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Journal of Comparative Physiology A

, Volume 189, Issue 6, pp 435–446 | Cite as

Fine control of call frequency by horseshoe bats

  • M. Smotherman
  • W. Metzner
Original Paper

Abstract

The auditory system of horseshoe bats is narrowly tuned to the sound of their own echoes. During flight these bats continuously adjust the frequency of their echolocation calls to compensate for Doppler-effects in the returning echo. Horseshoe bats can accurately compensate for changes in echo frequency up to 5 kHz, but they do so through a sequence of small, temporally-independent, step changes in call frequency. The relationship between an echo's frequency and its subsequent impact on the frequency of the very next call is fundamental to how Doppler-shift compensation behavior works. We analyzed how horseshoe bats control call frequency by measuring the changes occurring between many successive pairs of calls during Doppler-shift compensation and relating the magnitude of these changes to the frequency of each intervening echo. The results indicate that Doppler-shift compensation is mediated by a pair of (echo)frequency-specific sigmoidal functions characterized by a threshold, a slope, and an upper limit to the maximum change in frequency that may occur between successive calls. The exact values of these parameters necessarily reflect properties of the underlying neural circuitry of Doppler-shift compensation and the motor control of vocalization, and provide insight into how neural feedback can accommodate the need for speed without sacrificing stability.

Keywords

Doppler-shift compensation Echolocation Horseshoe bats Sensory feedback Sensory-motor integration 

Abbreviations

DSC

Doppler-shift compensation

Fecho

echo frequency

FVOC

vocalization frequency

ΔFVOC

change in call frequency

Notes

Acknowledgements

We thank Dr. R. Krahe for discussion and comments and K. Beeman for designing and tailoring most of the soft- and hardware used to simulate Doppler shifts. We are particularly grateful to Professors Shuyi Zhang and Wang Sung of the Chinese Academy of Sciences for invaluable help in collecting the bats and the Scientific Commission on Endangered Species and the Chinese Forestry Department for issuing the export permits. Supported by grants from NIH to W.M. (DC02538) and to M.S. (DC00397). All experiments comply with the Principles of animal care, publication No. 86-23, revised 1985 of the National Institute of Health and also with current US laws.

