Summary
The tonotopic organization of the inferior colliculus (IC) in two echolocating bats,Hipposideros speoris andMegaderma lyra, was studied by multiunit recordings.
InHipposideros speoris frequencies below the range of the echolocation signals (i.e. below 120 kHz) are compressed into a dorsolateral cap about 400–600 Μm thick. Within this region, neuronal sheets of about 4–5 Μm thickness represent a 1 kHz-band.
In contrast, the frequencies of the echolocation signals (120–140 kHz) are overrepresented and occupy the central and ventral parts of the IC (Fig. 3). In this region, neuronal sheets of about 80 Μm thickness represent a 1 kHz-band. The largest 1 kHz-slabs (400–600 Μm) represent frequencies of the pure tone components of the echolocation signals (130–140 kHz).
The frequency of the pure tone echolocation component is specific for any given individual and always part of the overrepresented frequency range but did not necessarily coincide with the BF of the thickest isofrequency slab. Thus hipposiderid bats have an auditory fovea (Fig. 10).
In the IC ofMegaderma lyra the complete range of audible frequencies, from a few kHz to 110 kHz, is represented in fairly equal proportions (Fig. 7). On the average, a neuronal sheet of 30 Μm thickness is dedicated to a 1 kHz-band, however, frequencies below 20 kHz, i.e. below the range of the echolocation signals, are overrepresented.
Audiograms based on thresholds determined from multiunit recordings demonstrate the specific sensitivities of the two bat species. InHipposideros speoris the audiogram shows two sensitivity peaks, one in the nonecholocating frequency range (10–60 kHz) and one within the auditory fovea for echolocation (130–140 kHz).Megaderma lyra has extreme sensitivity between 15–20 kHz, with thresholds as low as −24 dB SPL, and a second sensitivity peak at 50 kHz (Fig. 8).
InMegaderma lyra, as in common laboratory mammals, Q10dB-values of single units do not exceed 30, whereas inHipposideros speoris units with BFs within the auditory fovea reach Q10dB-values of up to 130.
InMegaderma lyra, many single units and multiunit clusters with BFs below 30 kHz show upper thresholds of 40–50 dB SPL and respond most vigorously to sound intensities below 30 dB SPL (Fig. 9). Many of these units respond preferentially or exclusively to noise. These features are interpreted as adaptations to detection of prey-generated noises.
The two different tonotopic arrangements (compare Figs. 3 and 7) in the ICs of the two species are correlated with their different foraging behaviours. It is suggested that pure tone echolocation and auditory foveae are primarily adaptations to echo clutter rejection for species foraging on the wing close to vegetation.
Similar content being viewed by others
Abbreviations
- BF :
-
Best frequency
- CF :
-
constant frequency
- FM :
-
frequency modulated
- IC :
-
inferior colliculus
- HS :
-
Hipposideros speoris
References
Aitkin LM, Fryman S, Blake DW, Webster WR (1972) Responses of neurons in the rabbit inferior colliculus. I. Frequency-specificity and topographic arrangement. Brain Res 47:77–90
Békésy G von (1960) Experiments on hearing. McGraw-Hill, New York
Bodenhamer RD, Pollak GD (1981) Time and frequency domain processing in the inferior colliculus of echolocating bats. Hearing Res 5:317–335
Bruns V (1976) Peripheral auditory tuning for fine frequency analysis by the CF-FM bat,Rhinolophus ferrumequinum. II. Frequency mapping in the cochlea. J Comp Physiol 106:87–97
Feng AS, Vater M (1985) Functional organization of the cochlear nucleus of rufous horseshoe bats (Rhinolophus rouxi): frequencies and internal connections are arranged in slabs. J Comp Neurol 235:529–553
Gallyas F (1979) Silver staining of myelin by means of physical development. Neurol Res 1:203–209
Gustafson Y, Schnitzler HU (1979) Echolocation and obstacle avoidance in the hipposiderid bat,Asellia tridens. J Comp Physiol 131:161–167
Habersetzer J, Schuller G, Neuweiler G (1984) Foraging behaviour and Doppler shift compensation in echolocating hipposiderid bats,Hipposideros bicolor andHipposideros speoris. J Comp Physiol A 155:559–567
Huang C, Fex J (1986) Tonotopic organization in the inferior colliculus of the rat demonstrated with the 2-deoxyglucose method. Exp Brain Res 61:506–512
Irvine DRF (1986) The auditory brainstem. Progr Sens Physiol 7. Springer, Berlin Heidelberg New York, pp 1–279
Link A, Marimuthu G, Neuweiler G (1986) Movement as a specific stimulus for prey catching behaviour in rhinolophid and hipposiderid bats. J Comp Physiol A 159:403–413
