- Email: [email protected]
Audition in echolocating bats
Audition Gerhard Zoologisches
lnstitut
In bat audition,
in echolocating
Neuweiler
and Sabine Schmidt
der Ludwig-Maximilians-Universitit,
major advances
tuning in the bats’ cochlea, information
bats
processing,
Current
have been made concerning
cortical
maps and the related
and the perceptual images.
Opinion
Mtinchen,
in Neurobiology
mechanisms
Germany
the frequency
subcortical creating
echo
auditory
1993, 3:563-569
Introduction
frequency tuning observed derstood [ 5 ]
In man and many mammals, perception of the outside world is dominated by the visual system. In contrast, echolocating mammals orient themselves by acoustical cues extracted from echoes of their emitted echolocation sounds. For studying neuronal processing of auditoty information, therefore, echolocating bats provide good models offering several experimental advantages including the existence of well differentiated nuclei of the ascending auditory pathway which are hypertrophied to various degrees, and the use of well defined echolocation signals as biologically relevant stimuli. These signals are species-specific and simply structured: they consist either of brief (0.5-5ms) frequency modulated (FM) sweeps only, or they can be combined with a longer (5-50 ms) constant frequency (CF) element (CF-FM signals). The echoes, which carry the information about the acoustical qualities of the bat’s environment, will be distorted replicas of these simple echolocation signals and will always occur time-locked to a preceeding vocalization.
Horseshoe bats, Rbinolophus rouxi, and mustached bats, Ptevonotusparnellii, are good models to study mechanisms of fine-tuning in the cochlea. These echolocating bats emit long lasting (10-100 ms) pure tones at an individual frequency within a narrow species-specific range (6G62 kHz in P, parnellii and 76-80 kHz in R. rouxi>. These tonal signals serve as carriers for brisk echo modulations imposed onto the pure tone echo by the beating wings of flying insects, the prey of these bats (for review see [4]). The bats’ cochleae feature an ‘auditory fOVea’: the narrow frequency band of a few kilohertz around the personal echo-frequency is represented in an expanded way and covers nearly a complete half turn of the cochlea [ 6,7]. Tuning curves of auditov units tuned to the fovea are extremely narrow (Qlodu-vdlues of up to 500 compared with a maximum of 2&3O in units receiving afferents from non-fovea1 parts of the cochlea, or from unspecialized cochleae of other echolocating bats or other mammals; for reviews see [3,4] ).
This review focuses on three controversial issuesnamely, fine frequency analysis in the cochlea, the computational maps and functional subdivisions of the auditory cortex and their possible subcortical substrates, and acoustical imaging by echolocating bats. For more detailed reviews on audition in echolocating bats see
This ultrafine tuning within the auditory fovea is correlated with distinct structural and cellular specializations of the organ of Corti just basal to the fovea1 section. These pecularities are thought to create reverberations [&lo] To account for the ultrafine tuning, it is necessaq to consider two components, namely, a predominantly passive mechanical resonator (established by the basilar membrane structure) and an electromechanical feedback from the OHCs, which is superimposed onto the mechanical oscillations and produces additional sensitiviq and sharp tuning.
11-41.
Fine frequency
analysis
in the cochlea
of bats
the mammalian auditor)l system, frequency analysis is achieved in the cochlea by a bank of low pass frequency filters, based on mechanical gradients of the basilar membrane. Outer hair cells (OHC) may add an active electro~mechanical element for increasing the sensitivity and fine-tuning of the cochlear frequency filters. How these mechanisms combine to achieve the narrow
in all mammals
is not yet un-
In
Mechanical resonance
Structural modifications of the organ of Corti, such as conspicuous thickenings of the basilar membrane, provide a steep, localized impedance discontinuity at the basal end of the fovea1 part of the basilar membrane. Incoming wdves of a frequency (resonance frequency) vev
Abbreviations AVCN manteroventral
cochlear
MNTB--medial OHC-outer
nucleus;
nucleus
of the
CF-constant trapezoid
frequency; body;
hair cell; PVCN-posteroventral
@
Current
FM-frequency
MSO-medial
cochlear
Biology
superior
modulated; olive;
nucleus;VNLL-ventral
Ltd ISSN 0959-4388
MGB-medial
OAE--otoacoustic nucleus
of the
geniculate
body;
emission; lateral
lemniscus.
563
564
Sensory
systems
close to the bat’s individual echo frequency should reverberate between the place of the impedance discontinuit) and the oval window [ 111. Evidence for such a reverberating system are ringing microphonics and otoacoustic emissions (OAE), which have a frequency just below that of the bat’s individual echo frequency and which are represented on the basilar membrane just apical to the place where the impedance discontinui? occurs [7,12], As in humans and laboratory mammals, frequencies of OA!Zs in bats are identical to those of high auditory sensitivity, This reverberating mechanical system may not only guarantee a high sensitivity at the echo-frequency, but also create a peak of insensitivity for frequencies slightly below the echo-frequency. For example, it has been suggested that interferences between the undamped resonator and lower stimulus frequencies produce the steep low-frequency flank of the sharply tuned echo filter in P. puvnellii, which may add to tuning and shut off the fovea1 frequency band from impacts of lower frequencies (M KZjssl, unpublished data). In mustached bats, it has been shown that the cochlear resonance frequency shifts along with body temperature and increases by 150 Hz when the bat is flying [13-l 51. The bat adjusts its emitted echolocation frequency to the shifting resonance. The small temperature eff‘ects (39 Hz “Cl) are consistent with a tuning mechanism that critically depends on mechanical interactions. Apparently these bat species, focusing fine frequency analysis onto a vety narrow individual band rather than evolving new filter systems, have enhanced the efficiency of frequency analysis of common mammalian mecha~ nisms to their limits.
Electromechanical membrane
feedback from
OHCs
to the basilar
oscillations
Two-tone distortions generated in the inner 6‘dr indicate non-linear amplifications thought to originate from OHC excitations which feed back to mechanical oscillations of the basilar membt-dne. Such distortions can be measured acoustically in the outer ear of bats. In mustached bats, large levels of the distortions close to the CF-frequenq can only be elicited with small frequency separations of the two tones [ 161. This indicates a high sensitivin and an outstanding mechanical frequency resolution in the cochlea. Like the OHCs of other mammals, bat OHCs contain a lateral subsurface cisternae system [9] which is thought to be involved in OHC motility. Application of salicylate, which is known to block OHC motility, was recent11 shown to reduce the level of distortion products bl 25-36 dB [ 171. This is indeed suggestive of a contribution from OHC motility to distortion production and hence to the generation of low auditory thresholds. The length of the OHCs and their stereocilia is remarkably constant within the basal cochlear turn of horseshoe bats [8,9] ; this may provide a basis for the expanded rep-
resentation (fovea).
of the narrow
echolocation
frequency
band
In the cochlea of bats, micromechanical processes in the OHCs may produce a high sensitivity and contribute to the fovea1 frequency representation. They are superimposed and fed back on macromechanical resonance which is crucial for enhanced tuning and the creation of local insensitivities. They shut off extremely fine fre cpency separation in the echo-frequency range from conventional frequency tuning at lower frequencies.
