Innovative Biomechanics for Directional Hearing in Small Flies

5 Pages·2001·2.2 MB·

by  Daniel Robert

Reference: Biol. Bull. 200: 190-194. (April 20(11)
Innovative Biomechanics for Directional Hearing
in Small Flies
DANIEL ROBERT
Laboratory ofBioacoustics, Institute ofZoology, University ofZurich,
Winterthurerstrasse 190, CH-8057 Zurich, Switzerland
Abstract. In humans and animals alike, the localizationof Introduction
sound constitutes a fundamental processing task of the
In the sense of evolution, sensory systems constitute
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animals, such as insects, the auditory receptors are forcibly evolutionary vantage point, the considerable diversity of
set close together, a design constraint imposing very short insect auditory systems (Hoy and Robert, 1996) can be
interaural distances. Due to the physics of sound propaga- regarded as an array oforiginal and adapted solutions to the
tion, the close proximity of the sound receivers results in particular problems of acoustic detection using small sen-
vanishingly small amplitude and time cues. Yet. because of sors. Because they evolved under the particular constraints
their directionality, small auditory systems embed original imposed by small body size, insects are likely to be of
and innovative solutions thatcanbe ofinspirational value to significant inspirational value for general problems of min-
some acute problems oftechnological miniaturization. Such iaturization. Our investigations are focused on questioning
ears are found in a parasitoid fly that acoustically locates its whether insects at the small end of the biometric range
singing cricket host. Anatomically rather unconventional, (millimeter and less) can be endowed with auditory organs,
the fly's auditory system is endowed with a directional whether they can be directionally sensitive, and if so, what
sensitivity that isbasedonthemechanical coupling between mechanisms are responsible for such directionality?
its two hemilateral tympanal membranes. The functional
principle permitting this directionality may be ofparticular Design Constraints for a Miniature Auditory System
relevance for technological applications necessitating sen-
sorsthatare lowcost, low weight, andlow energy. Basedon One such small insect is a parasitoid fly that acoustically
silicon-etching technology, early prototypes ofsub-millime- locates and attacks singing field crickets (Cade, 1975). As
ter acoustic sensors provide evidence for directional me- part of their reproductive cycle, female parasitoid flies
chanical responses. Further developments hold the promise Ormia ochracea must find their cricket hosts as a source of
ofapplications in hearing aid technology, vibration sensors, food fortheir larval offspring. Remarkably, successful song
and miniature video-acoustic surveillance systems. localization can take place in complete darkness, that is, in
the presence of acoustic information alone, but in the ab-
sence of visual and olfactory cues (Ramsauer and Robert,
E-mail: [email protected]
This paper was originally presented at a workshop titled Invertebrate 1999. 2000). Hence, because ofits crucial role in reproduc-
Sensory Information Processing: Implications for Biologically Inspired tion, audition is of great importance in the evolutionary
AutonomousSvstems.Theworkshop,whichwasheldattheJ.ErikJonsson history of these flies: promoting an increased reproductive
CenterfortheNationalAcademyofSciences,WoodsHole,Massachusetts, success, efficient audition is likely to be under acute selec-
finrothme1S5p-a1c7eALpirfielS2c0i0e0n,cewsasatstphoenMsaorriendebyBitohleogCiecnatleLrafboorraAtdovrayn,caenddSftuunddieeds tivBeoptrhesdseurtee.ction and localization of the singing host are
by the National Aeronautics and Space Administration underCooperative
Agreement NCC 2-896. mediated by a pair ofauditory sensory organs situated on
190
INNOVATIVE AUDITORY MICROMECHANICS
the anterior thoraxjust above the first pair of legs, which system of the fly. For humans, in comparison, ITDs at
are directly below the fly's neck (Robert ft al.. 1992) such an angle of incidence are much larger (Fig. IB),
(Fig. 1A). The ears of the fly are endowed with two thin varying from 500 /is to 700 /is, depending on head size,
tympanal membranes, the eardrums, that are set very the sound path considered, and the frequency considered.
