Skip to main content
Log in

Echo delay versus spectral cues for temporal hyperacuity in the big brown bat, Eptesicus fuscus

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

Big brown bats can discriminate between echoes that alternate in delay (jitter) by as little as 10–15 ns and echoes that are stationary in delay. This delay hyperacuity seems so extreme that it has been rejected in favor of an explanation in terms of artifacts in echoes, most likely spectral in nature, that presumably are correlated with delay. Using different combinations of digital, analog, and cable delays, we dissociated the overall delay of jittering echoes from the size of the analog component of delay, which alone is presumed to determine the strength of the apparatus artifact. The bats' performance remains invariant with respect to the overall delay of the jittering echoes, not with respect to the amount of analog delay. This result is not consistent with the possible use of delay-related artifacts produced by the analog delay devices. Moreover, both electronic and acoustic measurements disclose no spectral cues or impedance-mismatch reflections in delayed signals, just time-delays. The absence of artifacts from the apparatus and the failure of overlap and interference from reverberation to account for the 10-ns result means that closing the gap between the level of temporal accuracy plausibly explained from physiology and the level observed in behavior may require a better understanding of the physiology.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4A–D.
Fig. 5.
Fig. 6A, B.
Fig. 7A–D.

Similar content being viewed by others

Abbreviations

FM:

frequency-modulated

XCR:

cross-correlation function

References

  • Altes RA (1989) Ubiquity of hyperacuity. J Acoust Soc Am 85:943–952

    CAS  PubMed  Google Scholar 

  • Beedholm K, Møhl B (1998) Bat sonar: an alternative interpretation of the 10-ns jitter result. J Comp Physiol A 182:259–266

    Article  CAS  PubMed  Google Scholar 

  • Boonman AM, Parsons S, Jones G (2003) The influence of flight speed on the ranging performance of bats using frequency modulated echolocation pulses. J Acoust Soc Am 113:617–628

    Article  PubMed  Google Scholar 

  • Casseday JH, Covey E (1995) Mechanisms for analysis of auditory temporal patterns in the brainstem of echolocating bats. In: Covey E, Hawkins HL, Port RF (eds) Neural representation of temporal patterns. Plenum Press, New York, pp 25–51

  • Griffin DR (1958) Listening in the dark. Yale University Press, New Haven, CT

  • Grinnell AD (1995) Hearing in bats: an overview. In: Popper AN, Fay RR (eds) Hearing by bats. Springer handbook of auditory research. Springer, Berlin Heidelberg New York, pp 1–36

  • Hartley DJ, Suthers RA (1989) The sound emission pattern of the echolocating bat, Eptesicus fuscus. J Acoust Soc Am 85:1348–1351

    Google Scholar 

  • Heiligenberg W (1991) Neural nets in electric fish. MIT Press, Cambridge, MA

  • Koppl C (1997) Phase locking to high frequencies in the auditory nerve and cochlear nucleus magnocellularis of the barn owl, Tyto alba. J Neurosci 17:3312–3321

    PubMed  Google Scholar 

  • Kurta A, Baker RH (1990) Eptesicus fuscus. Mammal Spec 356:1-10

    Google Scholar 

  • Masters WM, Raver KAS, Kornacker K, Burnett SC (1997) Detection of jitter in intertarget spacing by the big brown bat Eptesicus fuscus. J Comp Physiol A 181:279–290

    Article  CAS  PubMed  Google Scholar 

  • Menne D, Kaipf I, Wagner I, Ostwald J, Schnitzler H-U (1989) Range estimation by echolocation in the bat Eptesicus fuscus: trading of phase versus time cues. J Acoust Soc Am 85:2642–2650

    CAS  PubMed  Google Scholar 

  • Moiseff A, Konishi M (1981) Neuronal and behavioral sensitivity to binaural time differences in the owl. J Neurosci 1:40–48

    CAS  PubMed  Google Scholar 

  • Moss CF, Schnitzler H-U (1989) Accuracy of target ranging in echolocating bats: acoustic information processing. J Comp Physiol A 165:383–393

    Google Scholar 

  • Moss CF, Schnitzler H-U (1995) Behavioral studies of auditory information processing. In: Popper AN, Fay RR (eds) Hearing by bats. Springer handbook of auditory research. Springer, Berlin Heidelberg New York, pp 87–145

  • Moss CF, Simmons JA (1993) Acoustic image representation of a point target in the bat, Eptesicus fuscus: evidence for sensitivity to echo phase in bat sonar. J Acoust Soc Am 93:1553–1562

    CAS  PubMed  Google Scholar 

  • Neretti N, Intrator N, Sanderson MI, Simmons JA (2003) Time-frequency computational model for echo-delay resolution in sonar images of the big brown bat, Eptesicus fuscus. J Acoust Soc Am 113:2137–2145

    Article  PubMed  Google Scholar 

  • Neuweiler G (2000) The biology of bats. Oxford University Press, New York

  • Pollak GD (1993) Some comments on the proposed perception of phase and nanosecond time disparities by echolocating bats. J Comp Physiol A 172:523–531