The role of the medial echolocating
superior
olive
in
bats
The medial superior olive (MSO) is considered to compute interaural time differences for coding the direction of a stimulus. In laboratory mammals, MS0 units get excitatory projections from the left and right anteroventral coclear nuclei (AVCN). According to Jeffress’ model which (cited in [ 181) the MS0 acts as a cross-correlator codes interaural time differences by excitatory delay lines feeding into MS0 coincidence detectors. The most convincing evidence for this model comes from work by Yin and Chan [ 181. But studies in echolocating bats have now questioned whether this concept of interaural time coding is applicable to the MS0 of all mammals [ 19-21,22-l. Neurons of the MS0 in echolocating bats behave entirely differently from those in carnivores [ 21,22-l. Most units are only excited from the contralateral AVCN and receive no input from the ipsilateral AVCN. In addition, these monaural units get strong glycinergic input from the medial nucleus of the trapezoid body (MNTB) which turns the originally sustained excitatory response into a brisk, phasic one. This was recently demonstrated by application of the glycineantagonist, strychnine [22*]. In echolocating bats, the MS0 is thus turned into a monaural circuitry with a strictly phasic output caused b> a strong inhibitory input from the MNTB. This inhibitoq pathway also exists in non-echolocating mammals, but is a very weak input by comparison with the strong excitatory afferences from both ears. At present, it is an enigma why in echolocation the ipsilateral excitatov input to the MS0 should be suppressed and the inhibitory input from the MNTB enhanced. Recordings from MS0 units suggest that they are well adapted to code and analyze amplitude modulations and their repetition rates in echo signals [ 22.1, Such repetitive modulations ny;1)’be caused by wing beats of the bats’ prey.
Ascending
auditory
pathway
and precise time
coding In echolocating bats, transmitter distributions and their functional impact in the ascending auditory pathway generaIll, conform to that found in non-echolocating mammals [23-271, However, the bat pathway contains an
Audition
additional functionally important substance, the Ca2+ binding protein ‘calbindin’. In the barn owl, calbindin has been associated with binaural circuits requiring precise time coding for processing directional cues [ 281. In contrast, a study in the mustached bat demonstrated that somata and nerve endings containing calbindin are predominantly seen in monaural nuclei [ 291. The calbindincontaining pathway starts from globular cells of the AVCN and from octopus cells of the posteroventral cochlear nucleus (PVCN) and projects, directly and via the MNTB, to the ventral nucleus of the lateral lemniscus (VNLL). The VNLL is hypertrophied and highly organized in monocellular sheets with large calyx-synapses in three different bat species [30] and in echolocating dolphins. Units of this specific nucleus respond in an exclusively phasic manner, with latencies unaltered by sound intensity and frequency. Such constant latencies are thought to be achieved by input integration over a wide array of afferents with different best frequencies, and, additionally, by high excitatory thresholds [ 301. All units of this nucleus precisely preserve timing information and, therefore, this pathway may be a prerequisite for calculating travel time between outgoing sound and returning echo. Travel time indicates the range between an echolocating bat and a target.
Cortical circuits
map of echo-ranging
and neural
for range finding
The first auditory cortex which could be clearly differentiated into functional and behaviourally relevant subdivisions was that of echolocating bats [31]. In the mustached bat, Suga and his colleagues described, among other divisions, a cortical ‘range-finding at-cd’. Neurons of this area are facilitated by pairs of FM stimuli with specific differences between first and second stimulus which mimic emitted sound and returning echo. This specific sensitivity to stimulus pairs qualifies such ‘FMFM units’ for coding travel time between emitted pulse and echo, and hence target range. The ‘best delays’ range from 0.4 to 18ms (corresponding to target ranges from 7 to 310cm) and are represented in a frontocaudal axis of the cortex. Excitation will shift from posterior to frontal places in the range finding area as a hunting bat approaches a flying insect. This basic concept of a computational range-finding map in the auditory cortex [32] has recently been refined and extended to other bat species [33-371. In spite of more than a decade of research, the neuronal circuits creating such precisely customized echosignalspecifity and delay-specifity in the cortex are not yet known. Units of a specifity similar to that of the rangefinding cortical units have been discovered in the medial geniculate body (MGB) but not in the interior colliculus which supplies the main auditory input to the MGR [38,391. Suga and his colleagues [l] have described a neural network that they designed for delay calculation based on
in echolocating
bats
Neuweiler and Schmidt
delay lines created by synaptic and axonal delays (for delays < 4 ms) and synaptic inhibition (delays > 4 ms). They assume that such a thalamic cross correlator (delay line) gets its input from collicular units tuned to different portions of FM signals. Inputs to the delay line should respond to a stimulus by only one spike and with a latency which is extremely constant and invariant to stimulus amplitude. Such time-coding lmits of high precision have been found in the VNLL [30]. However, this lemniscal nucleus only projects to the inferior colliculus, and collicular inputs to the MGB of similar or even higher precision of time coding have not yet been described. It seems that precise time coding disappears in a ‘Bermuda triangle’ between the lower level VNLL and the MGB, where it reappears. Studies on synaptical levels may finally elucidate how delay lines are established and time filters are created for tuning neurons to specific echo-delays, and hence to specific target distances. In the auditoty cortex of horseshoe bats and mustached bats, there is another large area which is specifically tuned to pure tones (CF) within the individual, narrow frequency band of the CF component in the echo-signal [40,41]. This cortical CF area is well suited for fine frequency discrimination because the units are extremely narrowly tuned and the narrow frequency band (which, for example, is 6&63 kHz in mustached bats) is tonotopically represented in an expanded fashion. In behavioral experiments, horseshoe bats and mustached bats detect deviations from the echo frequency as small as 50Hz or 0.06%. When muscimol, a potent agonist of y-aminobutyric acid, was applied to the CF area, fine frequency discrimination for frequency differences up to 0.5 kHz was temporarily disrupted whereas coarse frequency discrimination was not affected [42], Units of the CF area are facilitated when a pure tone of the echo-frequency is preceded by an FM stimulus similar to that emitted at the end of the echolocation signal [43*]. This is still another correlate to the neuronally and behaviorally well established fact that vocalization of an echolocation signal opens auditory time windows for enhanced echo processing (for review see [4] ). Thus, the CF area could serve as a fine frequency analyzer for even minute spectral cues imprinted onto the echo.