close together across the midline of the animal. In fact, It thus becomes apparent that microsecond-range ITDs,
while the tympanal membranes together span about 1.2 and possibly smaller ones, ought to constitute a major
mm in width, the mechanoreceptive sensory organs are difficulty for the auditor) system of the fly, both at the
separated from each other by only 520 /im (Robert et al.. mechanical and neural coding levels. Another difficulty
1994) (Fig. 1A). As expected from the fly's small size arises when the second directional cue, the interaural
and the resulting minute interaural distance, the largest intensity difference (IID), is considered. The behavior-
interaural time difference (ITD) generated by a passing ally relevant frequency range is that of the cricket's
sound wave does not exceed 2 /is (Robert etal., 1996). In calling song, which spans from 4.6 to 5.2 kHz. Since at
mm
the best possible case, for an azimuthal angle of inci- such frequencies the ratio of wavelength (66 at 5.2
dence of 90 off the longitudinal axis of the animal, the kHz) to interaural distance (520 /im) is larger than 100,
ITD was measured with probe microphones to be 1.45 /is diffraction is very unlikely to occur around the fly's
(SD: 0.49 /is. n = 10) (Fig. IB). Such time difference is body, or at her ears (Morse and Ingard, 1968). Measure-
clearly much too small to be encoded by the nervous ments made with custom probe microphones (100-/xm
acceptance diameter) and with Vx-in microphones (Briiel
& Kjaer type 4138, Naerum, Denmark) failed to indicate
Contralateral
diffraction-elicited sound pressure differences around the
fly that could constitute IID cues.
Admittedly, the minuscule ITD (1.7 jus) and IID (<1 dB)
generated from an incident sound wave constitute less than
reliable acoustic cues for directional hearing. This finding,
however, stands in sharp contrast to the behavioral capacity
of this fly to localize the song ofher host, as demonstrated
in the field and laboratory (Robert et al., 1992; Walker.
1993; Ramsauer and Robert, 2000).
Innovative Tympanal Mechanics
Taking place at the peripheral level of the tympanal
membranes, the first step in the process of hearing per-
tains to the conversion of acoustic energy into mechani-
cal energy. Thus, tympanal mechanics was examined in
response to incident sound waves, either with pure tones
mimicking cricket songs, or with band-limited white
noise. Using microscanning laser vibrometry (Robert and
Lewin, 1998), displacement velocities were assessed over
-90 -60 -40 -20 20 40 60 several hundred measurement locations on both tympanal
Angle of Incidence [degrees] membranes and on the associated cuticular elements. In
audFiitgouryreor1g.ansAuodfittohreypaarnasaittoomidy falyndOrtmeimaporoaclhraaccoeuastaircecluoecsa.ted(Ao)nTthhee aremspplointsuedetoarnadnpdhoamsenoirseespaosnsweelsloafsbpoutrhe ttoynmepasntiamlulim,etmh-e
anterior thorax, between the first pair oflegs (L) and the neck (N). The branes differ strongly from those expmecmted for two inde-
tympanal membranes (TM) are adjacent to each other and set close to- pendent pressure receivers set 0.5 apart (Fig. 2).