    CAS  PubMed  Google Scholar 

  • Pollak GD, Marsh DS, Bodenhamer R, Souther A (1977) Characteristics of phasic-on neurons in the inferior colliculus of unanesthetized bats with observations related to mechanisms for echo ranging. J Neurophysiol 40:926–941

    CAS  PubMed  Google Scholar 

  • Sanderson MI, Neretti N, Intrator N, Simmons JA (2003) Evaluation of an auditory model for echo delay accuracy in wideband biosonar. J Acoust Soc Am (in press)

  • Schnitzler H-U, Menne D, Hackbarth H (1985) Range determination by measuring time delay in echolocating bats. In: Michelsen A (ed) Time resolution in auditory systems. Springer, Berlin Heidelberg New York, pp 180–204

  • Shamma S, Klein D (2000) The case of the missing pitch templates: how harmonic templates emerge in the early auditory system. J Acoust Soc Am 107:2631–2644

    Article  CAS  PubMed  Google Scholar 

  • Simmons JA (1979) Perception of echo phase information in bat sonar. Science 207:1336–1338

    Google Scholar 

  • Simmons JA (1980) The processing of sonar echoes by bats. In: Busnel R-G, Fish JF (eds) Animal sonar systems. Plenum Press, New York, pp 695–714

  • Simmons JA (1993) Evidence for perception of fine echo delay and phase by the FM bat, Eptesicus fuscus. J Comp Physiol A 172:533–547

    CAS  PubMed  Google Scholar 

  • Simmons JA, Grinnell AD (1988) The performance of echolocation: acoustic images perceived by echolocating bats. In: Nachtigall P, Moore PWB (eds) Animal sonar systems: processing and performance. Plenum Press, New York, pp 353–385

  • Simmons JA, Vernon JA (1971) Echolocation: discrimination of targets by the bat, Eptesicus fuscus. J Exp Zool 176:315–328

    CAS  PubMed  Google Scholar 

  • Simmons JA, Ferragamo M, Moss CF, Stevenson SB, Altes RA (1990a) Discrimination of jittered sonar echoes by the echolocating bat, Eptesicus fuscus: the shape of target images in echolocation. J Comp Physiol A 167:589–616

    CAS  PubMed  Google Scholar 

  • Simmons JA, Moss CF, Ferragamo M (1990b) Convergence of temporal and spectral information into acoustic images of complex sonar targets perceived by the echolocating bat, Eptesicus fuscus. J Comp Physiol A 166:449–470

    CAS  PubMed  Google Scholar 

  • Simmons JA, Ferragamo MJ, Saillant PA, Haresign T, Wotton JM, Dear SP, Lee DN (1995) Auditory dimensions of acoustic images in echolocation. In: Popper AN, Fay RR (eds) Hearing by bats. Springer handbook of auditory research. Springer, Berlin Heidelberg New York, pp 146–190

  • Simmons JA, Saillant PA, Ferragamo MJ, Haresign T, Dear SP, Fritz J, McMullen TA (1996) Auditory computations for biosonar target imaging in bats. In: Hawkins HL, McMullen TA, Popper AN, Fay RR (eds) Auditory computation. Springer handbook of auditory research. Springer, Berlin Heidelberg New York, pp 401–468

  • Simmons JA, Ferragamo MJ, Moss CF (1998) Echo-delay resolution in sonar images of the big brown bat, Eptesicus fuscus. Proc Natl Acad Sci USA 95:12647–12652

    Article  CAS  PubMed  Google Scholar 

  • Weiss TF, Rose C (1988) A comparison of synchronization filters in different auditory receptor organs. Hear Res 33:175–188

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by ONR Grant Nos. N00014-89-J-3055, N00014-95-L-1123, and N00014-99-l-0350, by NSF Grant Nos. BCS-9216718 and BES-9622297, by NIMH Grant No. MH00521 (RSDA) and NIMH Training Grant No. MH19118, by McDonnell-Pew Grant No. T89-01245-023, and by Deafness Research Foundation funds. A workshop was held at Sandbjerg, Denmark, in August 1994, to examine current problems in echolocation. Much of the discussion focused on issues surrounding observations of jitter hyperacuity by bats, and results from additional jitter experiments and control procedures were presented at that meeting. Pursuant to requests from several workshop participants, this paper gathers together findings relevant to whether echo delay or spectral differences can explain the bats' performance. We thank colleagues at the Sandbjerg workshop for their constructive suggestions about these experiments. Care and use of the animals was supervised by Brown University veterinarians and the Institutional Animal Care and Use Committee in accordance with Principles of Animal Care no. 86-23 (revised 1985) of the US National Institutes of Health Publication.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. A. Simmons.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Simmons, J.A., Ferragamo, M.J. & Sanderson, M.I. Echo delay versus spectral cues for temporal hyperacuity in the big brown bat, Eptesicus fuscus . J Comp Physiol A 189, 693–702 (2003). https://doi.org/10.1007/s00359-003-0444-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-003-0444-9

Keywords

Navigation