Regulation
of echo level during
target
approach In addition to using the ability of echo processing neurons to cope with a wide dynamic range [30], bats use two mechanisms to compensate for range-dependent changes in echo level. The first is to lower the level of their sonar calls with decreasing target distance, an effect that has recently been systematically described [44,45]. The second mechanism involves reducing the sensitivity of the ears during sonar emissions by muscular activity in the middle ear and central suppression of the excitation. The time characteristic for regaining full sensitivity after a vocalization has been
565
566
Sensory
systems
regarded as an automatic gain control mechanism for targets closer than about 1 m [46]. Accordingly, the target detection thresholds decrease by about 11 dB per doubling of target range [46,47*], which is similar to the increase in echo level of a point target. More complex perceptual processes seem to be involved in a recent experiment where two targets were presented simultaneously at different distances [48*]. When interpreted in terms of an automatic gain control mechanism, the results of this experiment suggest an increase of auditory sensitivity by only 6dB per doubling of target range, AS an alternative interpretation, one might conjecture that the bats just estimated the loudness of the more distant target.
Towards a theory
of acoustical
imaging
Echolocating bats determine target range from the time difference between the emission of a sona.r call and the arrival of its echo [49]. Information about the object’s surface structure is encoded in a spectral deformation of the echo, which raises the question of how bats extract this information when discriminating between structured targets [ 501. A unified theov of echolocation has been developed that regards bat sonar as a means to create an auditoty image of space comparable to visual space representation [ 51,521. According to this theov, the tem~ poral information of the echo is retained while spectral information is transformed to temporal information by the auditol): system. Then, a temporal cross~correlationlike process integrates both object position and structure into a unified spatial acoustic image, which is ultimatel) perceived by the bats. The appeal of this theoT is that it promises to account for the discrimination of target distance. time jitter in the echoes, and object structure in terms of a single perceptual process. It is surprising, at least, that the largely d&rent time delays associated with the experimental threshold \ralucs for absolute distance determination (50--l 00 ps ) [49], structure discrimination ( - 1 ps) [ 53*]. and time jitter ( - 10 ns) [ 541 should be explained by a unified the0~. Simmons (e.g. [ 551) attributes these di&rences to experimental difficulties, such as the inevitable head movements of bats comparing two targets. Moreover, the experimental evidence for the transfornmation of spectral into temporal information by the bat’s auditoT system is not entirely convincing, as the time differences corresponding to the structures in question of 46 /-IS [ 511 and 100 ps [ 521, respectively, are of the order of the bat’s distance discrimination threshold. Therefore, even if the bats have measured time delays in these experiments, this finding cannot be extrapolated to account for texture discrimination in general, where differences in surface depth corresponding to time differences of only a few microseconds are discriminated by the bats. Incidentally, recent distance discrimination experiments, in which the echoes were substituted by filtered versions of a typical bat call or noise pulses, have raised some
doubt about the use of a temporal cross-correlation-like process for absolute distance determination [ 56.1. Of late, the unified theory of echolocation (see [52] has been challenged on both the functional and the perceptual level. Two studies [ 53*,57*] on the ability of echoloeating bats to discriminate between structured targets consisting of two reflective surfaces (two-front targets) have shown for the first time that a bat’s performance can be satisfactorily explained by a model based on the processing of echo spectra. Functionally, this description may be preferable to that by temporal cross-correlation as the physiological requirements of the spectral model (i.e., a frequency resolution on the order of a few kilohertz) are easily met, while the neuronal timing accuracy (below 1 ps) required by the temporal cross-correlation receiver has not been established in bats or other mam mals. On the perceptual level, Schmidt [53-j has pointed out that if bats use a note-monotonous function (for example, a cross-correlation function) to set up a psychologied depth scale, a convoluted image of space is obtained, as certain distinct points in space are represented 1,) the same image point. It is questionable why bats should have evolved a unique mechanism to obtain an inaccurate representation of small spatial structures. On the other hand, the assumption of a monotonous time function is incompatible with the experimental data [ 53*]. Due to such difficulties with a purely spatial interpretation, both studies [53*, 57.1 dismiss the idea of a unified representation of echo information, and propose that target distance and structure are different perceptual qualities, target structure being perceived as a timbre or coloration of the echo. The perception of this acoustical qualiv does not prey suppose a specific adaptation of bat sonar, but is rather a general abilip of the mammalian auditory system. The \iew that echo timbre is actuall!. used by the bats to solve texture discrimination tasks is supported by the finding that bats pre\iousl!~ trained to discriminate texture in an echolocation exp’eriment spontaneousl!, discriminate between colored sc~ids presented independentI> of the animals’ vocalizatio~7s [ 5301. A model that :111o~vsl’or perceptual qualities other than the mere temporal imaging postulated by the unified theon, ma!’ also account for a discrepancy obsened in the discrimination performance of the bats in identical experimental situations. depending on the initial training: Mogdans ct al. [ 570 j found that bats discriminated a twofront target with an internal time delay of 100 ps from an unstructured target in more than 90% of the tests if they had first been trained in a texture discrimination task (the discrimination of structured targets with variable internal delay from the unstructured target) and if the first echo front of the two-front target and the unstructured target were presented at the same absolute time delay. In con trast, only 7G?5% correct choices were recorded for the identical target setting [52], when the animals had been trained to a ranging task, i.e. to the 100 ps two-front target presented at a fixed absolute delay and an unstructured target presented at variable absolute delays. In view of
Audition
these observations we propose that a theory of acoustical imaging by bat sonar should incorporate several different discrimination strategies.
Conclusions The classic questions in auditory research of echolocation are still of continuing interest. The concepts for fine frequency analysis in the cochlea have become even more numerous and more complex. Non-invasive methods of analyzing cochlear mechanisms have been fully exploited. A real understanding of the mechanical and electromechanical filter systems will only be achieved by studying vibrational motions of the basilar membrane and by recordings from hair cells. In contrast to neuronal time coding in electroreceptive fish [58], the neural circuits for computing echo travel time and for precise time marking of auditory events in echolocation are not yet known. However, substrates have been identified (MGB and VNLL) where studies on the synaptic connectivities by intracellular recordings and and in tissue slices may patch-clamping methods in zu’z~o give us guidelines into the labyrinth of subcortical echo information processing. The long lasting and ongoing dispute over a predominantly temporal or spectral basis of acoustical imaging is currently bringing forth a more pluralistic attitude, which admits several concurrent perceptual mechanisms. The development of more precise models of how these mechanisms cooperate will require further behavioral experiments characterizing the temporal and spectral properties of the bats’ auditory system.
5.
References
for many suggestions
and recommended
Papers of particular interest, published review, have been highlighted as: of special interest of outstanding interest
and critical
reading
within
the annual
period
6.
VATEK
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Acknowledgements We thank M Kossl and B Grothe reading of the manuscript
in echolocating
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This recent publication
may pave the way for a long awdited new IkId of
research: the neuronal analysis of complex spectral features of echoes which prObdbly code paranwters crucial for target identification. -l-t.