gcberotinhdnegerectbiisyonmtahbdeeetmwioedfelnitnhetihcekoefrtwtcohuetiTcaMlneismtahalacnr(ovsTesrMtstihcaealnmddiadhlsiahnseed,thletihnees)h.ianpPtereorovtfiydmaipnacgnoaalta Faibrlsytlys,mailnldedpiefnfdeernetncerseceiinvearmsplwiotuuldde,inwdhiecrateeasimtmheeasfulyr'-s
hanger.Twodepressionsatbothendsofthe intertympanalbridge indicate tympana undergo large differences in their vibrations
theinsertionpointofthesensoryorgans(arrows).Arrowsalsopointtothe above about 4.5 kHz (Fig. 2A). Secondly, independent
interauraldistance.(B)Interauraltimedifference(ITD)asafunctionofthe receivers such as microphones indicate interaural time
angle ofincidence ofthe sound stimulus. Right ordinate: ITDs calculated delays on the orderof2 /is (Fig. IB), an ITD significantly
dcfoaerlvcihuaultamitoaennd)ssf(oheroawarsnseIipnTatDrearmtauieroaansluodfries1mt7ea0nncmtemm)oa.fd0Le.e6fattmomr9.di0nDaatatez:aimIpuoTtiDhnstaan(twdtih5tehkfsHltyz'asntdeoaanrreds, smmaaxlilmearlthdaenfltehcetidoenl)ayosbs(earlvseodmeinastuheremdecahsatnhiecpahlarseesplaognsaet
with two probe microphones located at the TMs. of the tympanal membranes (on average; 55 /is; SD: 12
192 D. ROBERT
The Process of Intertympanal Coupling
In an effort to unite structure and function in a functional
explanation, the reconstitution of actual tympanal deflec-
tions provides key information on the anatomical basis for
the observed mechanical behavior. The particularity and
perhaps uniqueness of these ears is that they are physi-
cally connected by an unpaired cuticular structure, the in-
tertympanal bridge (Figs. 1A, 4A). This bridge is thicker
(2-10 jrni), and therefore stiffer, than the surrounding tym-
panal membranes (0.2-1 /urn) to which it attaches. Thus, the
tympana are mechanically linked by a relatively rigid cu-
1 3 5 7 9 11 13 15 17 19 21 23 25 ticular bridge, a fact that can also be easily assessed by
Frequency [Hz] gently deflecting one tympanic membrane downwards with
B.
100
midline
contra
1 1 1 1 1 1 1 1 1
1 3 5 7 9 11 13 15 17 19 21 23 25
Frequency [Hz]
Figure 2. Mechanical response ofthe tympanal membranes in ampli-
tude and time. (A) Difference amplitude spectrum of the mechanical ipsi
response at the anatomical locations indicated in the inset (arrows). The midline
contralateralmechanicalresponseissubtractedfromtheipsilateralone.(B)
Timedelaybetweentheipsilateralandcontralateralmechanicalresponses, contra
calculated from the difference phase spectrum. Sound stimulus at 45
incidence in azimuth, band-limited white noise (1-30 kHz). 300
=
;u.s, n 769 frequency points) (Fig. 2B). In effect, these
measurements indicate that the mechanical response of
the tympanal membranes has a pronounced directionality.
Interaural time and intensity differences in the mechan-
ical response of the tympana are significantly larger than
those available in the acoustic field. The analysis of
tympanal deflection shapes (see Fig. 3A) provides evi-
dence that such differences between the ipsilateral and
contralateral responses are due to the particular mechan-
ical properties of this small tympanal system. Reflecting
the asymmetrical responses reported earlier (Fig. 2). de-
wflheiclteionthsehaippessilaatterfarleqtueynmcpieasnuamrouunndde5rgkoHezs ianndicoauttewtahradt CitoyhFweiargseunrmceoen3.ivtaoluTreeysdmpeataxcn3ea6el4dedledofcl0ae.tc9it5oi,nosninosdvhieacrpaettsiy.nmgp(alAinlttalTleycamonpndatnanamoilnn-avttiybimropanatniboaynluvanercleooarcs--.