Marimuthu G, Neuweiler G (1987) The use of acoustical cues for prey detection by the Indian false vampire bat,Megaderma lyra. J Comp Physiol A 160:509–515
Merzenich MM, Roth GL, Andersen RA, Knight PL, Colwell SA (1977) Some basic features of organization of the central auditory system. In: Evans EF, Wilson JP (eds) Psychophysics and physiology of hearing. Academic Press, London, pp 485–497
Neuweiler G (1970) Neurophysiologische Untersuchungen zum Echoortungssystem der Großen Hufeisennase,Rhinolophus ferrumequinum. Z Vergl Physiol 67:273–306
Neuweiler G (1984) Foraging, echolocation and audition in bats. Naturwissenschaften 71:446–455
Neuweiler G, Bruns V, Schuller G (1980) Ears adapted for the detection of motion, or how echolocating bats have exploited the capacities of the mammalian auditory system. J Acoust Soc Am 68:741–753
Neuweiler G, Singh S, Sripathi K (1984) Audiograms of a South Indian bat community. J Comp Physiol A 154:133–142
Neuweiler G, Metzner W, Heilmann U, Rübsamen R, Eckrich M, Costa HH (1987) Foraging behaviour and echolocation in the rufous horseshoe batRhinolophus rouxi of Sri Lanka. Behav Ecol Sociobiol 20:53–67
Ostwald J (1984) Tonotopical organization and pure tone response characteristics of single units in the auditory cortex of the Greater Horseshoe Bat,Rhinolophus ferrumequinum. J Comp Physiol A 155:821–834
Peters A (1987) Analyse der Frequenzrepräsentation im Innenohr der echoortenden FledermausHipposideros lankadiva. Diplomarbeit, TU München
Pollak GD, Schuller G (1981) Tonotopic organization and encoding features of single units in the inferior colliculus of horseshoe bats: functional implications for prey identification. J Neurophysiol 45:208–226
Pye JD (1980) Echolocation signals and echoes in air. In: Busnel RG, Fish JF (eds) Animal sonar systems. Plenum Press, New York London, pp 309–353
Rübsamen R (1987) Ontogenesis of the echolocation system in the rufous horseshoe bat,Rhinolophus rouxi. J Comp Physiol A 161:899–913
Schmidt S, Türke B, Vogler B (1984) Behavioral audiogram from the batMegaderma lyra. Myotis 22:62–66
Schnitzler HU, Menne D, Kober R, Heblich K (1983) The acoustical image of fluttering insects in echolocating bats. In: Huber F, Markl H (eds) Neuroethology and behavioral physiology. Springer, Berlin Heidelberg New York, pp 235–250
Schuller G (1980) Hearing characteristics of Doppler shift compensation of South-Indian CF-FM bats. J Comp Physiol 139:349–356
Schuller G (1984) Natural ultrasonic echoes from wing beating insects are encoded by collicular neurons in the CF-FM bat,Rhinolophus ferrumequinum. J Comp Physiol A 155:121–128
Schuller G, Pollak G (1979) Disproportionate frequency representation in the inferior colliculus of Doppler-compensating Greater Horseshoe Bats: evidence for an acoustic fovea. J Comp Physiol 132:47–54
Serviere J, Webster WR, Calford MB (1984) Isofrequency labelling revealed by a combined [14C]-2-deoxyglucose, electrophysiological and horseradish peroxydase study of the inferior colliculus of the cat. J Comp Neurol 228:463–477
Stiebler I, Ehret G (1985) Inferior colliculus of the house mouse. I. A quantitative study of tonotopic organization, frequency representation, and tone-threshold distribution. J Comp Neurol 238:65–76
Suga N (1969) Classification of inferior collicular neurones of bats in terms of responses to pure tones, FM sounds and noise bursts. J Physiol 200:555–574
Vater M (1982) Single unit responses in cochlear nucleus of horseshoe bats to sinusoidal frequency and amplitude modulated signals. J Comp Physiol 149:369–388
Vater M, Feng AS, Betz M (1985) An HRP-study of the frequency-place map of the horseshoe bat cochlea: morphological correlates of the sharp tuning to a narrow frequency band. J Comp Physiol A 157:671–686
Webster WR, Serviere J, Crewther D, Crewther S (1984) Isofrequency 2-DG contours in the inferior colliculus of the awake monkey. Exp Brain Res 56:425–437
Witzke P (1987) Passiv akustische Lateralisation bei der Lyra-Fledermaus,Megaderma lyra. Diplomarbeit, Fakultät Biologie, Universität München
Zook JM, Winer JA, Pollak GD, Bodenhamer RD (1985) Topology of the central nucleus of the mustache bat's inferior colliculus: correlation of single unit properties and neuronal architecture. J Comp Neurol 231:530–546
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Rübsamen, R., Neuweiler, G. & Sripathi, K. Comparative collicular tonotopy in two bat species adapted to movement detection,Hipposideros speoris andMegaderma lyra . J. Comp. Physiol. 163, 271–285 (1988). https://doi.org/10.1007/BF00612436
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00612436