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SIMRK)NSJA, MOFFAT ALM, MASTEK~K’M: Sonar Gain Control and Echo Detection Thresholds in the EchoIocating Bat, Eptesicus fuscus. .J Acoust Sot Am 1992, 91:115(tll63. Echo detection thresholds van: with target distance due to the middle ear muscle activiy associated with sonar emissions. Although backward masking by clutter echoes is excluded in this study, the echo detection thresholds determined confirm the previously described Improvement m thresholds of 11 dB per doubling of target range [46]. This finding must be compared with [&=I,
47. .
48.
IiARTLEY DJ: Stabilization of Perceived Echo Amplitudes in Echolocating Bats. I. Echo Detection and Automatic Gain Control in the Big Brown Bat, Eptesicus fuscus, and the Fishing Bat, Noctilio leporinus. ,J Amus/ Sot Am 1992, 91:112@1132. In the first part of the paper, the backward masking effect of clutter echoes from the loudspeaker on the detectabiliy of a phantom target is studied, and receiver operating characteristics for target detection are obtained. Neither question has been explicitly addressed in former studies with echolocating bats. A second experiment mvestigates how bats evaluate the level of a far phantom target in the presence of a near phantom target of constant level. The results are presented as evil dence for a reduction of auditoy sensithity (due to middle ear muscle contractions and /or central suppression) by 6 dB per halving of target range, which contradicts the findings reported in [46,47]. .
49.
SIMMONSJA: The Resolution of Target Range by Echolocating Bats. J z‘kO/tSt sac AI12 1973, 54:157 173.
50.
SIMMONS JA. LALTNDERWA, LAVENIXK BA, IXIKOSHO~ CF, KIEFEKSW, I.&IL~NGSTOS R, SCALLETAC, CKOU’IEY DE: Target
36
MAEKAuA M, WONG D, I-‘.ksct~
37.
SHAVNONHARTMANS, Wow
38.
OISEN JF, SU(;A N: Combination-sensitive Neurons in the Medial Geniculate Body of the Mustached Bat: Encoding of Target Range Information. / Neurop&sio/ 1991, 65:1275- 1295.
52.
39.
OLSENJF, SUGA N: Combination-sensitive Neurons in the Medial Geniculate Body of the Mustached Bat: Encoding of Relative Velocity Information. ,/ Neurophysiol 1991.
of Structured Phantom Targets in the Echolocating Bat, Megaderma lyra. ,I Acoust Sot Am 1992, 91:2203-2223. The ability of LX !JVZ to discriminate between structured phantom tar gets with two echo fronts is characterized, and different functional mode els of echo processing are tested. The results show that the discrimination of target surface stmcturr can be explained as a discrimination of echo spectra. A dual perceptual model of echolocation is supported which holds that the hats perceive object distance and texture as sep arate qualities.
WG: Spectral Selectivity of FM-FM Neurons in the Auditory Cortex of the Echolocating Bat, Myotis lucz~ugus. J Cow@ P&iol [Al 1992, 171:513-522. D, MA~,KAUC’ M: A Processing
of Pure-tone and FM Stimuli in the Auditory Cortex of the FM Bat, Myotis lucifugus. Hear Rm 1992, 61:179-188.
65:1254-1274
40.
SUCA N: Disproportionate Tonotopic Representation Processing CF.FM Sonar Signals in the Mustached Auditory Cortex. Science 1976, 194:542-544.
41.
O%~AU, J: Tonotopical Organization and Pure Tone Response Characteristics of Single Units in the Auditory Cortex of the Greater Horseshoe Bat. .r Camp Phq’siol [A] 1984,
for Bat’s
Structure and Echo Spectral Discrimination ing Bats. Science 1974, 186:1130~1132. il.
1992, @%:1613-1623.
of the DSCF Cortex with Muscimol Disrupts Frein the Mustached Bat. J Neurop/qsio/
Basis for Target DiscrimBats. .I ncozrsf Sot Am 19X9,
SIMM~~VS JA, Moss CF, FERRAGAMOM: Convergence of Temporal and Spectral Information into Acoustic Images of Complex Sonar Targets Perceived by the Echolocating Bat, Eptesicus fuscus. .I Camp P@iol iA/ 1990, 166:44W70.
53. .
SCFIMID~S: Perception
54.
SIMMONSJA, FEIUXAGAMO M, Moss CF, STCVENSONSD, ALXS RA: Discrimination of Jittered Sonar Echoes by the Echolocating Bat Eptesicus fuscus The Shape of Target Images in Echolocation. J Camp Pblsiol /A/ 1990, 167:58=16.
KIQ~JIMARO~JX II, GAI~NI SJ, SXA N: Inactivation
Area of the Auditory quency Discrimination
SIMMONSJA, CHKN I.: The Acoustic
ination by FM Echolocating 86:1333-1350.
155:821-834.
42.
by Echolocat-
55.
SIMMONSJA, GR~NNELL AD The Performance
Acoustic
Images
Perceived
by Echolocating
of Echolocation: Bats. In Arzimal
Audition
56 .
Target Ranging and the Role of Time-Frequency Structure of Synthetic Echoes in Big Brown Bats, Eptesesicus fuscus. .I Camp P!?vsiol [A] 1992, 170:83-92. The impact of echo structure on the ability to discnmmate range differences is studied in a phantom target experiment in which the bats’ vocalizations are used to trimer the emission of a playback ‘echo‘. Play back ‘echoes’ tested are differently filtered versions of a typical Eptrsicus call, and noise pulses of equivalent spectral content. The good ranging performance with these artificial echoes questions the concept of a tem poral crOSScOrr&tiOn reccwr for ranging in echolocating bats. 57. .
S~~RLVKKE A:
IMOGDANS J, Two-wavefront
S~~INI’I’%II:H
Echoes
HLI, OSTXCAI.IIJ: Discrimination of by the Big Brown Bat, Eptesicus
in echolocating
bats Neuweiler
and Schmidt
fuscus. Behavioral Experiments and Receiver Simulations. ./ Con@ Ph)siol /A] 1993, 172:309-- 323. The study characterizes the ahilit) of IS Jirscus to discriminate between structured phantom targets with two echo wavefronts and a target with one echo wavefront. Several functional models of echo processing are discussed. While an energ) detector model fails to account for the discrtmination performance, both a temporal cross-correlation receiver and a spectral correlation model match the behavioral data. For heuristic reasons, it is suggested that the bats perceived differences in echo spectra rather than estimating range in this discrimination task. 58.
W: Nrzrrul Nets in Lktric MIT Press: 1991.
HEIUGENRERG
I+sb. Cambridge,
G Neuweiler and S Schmidt, Zoologisches Institut der I’niversitat, Box 20 21 36, D HO021 Munchen, Germany.
Mk
PO
569
lnstitut
In bat audition,
in echolocating
Neuweiler
and Sabine Schmidt
der Ludwig-Maximilians-Universitit,
major advances
tuning in the bats’ cochlea, information
bats
processing,
Current
have been made concerning
cortical
maps and the related
and the perceptual images.