deflection, the contralateral tympanum experiences an related noise. Stimulus: band-limited random noise (1 to 30 kHz; 94 dB
inward deflection, but of much lesser amplitude (Fig. SPL (sound pressure level]) at90 azimuth tothe longitudinal axis ofthe
3B). Such asymmetry in the response is due to the fact fly. Ipsilateral andcontralateral conventions asindicated. (B) Upperpanel
tvhiabtrattihengtiwnodehpeemnidleanttelrya.l Tthyemptaynamlpanmaemabrreaninesfacatreconno-t dastehfo5lwekcstHimzoanexxriceimatcuahtmeidoonuhtaflwrfaeqraudepnedceryfil.oedcLtloiawtoener,rofep.gta.hn,eel1ip0ds0eipl/aiJt.csetrslaalttehtre.ymXmpaaaxnxaiislm:umlmeatmeirbanrlw;aanrYed:
nected, across the midline, by a specialized cuticular ventral; Z: axis of measured tympanal deflections. For animation ofde-
structure (Robert et al., 1994, 1996). flection, please visit: www.unizh.ch/~ormia/research_flies.html
INNOVATIVE AUDITORY MICROMECHANICS
The kHz), the deflections of the ipsilateral and contralateral
intertympanal bridge membranes show little difference in amplitude andphase. In
this case, the forces applied to the bridge (Fig. 4B) have a
phase difference of only 1 and result in sympathetic de-
flections, owing to the bendingofthe bridge (Fig. 4C, mode
1 ). At this frequency ofexcitation, the first mode ofdeflec-
tion dominates the response. Excitation of this first mode
results in little directionality or asymmetry in the me-
chanical response, as shown for frequencies lower than
B. Flexible hinge F about 3 kHz (Fig. 2A). As stimulus frequency increases, a
p^t) 2(t) transition to the second mode ofdeflection is expressed by
the rocking motion of the bridge (Fig. 4, mode 2). Note-
IRdl ] worthy is the fact that for intermediate frequencies (i.e., 5
Fulcrum kHz) and a given effective interaural distance, the phase
difference in the driving forces increases. At 5 kHz, this
phase is very small 2.6 yet, it is sufficient to drive this
system to its rocking mode (Fig. 3B). A combination of
mode 1 these two modes (rocking and bending) will take place at
even higher frequencies (e.g., \5 kHz) and result in the
deflection of the ipsilateral tympanum, but in the silencing
of the contralateral one (Fig. 4C, mode 1+2). Hence, the
relative flexibility of the bridge, be it localized at the ful-
crum point or distributed along the lateral arms, constitutes
the key to the directionality of the observed mechanical
response.
In addition, experiments of mechanical actuation in the
Figure4. Theanatomyofmechanicalcoupling,andvibrationalmodes absence of sound have demonstrated that mechanical cou-
of the flexible intertympanal bridge. (A) Close-up of the intertympanal pling is mediated and can be explained by the action ofthe
bridgeconnectingthetympanalmembranes. (B)Simplemechanical model intertympanal bridge alone (Robert et at., 1998). The me-
oflfextihbelebrciedngteralashainsgeees(a=w).en(dC)oweOdnwtihtehbtawsoisriogfidthbearslasceornnveicbtreodmebtyrica chanical actuation ofone tympanum at amplitudes ofabout
micromechanical analysis, it is suggested that two basic modes can char- 10 nanometers mimicking the displacement amplitudes
acterize the observed mechanical response. Bending occurred at low fre- observed during acoustic stimulation elicits a correlated
quencies (mode 1; <4kHz), whereasrocking was measuredat intermedi- mechanical displacement ofthe other tympanum. The finite
ate frequencies (mode 2: 5-1 kHz). At higher frequencies (\5 kHz and flexibility ofthe intertympanal bridge accounts for the IIDs
atbyomvpe)a,nubmenodnilnyg(maonddero1ck+in2g).modes combine to elicit motion in one and ITDs in the mechanical deflections, for which two
modes dominate at different frequencies (Robert et al..
1996). Hence, in summary, the mechanical structure of the
a human hair, and observing the other deflect upwards as a hearing organs increases the minimal acoustic interaural
result. time and amplitude difference cues into more substantial
Deflection shapes obtainedby microscanning laserDopp- mechanical cues that can be processed by the nervous
ler vibrometry for different stimulus frequencies (e.g., 2, 5 system (Robert et al., 1996).
or 15 kHz) reveal that this micromechanical system can
produce several different patterns of deflection that are Intertympanal Coupling as an Evolutionary Novelty
reminiscent of the movements of a flexible seesaw (Fig.