References

  1. Behrend O, Kössl M, Schuller G (1999) Binaural influences on Doppler shift compensation of the horseshoe bat Rhinolophus rouxi. J Comp Physiol A 185:529–538CrossRefPubMedGoogle Scholar
  2. Gaioni SJ, Riquimaroux H, Suga N (1990) Biosonar behavior of mustached bats swung on a pendulum prior to cortical ablation. J Neurophysiol 64:1801–1817PubMedGoogle Scholar
  3. Grinnell AD (1989) Sensory-motor control: listening to the voice within. Nature 341:488–489PubMedGoogle Scholar
  4. Kobler JB, Wilson BS, Henson OW Jr, Bishop AL (1985) Echo intensity compensation by echolocating bats. Hear Res 20:99–108PubMedGoogle Scholar
  5. Konstantinov AI, Makarov AK, Movchan EV, Sokolov BV, Goriniskii IA (1988) Sensory system for echolocation in horseshoe bats (in Russian). Russian Academy of Sciences, MoscowGoogle Scholar
  6. Long GR, Schnitzler HU (1975) Behavioural audiograms from the bat, Rhinolophus ferrumequinum. J Comp Physiol 100:211–219Google Scholar
  7. Metzner W (1989) A possible neuronal basis for Doppler-shift compensation in echo-locating horseshoe bats. Nature 341:529–532PubMedGoogle Scholar
  8. Metzner W (1993) An audio-vocal interface in echolocating horseshoe bats. J Neurosci 13:1899–1915PubMedGoogle Scholar
  9. Metzner W, Zhang SY, Smotherman MS (2002) Doppler-shift compensation behavior in horseshoe bats revisited: auditory feedback controls both a decrease and an increase in call frequency. J Exp Biol 205:1607–1616PubMedGoogle Scholar
  10. Neumann I, Schuller G (1991) Spectral and temporal gating mechanisms enhance the clutter rejection in the echolocating bat, Rhinolophus rouxi. J Comp Physiol A 169:109–116PubMedGoogle Scholar
  11. Neuweiler G (2000) The biology of bats. Oxford University Press, New YorkGoogle Scholar
  12. Neuweiler G, Metzner W, Heilmann U, Rubsamen R, Eckrich M, Costa HH (1987) Foraging behaviour and echolocation in the rufous horseshoe bats, Rhinolophus rouxi, of Sri Lanka. Behav Ecol Sociobiol 20:53–67Google Scholar
  13. Pillat J, Schuller G (1998) Audiovocal behavior of Doppler-shift compensation in the horseshoe bat survives bilateral lesion of the paralemniscal tegmental area. Exp Brain Res 119:17–26CrossRefPubMedGoogle Scholar
  14. Rübsamen R, Schuller G (1981) Laryngeal nerve activity during pulse emission in the CF-FM bat, Rhinolophus ferrumequinum. II. The recurrent laryngeal nerve. J Comp Physiol A 143:323–327Google Scholar
  15. Schnitzler HU (1967) Compensation of Doppler effects in horseshoe bats. Naturwissenschaften 54:523PubMedGoogle Scholar
  16. Schnitzler HU (1968) Die Ultraschallortungslaute der Hufeisennasen-Fledermäuse (Chiroptera, Rhinolophidae) in verschiedenen Orientierungssituationen. Z Vergl Physiol 57:376–408Google Scholar
  17. Schnitzler HU (1973) Control of Doppler shift compensation in the greater horseshoe bat, Rhinolophus ferrumequinum. J Comp Physiol 82:79–92Google Scholar
  18. Schnitzler HU, Henson OWJ (1980) Performance of airborne animal sonar systems. I Microchirotera. In: Bushnel RG, Fish JF (eds) Animal sonar systems. Plenum Press, New York, pp 109–181Google Scholar
  19. Schuller G (1974) The role of overlap of echo with outgoing echolocation sound in the bat, Rhinolophus ferrumequinum. Naturwissenschaften 61:171–172Google Scholar
  20. Schuller G (1977) Echo delay and overlap with emitted orientation sounds and Doppler-shift compensation in the bat, Rhinolophus ferrumequinum. J Comp Physiol 114:103–114Google Scholar
  21. Schuller G (1986) Influence of echolocation pulse rate on Doppler-shift compensation control system in the greater horseshoe bat. J Comp Physiol A 158:239–246Google Scholar
  22. Schuller G, Pollak GD (1979) Disproportionate frequency representation in the inferior colliculus of Doppler-compensating greater horseshoe bats, Rhinolophus ferrumequinum. J Comp Physiol 132:47–54Google Scholar
  23. Schuller G, Suga N (1976) Storage of Doppler-shift information in the echolocation system of the 'CF-FM' bat, Rhinolophus ferrumequinum. J Comp Physiol 105:9-14Google Scholar
  24. Schuller G, Beuter K, Schnitzler HU (1974) Response to frequency-shifted artificial echoes in the bat, Rhinolophus ferrumequinum. J Comp Physiol 89:275–286Google Scholar
  25. Schuller G, Beuter K, Rübsamen R (1975) Dynamic properties of the compensation system for Doppler-shifts in the bat, Rhinolophus ferrumequinum. J Comp Physiol 97:113–125Google Scholar
  26. Simmons JA (1974) Response of the Doppler echolocation system in the bat, Rhinolophus ferrumequinum. J Acoust Soc Am 56:672–682PubMedGoogle Scholar
  27. Simmons JA, Fenton MB, O'Farrell MJ (1979) Echolocation and pursuit of prey by bats. Science 203:16–21PubMedGoogle Scholar
  28. Smotherman M, Metzner W (2003) Effects of echo intensity on Doppler-shift compensation behavior in horseshoe bats. J Neurophysiol 89:814–821PubMedGoogle Scholar
  29. Smotherman MS, Zhang S, Metzner W (2003) A neural basis for auditory feedback control of vocal pitch. J Neurosci 23:1464–1477PubMedGoogle Scholar
  30. Suga N, Simmons JA, Jen PH (1975) Peripheral specialization for fine analysis of Doppler-shifted echoes in the auditory system of the "CF-FM" bat Pteronotus parnellii. J Exp Biol 63:161–192PubMedGoogle Scholar
  31. Tian B, Schnitzler HU (1997) Echolocation signals of the greater horseshoe bat (Rhinolophus ferrumequinum) in transfer flight and during landing. J Acoust Soc Am 101:2347–2364CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  1. 1.Department of Physiological ScienceUCLALos AngelesUSA

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