Opinion
Mtinchen,
in Neurobiology
mechanisms
Germany
the frequency
subcortical creating
echo
auditory
1993, 3:563-569
Introduction
frequency tuning observed derstood [ 5 ]
In man and many mammals, perception of the outside world is dominated by the visual system. In contrast, echolocating mammals orient themselves by acoustical cues extracted from echoes of their emitted echolocation sounds. For studying neuronal processing of auditoty information, therefore, echolocating bats provide good models offering several experimental advantages including the existence of well differentiated nuclei of the ascending auditory pathway which are hypertrophied to various degrees, and the use of well defined echolocation signals as biologically relevant stimuli. These signals are species-specific and simply structured: they consist either of brief (0.5-5ms) frequency modulated (FM) sweeps only, or they can be combined with a longer (5-50 ms) constant frequency (CF) element (CF-FM signals). The echoes, which carry the information about the acoustical qualities of the bat’s environment, will be distorted replicas of these simple echolocation signals and will always occur time-locked to a preceeding vocalization.
Horseshoe bats, Rbinolophus rouxi, and mustached bats, Ptevonotusparnellii, are good models to study mechanisms of fine-tuning in the cochlea. These echolocating bats emit long lasting (10-100 ms) pure tones at an individual frequency within a narrow species-specific range (6G62 kHz in P, parnellii and 76-80 kHz in R. rouxi>. These tonal signals serve as carriers for brisk echo modulations imposed onto the pure tone echo by the beating wings of flying insects, the prey of these bats (for review see [4]). The bats’ cochleae feature an ‘auditory fOVea’: the narrow frequency band of a few kilohertz around the personal echo-frequency is represented in an expanded way and covers nearly a complete half turn of the cochlea [ 6,7]. Tuning curves of auditov units tuned to the fovea are extremely narrow (Qlodu-vdlues of up to 500 compared with a maximum of 2&3O in units receiving afferents from non-fovea1 parts of the cochlea, or from unspecialized cochleae of other echolocating bats or other mammals; for reviews see [3,4] ).
This review focuses on three controversial issuesnamely, fine frequency analysis in the cochlea, the computational maps and functional subdivisions of the auditory cortex and their possible subcortical substrates, and acoustical imaging by echolocating bats. For more detailed reviews on audition in echolocating bats see
This ultrafine tuning within the auditory fovea is correlated with distinct structural and cellular specializations of the organ of Corti just basal to the fovea1 section. These pecularities are thought to create reverberations [&lo] To account for the ultrafine tuning, it is necessaq to consider two components, namely, a predominantly passive mechanical resonator (established by the basilar membrane structure) and an electromechanical feedback from the OHCs, which is superimposed onto the mechanical oscillations and produces additional sensitiviq and sharp tuning.
11-41.
Fine frequency
analysis
in the cochlea
of bats
the mammalian auditor)l system, frequency analysis is achieved in the cochlea by a bank of low pass frequency filters, based on mechanical gradients of the basilar membrane. Outer hair cells (OHC) may add an active electro~mechanical element for increasing the sensitivity and fine-tuning of the cochlear frequency filters. How these mechanisms combine to achieve the narrow
in all mammals
is not yet un-
In
Mechanical resonance
Structural modifications of the organ of Corti, such as conspicuous thickenings of the basilar membrane, provide a steep, localized impedance discontinuity at the basal end of the fovea1 part of the basilar membrane. Incoming wdves of a frequency (resonance frequency) vev
Abbreviations AVCN manteroventral
cochlear
MNTB--medial OHC-outer
nucleus;
nucleus
of the
CF-constant trapezoid
frequency; body;
hair cell; PVCN-posteroventral
@
Current
FM-frequency
MSO-medial
cochlear
Biology
superior
modulated; olive;
nucleus;VNLL-ventral
Ltd ISSN 0959-4388
MGB-medial
OAE--otoacoustic nucleus
of the
geniculate
body;
emission; lateral
lemniscus.
563
564
Sensory
systems
close to the bat’s individual echo frequency should reverberate between the place of the impedance discontinuit) and the oval window [ 111. Evidence for such a reverberating system are ringing microphonics and otoacoustic emissions (OAE), which have a frequency just below that of the bat’s individual echo frequency and which are represented on the basilar membrane just apical to the place where the impedance discontinui? occurs [7,12], As in humans and laboratory mammals, frequencies of OA!Zs in bats are identical to those of high auditory sensitivity, This reverberating mechanical system may not only guarantee a high sensitivity at the echo-frequency, but also create a peak of insensitivity for frequencies slightly below the echo-frequency. For example, it has been suggested that interferences between the undamped resonator and lower stimulus frequencies produce the steep low-frequency flank of the sharply tuned echo filter in P. puvnellii, which may add to tuning and shut off the fovea1 frequency band from impacts of lower frequencies (M KZjssl, unpublished data). In mustached bats, it has been shown that the cochlear resonance frequency shifts along with body temperature and increases by 150 Hz when the bat is flying [13-l 51. The bat adjusts its emitted echolocation frequency to the shifting resonance. The small temperature eff‘ects (39 Hz “Cl) are consistent with a tuning mechanism that critically depends on mechanical interactions. Apparently these bat species, focusing fine frequency analysis onto a vety narrow individual band rather than evolving new filter systems, have enhanced the efficiency of frequency analysis of common mammalian mecha~ nisms to their limits.
Electromechanical membrane
feedback from
OHCs
to the basilar
oscillations
Two-tone distortions generated in the inner 6‘dr indicate non-linear amplifications thought to originate from OHC excitations which feed back to mechanical oscillations of the basilar membt-dne. Such distortions can be measured acoustically in the outer ear of bats. In mustached bats, large levels of the distortions close to the CF-frequenq can only be elicited with small frequency separations of the two tones [ 161. This indicates a high sensitivin and an outstanding mechanical frequency resolution in the cochlea. Like the OHCs of other mammals, bat OHCs contain a lateral subsurface cisternae system [9] which is thought to be involved in OHC motility. Application of salicylate, which is known to block OHC motility, was recent11 shown to reduce the level of distortion products bl 25-36 dB [ 171. This is indeed suggestive of a contribution from OHC motility to distortion production and hence to the generation of low auditory thresholds. The length of the OHCs and their stereocilia is remarkably constant within the basal cochlear turn of horseshoe bats [8,9] ; this may provide a basis for the expanded rep-
resentation (fovea).
of the narrow
echolocation
frequency
band
In the cochlea of bats, micromechanical processes in the OHCs may produce a high sensitivity and contribute to the fovea1 frequency representation. They are superimposed and fed back on macromechanical resonance which is crucial for enhanced tuning and the creation of local insensitivities. They shut off extremely fine fre cpency separation in the echo-frequency range from conventional frequency tuning at lower frequencies.