4B). The simple mechanical model shown in Figure 4B has As such, the process of mechanical coupling between
been proposed as a reasonable functional, and intuitively tympanal membranes, and its amplification effect on inter-
accessible, approximation ofthis unconventional peripheral aural auditory cues, seems to be unique to flies. In essence,
auditory system (Miles et al, 1995: Robert et al. 1996). intertympanal coupling constitutes a novel mechanism for
The physical actionofthe intertympanal bridge is toconvert directional hearing, representing a third kind of directional
small acoustic ITDs into larger time and amplitude differ- receiverforterrestrial animals. One otherkindofdirectional
ences at the mechanical level. The functional principle for system is found in most vertebrates, and is based on two
this effect resides in the somewhat complex linear interac- acoustically isolated pressurereceivers set apart on the head
tion between two coupled oscillators the tympanal mem- ofthe animal. In other small animals, such as frogs (Narins
branes. Very briefly, for low frequencies of stimulation (2 etui. 1988) and some birds (Calfordand Piddington. 1988),
194 D. ROBERT
the auditory receivers are acoustically coupled (pressure- Literature Cited
difference receivers), a system that has been shown to result Cade, VV. H. 1975. Acoustically orienting parasitoid: fly phonotaxis to
in the amplification ofthe perceivable ITDs and IIDs avail- cricket song. Science 190: 1312-1313.
able in the sound field. Calford, M. B., and R. W. Piddington. 1988. Avian interaural canal
enhances interaural delay. J. Comp. Physiol. A 162: 503-510.
Conclusions Hoy, R. R., and D. Robert. 1996. Tympanal hearing in insects. Anna.
Rev. Emomol. 41: 433-450.
One of the outcomes of the research presented here has Miles, R. N., D. Robert, and R. R. Hoy. 1995. Mechanically coupled
been to explore the possibility of transferring the mecha- earsfordirectionalhearingintheparasitoidfly O. ochracea. J.Acousl.
nism ofintertympanal coupling to microsensor technology. MorsSoec,.PA.mM..,98a(n6)d:K3.05U9.-I3n0g7a0r.d. 1968. TheoreticalAcoustics. McGraw
Abstracting the functional principle unraveled in the para- Hill, New York. Pp. 418-422.
sitoid fly may indeed contribute to the development of Narins, P. M., G. Ehret, and J. Tautz. 1988. Accessory pathway for
subminiature microphones. Besides the inherent direction- sound transfer in a neotropical frog. Proc. Natl. Acad. Sci. USA 85:
ality ofthe receiver's mechanics despite its small size, two 1508-1512.
other, definite and foreseeable, advantages of fly-inspired Ramsauer, N., and D. Robert. 1999. Acoustic attraction ofthe parasi-
acoustic receivers would be their low cost and low energy toidflyOrmiaochraceatothesongofitshost.J.Acoust. Soc.Am. 105:
1319.
consumption. Indeed, one of the possible attractive aspects Ramsauer,N., and D. Robert. 2000. Phonotactic orientation in apara-
of such a system is the fact that the first stage of acoustic sitoid fly. Naturwissenschqften 87: 315-319.
processing is made on a mechanical basis, without the Robert, D., and A. Lewin. 1998. Microscannmg laser vibrometry ap-
intervention ofenergy-consuming electronics. Using micro- plied to the biomechanical study ofsmall auditory systems. Pp. 564-
electromechanical systems technology (MEMS), our early 571 in ThirdInternational Conference ofVibration Measurements by
prototypes etched on silicon wafers provide evidence that Laser Techniques. Ancona. Italy. E. P. Tomasini. ed. Proceedings of
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Finally, possible applications can be envisaged that could Robert, D., M. P. Read, and R. R. Hoy. 1994. The tympanal hearing
contribute to the development of hearing aids or miniature organoftheparasitoidflyOrmiaochracea(Diptera,Tachinidae,Ornii-
personal communication devices endowed with improved Robeinrit).,CDe.l,lRT.isNs.ueMiRleess.,2a7n5:d6R3.-7R8..Hoy. 1996. Directional hearing by
receiver acoustics, or small surveillance systems capable of mechanical coupling in the parasitoid fly Ormia ochracea. J. Comp.
pinpointing a source of noise. Physio/. A 179: 29-44.
Robert,D.,R.N.Miles,and R. R.Hoy. 1998. Tympanalmechanicsin
Acknowledgments the parasitoid fly Ormia ochracea: intertympanal coupling during
mechanical vibration. J. Comp. Physiol. A 183: 443-452.
This work was supported by the Swiss National Science Walker. T. J. 1993. Phonotaxis in female Ormia ochracea (Diptera,
Foundation. Tachinidae).aparasitoidoffieldcrickets.J.InsectBehav. 6: 389-410.