mechanical sensitivity. (Data courtesy of J.
C. Jackson, unpubl.)
produced by a female is what the male auditory system has evolved to
detect (Clements 1999). The sound of passing females was recorded and
analyzed to characterize their likely amplitude profile and time course.
The amplitude profile can be approximated by a Lorentzian function,
reflecting the transient onset and offset of the sound of a passing female
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mosquito (Jackson and Robert 2006). Playing back sound at 400 Hz
carrier frequency mimicking a female, with such amplitude profile, generates a mechanical response that is quite unexpected but highlights the
functional complexity of the mosquito auditory system (Fig. 5A).
The gain of the antenna’s mechanical response is nonlinear, as
expected, but the time evolution reveals that enhanced mechanical sensitivity (gain) occurs on two occasions. As sound intensity increases,
antennal gain exhibits a transient peak (Fig. 5, time ~1.2 seconds, sound
intensity ~1 millimeter per second), followed by a compression trough
coinciding with the time of maximum intensity of stimulation. Remarkably, a large gain peak takes place as stimulus intensity rapidly decreases.
The peak of that secondary gain occurs at time ~2.7 seconds in this
example, and coincides with sound intensities much smaller (micrometer
range) than those that elicited the primary gain. Such gain fluctuations
do not occur in mosquitoes that are freshly killed or anesthetized.
This result provides first insight into the possible ultimate function
of active mechanisms in insect hearing (Jackson and Robert 2006). The
prolonged enhancement of gain allows the antenna to oscillate at the frequency of the female flight for a little bit longer. In effect, it extends the
hearing range of the male mosquito by several body lengths, a distance
which is not negligible in view of the severe attenuation of sound intensity in the near-field. Clearly, behavioral experiments are now needed to
test the predicted extension of the male auditory range, and his capacity
to detect and orient toward passing females, with and without the help
of active auditory mechanisms.
A recent behavioral and acoustical study reports on the acoustic
interactions between male and female of T. brevipalpis, providing not
only a well-needed behavioral context for mosquito hearing, but also a
precious insight on what happens when a female enters the detection
space of a male (Gibson and Russell 2006). Measuring the acoustic radiation close to tethered flying animals, that study establishes that the flight
tones of both males and females are about 420 Hz and that, notably,
frequencies can be quite variable, ranging from ~300 Hz to 500 Hz. In
males, change in flight frequency is observed to take place in response to
stimulation with a 450-Hz synthetic sound (Fig. 5B); the male’s flight frequency departs from 435 Hz to gradually converge to and hover around
the stimulus frequency, even outlasting stimulus duration.
Remarkably, when male and female tethered mosquitoes are brought
together close enough, their flight tones tend to converge, sometimes
generating the frequency beats indicative of near-tuning (Fig. 5C). Interestingly, both male and female seem to be capable of altering their flight
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Figure 5. Gain fluctuations of antennal mechanics and adaptive flight-tone
behavior of T. brevipalpis in response to female-like acoustic stimulation. (A)
Time-resolved gain fluctuations of the male antenna in response to an acoustic
stimulus mimicking the amplitude and temporal profiles of a passing female.
Gain curves show superimposed responses from five stimulus presentations. The
control curve (at gain 2) shows the linear gain response of a freshly killed male
mosquito. Stimulus curve is the Lorentzian function approximating a female
flyby sound profile. (Modified, with permission, from Jackson and Robert 2006
© National Academy of Sciences, U.S.A.) (B) Sonographic representation of the
flight tone (435 Hz) of a male T. brevipalpis, and its response to the presentation of a 450-Hz tone. The flight frequency of the male increases gradually to
nearly match that of the stimulus. (C) Flight tone of a male in solo flight until
a flying female is brought within auditory range. After several seconds, male and
female flight tone frequencies nearly match. (Modified, with permission, from
Gibson and Russell 2006 © Elsevier.)
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tones, sometimes meeting halfway (Gibson and Russell 2006). This “flying
in tune” happens within seconds, a timescale similar to that bringing
about gain fluctuations in antennal mechanics (Jackson and Robert
2006). Conversely, male–male interactions lead to a divergence in flight
tones. Speculatively, this aversive reaction brings the males apart acoustically, possibly avoiding same-sex courtship, but also perhaps constituting
a form of competition in the frequency domain of the acoustic space
surrounding them. Interestingly, the study by Gibson and Russell also
shows that the behavioral frequency specificity of males is higher than
that of the mechanical response of the male antenna. The role of active
auditory mechanisms in determining the acoustic sensitivity, the frequency selectivity, and the time-resolved dynamics of this intriguing
mate-recognition behavior remains to be investigated, using the multiple
tools available to insect auditory science.
In conclusion, it may be reasonable to suggest that understanding the
mechanics and neurobiology of sound reception in diverse insect species
continues to unveil the multiplicity of mechanisms by which biological
structures can respond to sound and, considering the larger issues of cell
signaling and energetics, transduce and/or dissipate flows of acoustic
energy that vary greatly in their amplitude and frequency domains. How
this is exactly done remains a central challenge. One may also want to
advocate, finally, that the great experimental amenability of insects
(Kernan and Zuker 1995; Eberl 1999), their unmatched ability to make
complex biology happen at the small end of the biometric scale, along
with their awe-inspiring diversity in form and function (Grimaldi and
Engel 2005), are poised to contribute original insights into the fascinating
mechanisms of hearing.
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Auditory Systems in Insects - Cold Spring Harbor Monograph Archive

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