The role of the medial echolocating
superior
olive
in
bats
The medial superior olive (MSO) is considered to compute interaural time differences for coding the direction of a stimulus. In laboratory mammals, MS0 units get excitatory projections from the left and right anteroventral coclear nuclei (AVCN). According to Jeffress’ model which (cited in [ 181) the MS0 acts as a cross-correlator codes interaural time differences by excitatory delay lines feeding into MS0 coincidence detectors. The most convincing evidence for this model comes from work by Yin and Chan [ 181. But studies in echolocating bats have now questioned whether this concept of interaural time coding is applicable to the MS0 of all mammals [ 19-21,22-l. Neurons of the MS0 in echolocating bats behave entirely differently from those in carnivores [ 21,22-l. Most units are only excited from the contralateral AVCN and receive no input from the ipsilateral AVCN. In addition, these monaural units get strong glycinergic input from the medial nucleus of the trapezoid body (MNTB) which turns the originally sustained excitatory response into a brisk, phasic one. This was recently demonstrated by application of the glycineantagonist, strychnine [22*]. In echolocating bats, the MS0 is thus turned into a monaural circuitry with a strictly phasic output caused b> a strong inhibitory input from the MNTB. This inhibitoq pathway also exists in non-echolocating mammals, but is a very weak input by comparison with the strong excitatory afferences from both ears. At present, it is an enigma why in echolocation the ipsilateral excitatov input to the MS0 should be suppressed and the inhibitory input from the MNTB enhanced. Recordings from MS0 units suggest that they are well adapted to code and analyze amplitude modulations and their repetition rates in echo signals [ 22.1, Such repetitive modulations ny;1)’be caused by wing beats of the bats’ prey.
Ascending
auditory
pathway
and precise time
coding In echolocating bats, transmitter distributions and their functional impact in the ascending auditory pathway generaIll, conform to that found in non-echolocating mammals [23-271, However, the bat pathway contains an
Audition
additional functionally important substance, the Ca2+ binding protein ‘calbindin’. In the barn owl, calbindin has been associated with binaural circuits requiring precise time coding for processing directional cues [ 281. In contrast, a study in the mustached bat demonstrated that somata and nerve endings containing calbindin are predominantly seen in monaural nuclei [ 291. The calbindincontaining pathway starts from globular cells of the AVCN and from octopus cells of the posteroventral cochlear nucleus (PVCN) and projects, directly and via the MNTB, to the ventral nucleus of the lateral lemniscus (VNLL). The VNLL is hypertrophied and highly organized in monocellular sheets with large calyx-synapses in three different bat species [30] and in echolocating dolphins. Units of this specific nucleus respond in an exclusively phasic manner, with latencies unaltered by sound intensity and frequency. Such constant latencies are thought to be achieved by input integration over a wide array of afferents with different best frequencies, and, additionally, by high excitatory thresholds [ 301. All units of this nucleus precisely preserve timing information and, therefore, this pathway may be a prerequisite for calculating travel time between outgoing sound and returning echo. Travel time indicates the range between an echolocating bat and a target.
Cortical circuits
map of echo-ranging
and neural
for range finding
The first auditory cortex which could be clearly differentiated into functional and behaviourally relevant subdivisions was that of echolocating bats [31]. In the mustached bat, Suga and his colleagues described, among other divisions, a cortical ‘range-finding at-cd’. Neurons of this area are facilitated by pairs of FM stimuli with specific differences between first and second stimulus which mimic emitted sound and returning echo. This specific sensitivity to stimulus pairs qualifies such ‘FMFM units’ for coding travel time between emitted pulse and echo, and hence target range. The ‘best delays’ range from 0.4 to 18ms (corresponding to target ranges from 7 to 310cm) and are represented in a frontocaudal axis of the cortex. Excitation will shift from posterior to frontal places in the range finding area as a hunting bat approaches a flying insect. This basic concept of a computational range-finding map in the auditory cortex [32] has recently been refined and extended to other bat species [33-371. In spite of more than a decade of research, the neuronal circuits creating such precisely customized echosignalspecifity and delay-specifity in the cortex are not yet known. Units of a specifity similar to that of the rangefinding cortical units have been discovered in the medial geniculate body (MGB) but not in the interior colliculus which supplies the main auditory input to the MGR [38,391. Suga and his colleagues [l] have described a neural network that they designed for delay calculation based on
in echolocating
bats
Neuweiler and Schmidt
delay lines created by synaptic and axonal delays (for delays < 4 ms) and synaptic inhibition (delays > 4 ms). They assume that such a thalamic cross correlator (delay line) gets its input from collicular units tuned to different portions of FM signals. Inputs to the delay line should respond to a stimulus by only one spike and with a latency which is extremely constant and invariant to stimulus amplitude. Such time-coding lmits of high precision have been found in the VNLL [30]. However, this lemniscal nucleus only projects to the inferior colliculus, and collicular inputs to the MGB of similar or even higher precision of time coding have not yet been described. It seems that precise time coding disappears in a ‘Bermuda triangle’ between the lower level VNLL and the MGB, where it reappears. Studies on synaptical levels may finally elucidate how delay lines are established and time filters are created for tuning neurons to specific echo-delays, and hence to specific target distances. In the auditoty cortex of horseshoe bats and mustached bats, there is another large area which is specifically tuned to pure tones (CF) within the individual, narrow frequency band of the CF component in the echo-signal [40,41]. This cortical CF area is well suited for fine frequency discrimination because the units are extremely narrowly tuned and the narrow frequency band (which, for example, is 6&63 kHz in mustached bats) is tonotopically represented in an expanded fashion. In behavioral experiments, horseshoe bats and mustached bats detect deviations from the echo frequency as small as 50Hz or 0.06%. When muscimol, a potent agonist of y-aminobutyric acid, was applied to the CF area, fine frequency discrimination for frequency differences up to 0.5 kHz was temporarily disrupted whereas coarse frequency discrimination was not affected [42], Units of the CF area are facilitated when a pure tone of the echo-frequency is preceded by an FM stimulus similar to that emitted at the end of the echolocation signal [43*]. This is still another correlate to the neuronally and behaviorally well established fact that vocalization of an echolocation signal opens auditory time windows for enhanced echo processing (for review see [4] ). Thus, the CF area could serve as a fine frequency analyzer for even minute spectral cues imprinted onto the echo.
Regulation
of echo level during
target
approach In addition to using the ability of echo processing neurons to cope with a wide dynamic range [30], bats use two mechanisms to compensate for range-dependent changes in echo level. The first is to lower the level of their sonar calls with decreasing target distance, an effect that has recently been systematically described [44,45]. The second mechanism involves reducing the sensitivity of the ears during sonar emissions by muscular activity in the middle ear and central suppression of the excitation. The time characteristic for regaining full sensitivity after a vocalization has been
565
566
Sensory
systems
regarded as an automatic gain control mechanism for targets closer than about 1 m [46]. Accordingly, the target detection thresholds decrease by about 11 dB per doubling of target range [46,47*], which is similar to the increase in echo level of a point target. More complex perceptual processes seem to be involved in a recent experiment where two targets were presented simultaneously at different distances [48*]. When interpreted in terms of an automatic gain control mechanism, the results of this experiment suggest an increase of auditory sensitivity by only 6dB per doubling of target range, AS an alternative interpretation, one might conjecture that the bats just estimated the loudness of the more distant target.
Towards a theory
of acoustical
imaging
Echolocating bats determine target range from the time difference between the emission of a sona.r call and the arrival of its echo [49]. Information about the object’s surface structure is encoded in a spectral deformation of the echo, which raises the question of how bats extract this information when discriminating between structured targets [ 501. A unified theov of echolocation has been developed that regards bat sonar as a means to create an auditoty image of space comparable to visual space representation [ 51,521. According to this theov, the tem~ poral information of the echo is retained while spectral information is transformed to temporal information by the auditol): system. Then, a temporal cross~correlationlike process integrates both object position and structure into a unified spatial acoustic image, which is ultimatel) perceived by the bats. The appeal of this theoT is that it promises to account for the discrimination of target distance. time jitter in the echoes, and object structure in terms of a single perceptual process. It is surprising, at least, that the largely d&rent time delays associated with the experimental threshold \ralucs for absolute distance determination (50--l 00 ps ) [49], structure discrimination ( - 1 ps) [ 53*]. and time jitter ( - 10 ns) [ 541 should be explained by a unified the0~. Simmons (e.g. [ 551) attributes these di&rences to experimental difficulties, such as the inevitable head movements of bats comparing two targets. Moreover, the experimental evidence for the transfornmation of spectral into temporal information by the bat’s auditoT system is not entirely convincing, as the time differences corresponding to the structures in question of 46 /-IS [ 511 and 100 ps [ 521, respectively, are of the order of the bat’s distance discrimination threshold. Therefore, even if the bats have measured time delays in these experiments, this finding cannot be extrapolated to account for texture discrimination in general, where differences in surface depth corresponding to time differences of only a few microseconds are discriminated by the bats. Incidentally, recent distance discrimination experiments, in which the echoes were substituted by filtered versions of a typical bat call or noise pulses, have raised some
doubt about the use of a temporal cross-correlation-like process for absolute distance determination [ 56.1. Of late, the unified theory of echolocation (see [52] has been challenged on both the functional and the perceptual level. Two studies [ 53*,57*] on the ability of echoloeating bats to discriminate between structured targets consisting of two reflective surfaces (two-front targets) have shown for the first time that a bat’s performance can be satisfactorily explained by a model based on the processing of echo spectra. Functionally, this description may be preferable to that by temporal cross-correlation as the physiological requirements of the spectral model (i.e., a frequency resolution on the order of a few kilohertz) are easily met, while the neuronal timing accuracy (below 1 ps) required by the temporal cross-correlation receiver has not been established in bats or other mam mals. On the perceptual level, Schmidt [53-j has pointed out that if bats use a note-monotonous function (for example, a cross-correlation function) to set up a psychologied depth scale, a convoluted image of space is obtained, as certain distinct points in space are represented 1,) the same image point. It is questionable why bats should have evolved a unique mechanism to obtain an inaccurate representation of small spatial structures. On the other hand, the assumption of a monotonous time function is incompatible with the experimental data [ 53*]. Due to such difficulties with a purely spatial interpretation, both studies [53*, 57.1 dismiss the idea of a unified representation of echo information, and propose that target distance and structure are different perceptual qualities, target structure being perceived as a timbre or coloration of the echo. The perception of this acoustical qualiv does not prey suppose a specific adaptation of bat sonar, but is rather a general abilip of the mammalian auditory system. The \iew that echo timbre is actuall!. used by the bats to solve texture discrimination tasks is supported by the finding that bats pre\iousl!~ trained to discriminate texture in an echolocation exp’eriment spontaneousl!, discriminate between colored sc~ids presented independentI> of the animals’ vocalizatio~7s [ 5301. A model that :111o~vsl’or perceptual qualities other than the mere temporal imaging postulated by the unified theon, ma!’ also account for a discrepancy obsened in the discrimination performance of the bats in identical experimental situations. depending on the initial training: Mogdans ct al. [ 570 j found that bats discriminated a twofront target with an internal time delay of 100 ps from an unstructured target in more than 90% of the tests if they had first been trained in a texture discrimination task (the discrimination of structured targets with variable internal delay from the unstructured target) and if the first echo front of the two-front target and the unstructured target were presented at the same absolute time delay. In con trast, only 7G?5% correct choices were recorded for the identical target setting [52], when the animals had been trained to a ranging task, i.e. to the 100 ps two-front target presented at a fixed absolute delay and an unstructured target presented at variable absolute delays. In view of
Audition
these observations we propose that a theory of acoustical imaging by bat sonar should incorporate several different discrimination strategies.
Conclusions The classic questions in auditory research of echolocation are still of continuing interest. The concepts for fine frequency analysis in the cochlea have become even more numerous and more complex. Non-invasive methods of analyzing cochlear mechanisms have been fully exploited. A real understanding of the mechanical and electromechanical filter systems will only be achieved by studying vibrational motions of the basilar membrane and by recordings from hair cells. In contrast to neuronal time coding in electroreceptive fish [58], the neural circuits for computing echo travel time and for precise time marking of auditory events in echolocation are not yet known. However, substrates have been identified (MGB and VNLL) where studies on the synaptic connectivities by intracellular recordings and and in tissue slices may patch-clamping methods in zu’z~o give us guidelines into the labyrinth of subcortical echo information processing. The long lasting and ongoing dispute over a predominantly temporal or spectral basis of acoustical imaging is currently bringing forth a more pluralistic attitude, which admits several concurrent perceptual mechanisms. The development of more precise models of how these mechanisms cooperate will require further behavioral experiments characterizing the temporal and spectral properties of the bats’ auditory system.
5.
References
for many suggestions
and recommended
Papers of particular interest, published review, have been highlighted as: of special interest of outstanding interest
and critical
reading
within
the annual
period
6.
VATEK
7
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N, OLSEN JF, I~IITI~AN JA: Specialized Subsystems for Processing Biologically Important Complex Sounds: Crosscorrelation Analysis for Ranging in the Bat’s Brain. Cold Spring Hurb Symp Quant Rio1 1990, 55:585%597.
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GD, CASEDAY JH: 7hr Neural tn Rats Berlin: Springer Verlag; 1989.
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H~NS~X MM, HENSON OW: Specializations for Sharp Tuning in the Mustached Bat: The Tectorial Membrane and Spiral Limbus. Hem Kes 1991, 56:122&132.
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KOSSI. M. VATER M:
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KULX’AHARAN, LOOK JM Projections to the Medial Superior Olive from the Medial and Lateral Nuclei of the Trapezoid Body in Rodents and Bats. J Comp Neural 1992, 324:522-538.
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Two-tone Distortions from the Bat Pteronotus pamellii Re1992, Tuning. Natrrrzc,i~~erIscl,~l
M: High Frequency Distortion Products from the Ears of 2 Bat Species, Megaderma Myra and Carollia perspicillata. Hear Rrs 1992, 60:15&164. TCT, CHAN JCK: Interaural Time Superior Olive of Cat. ./ Neuropbysio/
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8.
of
S&A
bats Neuweiler
DALL.05 P, COKEY
in Cochlear
Acknowledgements We thank M Kossl and B Grothe reading of the manuscript
in echolocating
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This recent publication
may pave the way for a long awdited new IkId of
research: the neuronal analysis of complex spectral features of echoes which prObdbly code paranwters crucial for target identification. -l-t.
HAKTIYY DJ: Stabilization
of Perceived Echo Amplitudes in Echolocating Bats. II. The Acoustic Behavior of the Big Brown Bat, Eptesicus fuscus, when Tracking Moving Prey. J Aco~rst Sot Am 1992, 91:1133-1149.
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VocalJ .E@
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SIMRK)NSJA, MOFFAT ALM, MASTEK~K’M: Sonar Gain Control and Echo Detection Thresholds in the EchoIocating Bat, Eptesicus fuscus. .J Acoust Sot Am 1992, 91:115(tll63. Echo detection thresholds van: with target distance due to the middle ear muscle activiy associated with sonar emissions. Although backward masking by clutter echoes is excluded in this study, the echo detection thresholds determined confirm the previously described Improvement m thresholds of 11 dB per doubling of target range [46]. This finding must be compared with [&=I,
47. .
48.
IiARTLEY DJ: Stabilization of Perceived Echo Amplitudes in Echolocating Bats. I. Echo Detection and Automatic Gain Control in the Big Brown Bat, Eptesicus fuscus, and the Fishing Bat, Noctilio leporinus. ,J Amus/ Sot Am 1992, 91:112@1132. In the first part of the paper, the backward masking effect of clutter echoes from the loudspeaker on the detectabiliy of a phantom target is studied, and receiver operating characteristics for target detection are obtained. Neither question has been explicitly addressed in former studies with echolocating bats. A second experiment mvestigates how bats evaluate the level of a far phantom target in the presence of a near phantom target of constant level. The results are presented as evil dence for a reduction of auditoy sensithity (due to middle ear muscle contractions and /or central suppression) by 6 dB per halving of target range, which contradicts the findings reported in [46,47]. .
49.
SIMMONSJA: The Resolution of Target Range by Echolocating Bats. J z‘kO/tSt sac AI12 1973, 54:157 173.
50.
SIMMONS JA. LALTNDERWA, LAVENIXK BA, IXIKOSHO~ CF, KIEFEKSW, I.&IL~NGSTOS R, SCALLETAC, CKOU’IEY DE: Target
36
MAEKAuA M, WONG D, I-‘.ksct~
37.
SHAVNONHARTMANS, Wow
38.
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52.
39.
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of Structured Phantom Targets in the Echolocating Bat, Megaderma lyra. ,I Acoust Sot Am 1992, 91:2203-2223. The ability of LX !JVZ to discriminate between structured phantom tar gets with two echo fronts is characterized, and different functional mode els of echo processing are tested. The results show that the discrimination of target surface stmcturr can be explained as a discrimination of echo spectra. A dual perceptual model of echolocation is supported which holds that the hats perceive object distance and texture as sep arate qualities.
WG: Spectral Selectivity of FM-FM Neurons in the Auditory Cortex of the Echolocating Bat, Myotis lucz~ugus. J Cow@ P&iol [Al 1992, 171:513-522. D, MA~,KAUC’ M: A Processing
of Pure-tone and FM Stimuli in the Auditory Cortex of the FM Bat, Myotis lucifugus. Hear Rm 1992, 61:179-188.
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40.
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41.
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for Bat’s
Structure and Echo Spectral Discrimination ing Bats. Science 1974, 186:1130~1132. il.
1992, @%:1613-1623.
of the DSCF Cortex with Muscimol Disrupts Frein the Mustached Bat. J Neurop/qsio/
Basis for Target DiscrimBats. .I ncozrsf Sot Am 19X9,
SIMM~~VS JA, Moss CF, FERRAGAMOM: Convergence of Temporal and Spectral Information into Acoustic Images of Complex Sonar Targets Perceived by the Echolocating Bat, Eptesicus fuscus. .I Camp P@iol iA/ 1990, 166:44W70.
53. .
SCFIMID~S: Perception
54.
SIMMONSJA, FEIUXAGAMO M, Moss CF, STCVENSONSD, ALXS RA: Discrimination of Jittered Sonar Echoes by the Echolocating Bat Eptesicus fuscus The Shape of Target Images in Echolocation. J Camp Pblsiol /A/ 1990, 167:58=16.
KIQ~JIMARO~JX II, GAI~NI SJ, SXA N: Inactivation
Area of the Auditory quency Discrimination
SIMMONSJA, CHKN I.: The Acoustic
ination by FM Echolocating 86:1333-1350.
155:821-834.
42.
by Echolocat-
55.
SIMMONSJA, GR~NNELL AD The Performance
Acoustic
Images
Perceived
by Echolocating
of Echolocation: Bats. In Arzimal
Audition
56 .
Target Ranging and the Role of Time-Frequency Structure of Synthetic Echoes in Big Brown Bats, Eptesesicus fuscus. .I Camp P!?vsiol [A] 1992, 170:83-92. The impact of echo structure on the ability to discnmmate range differences is studied in a phantom target experiment in which the bats’ vocalizations are used to trimer the emission of a playback ‘echo‘. Play back ‘echoes’ tested are differently filtered versions of a typical Eptrsicus call, and noise pulses of equivalent spectral content. The good ranging performance with these artificial echoes questions the concept of a tem poral crOSScOrr&tiOn reccwr for ranging in echolocating bats. 57. .
S~~RLVKKE A:
IMOGDANS J, Two-wavefront
S~~INI’I’%II:H
Echoes
HLI, OSTXCAI.IIJ: Discrimination of by the Big Brown Bat, Eptesicus
in echolocating
bats Neuweiler
and Schmidt
fuscus. Behavioral Experiments and Receiver Simulations. ./ Con@ Ph)siol /A] 1993, 172:309-- 323. The study characterizes the ahilit) of IS Jirscus to discriminate between structured phantom targets with two echo wavefronts and a target with one echo wavefront. Several functional models of echo processing are discussed. While an energ) detector model fails to account for the discrtmination performance, both a temporal cross-correlation receiver and a spectral correlation model match the behavioral data. For heuristic reasons, it is suggested that the bats perceived differences in echo spectra rather than estimating range in this discrimination task. 58.
W: Nrzrrul Nets in Lktric MIT Press: 1991.
HEIUGENRERG
I+sb. Cambridge,
G Neuweiler and S Schmidt, Zoologisches Institut der I’niversitat, Box 20 21 36, D HO021 Munchen, Germany.
Mk
PO
569