Skip to main content
SpringerLink
Log in

Neural coding of echo-envelope disparities in echolocating bats

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

Abstract

The effective use of echolocation requires not only measuring the delay between the emitted call and returning echo to estimate the distance of an ensonified object. To locate an object in azimuth and elevation, the bat’s auditory system must analyze the returning echoes in terms of their binaural properties, i.e., the echoes’ interaural intensity and time differences (IIDs and ITDs). The effectiveness of IIDs for echolocation is undisputed, but when bats ensonify complex objects, the temporal structure of echoes may facilitate the analysis of the echo envelope in terms of envelope ITDs. Using extracellular recordings from the auditory midbrain of the bat, Phyllostomus discolor, we found a population of neurons that are sensitive to envelope ITDs of echoes of their sonar calls. Moreover, the envelope-ITD sensitivity improved with increasing temporal fluctuations in the echo envelopes, a sonar parameter related to the spatial statistics of complex natural reflectors like vegetation. The data show that in bats envelope ITDs may be used not only to locate external, prey-generated rustling sounds but also in the context of echolocation. Specifically, the temporal fluctuations in the echo envelope, which are created when the sonar emission is reflected from a complex natural target, support ITD-mediated echolocation.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

AC:

Auditory cortex

BF:

Best frequency

IC:

Inferior colliculus

IR:

Impulse response

ITD:

Interaural time difference

IID:

Interaural intensity difference

M4:

Fourth moment

PLC:

Preferring leading contralateral

PLI:

Preferring leading ipsilateral

PSTH:

Peri-stimulus time histogram

References

  • Bernstein L, Trahiotis C (2002) Enhancing sensitivity to interaural delays at high frequencies by using “transposed stimuli”. J Acoust Soc Am 112:1026–1036

    Article  PubMed  Google Scholar 

  • Bernstein LR, Trahiotis C (2007) Why do transposed stimuli enhance binaural processing? Interaural envelope correlation vs envelope normalized fourth moment. J Acoust Soc Am 121:EL23–EL28

    Article  PubMed  Google Scholar 

  • Borina F, Firzlaff U, Schuller G, Wiegrebe L (2008) Representation of echo roughness and its relationship to amplitude-modulation processing in the bat auditory midbrain. Eur J Neurosci 27:2724–2732

    Article  PubMed  Google Scholar 

  • Brand A, Behrend O, Marquardt T, McAlpine D, Grothe B (2002) Precise inhibition is essential for microsecond interaural time difference coding. Nature 417:543–547

    Article  PubMed  CAS  Google Scholar 

  • Covey E (2005) Neurobiological specializations in echolocating bats. Anat Rec A Discov Mol Cell Evol Biol 287:1103–1116

    PubMed  Google Scholar 

  • Covey E, Vater M, Casseday J (1991) Binaural properties of single units in the superior olivary complex of the mustached bat. J Neurophysiol 66:1080–1094

    PubMed  CAS  Google Scholar 

  • Firzlaff U, Schoernich S, Hoffmann S, Schuller G, Wiegrebe L (2006) A neural correlate of stochastic echo imaging. J Neurosci 26:785–791

    Article  PubMed  CAS  Google Scholar 

  • Fuzessery Z (1997) Acute sensitivity to interaural time differences in the inferior colliculus of a bat that relies on passive sound localization. Hear Res 109:46–62

    Article  PubMed  CAS  Google Scholar 

  • Fuzessery ZM, Buttenhoff P, Andrews B, Kennedy JM (1993) Passive sound localization of prey by the pallid bat (Antrozous p. pallidus). J Comp Physiol A 171:767–777

    Article  PubMed  CAS  Google Scholar 

  • Griffin SJ, Bernstein LR, Ingham NJ, McAlpine D (2005) Neural sensitivity to interaural envelope delays in the inferior colliculus of the guinea pig. J Neurophysiol 93:3463–3478

    Article  PubMed  Google Scholar 

  • Grothe B (2000) The evolution of temporal processing in the medial superior olive, an auditory brainstem structure. Prog Neurobiol 61:581–610

    Article  PubMed  CAS  Google Scholar 

  • Grothe B, Park TJ (1995) Time can be traded for intensity in the lower auditory system. Naturwissenschaften 82:521–523

    Article  PubMed  CAS  Google Scholar 

  • Grunwald J, Schoernich S, Wiegrebe L (2004) Classification of natural textures in echolocation. Proc Natl Acad Sci USA 101:5670–5674

    Article  PubMed  CAS  Google Scholar 

  • Hartmann W, Pumplin J (1988) Noise power fluctuations and the masking of sine signals. J Acoust Soc Am 83:2277–2289

    Article  PubMed  CAS  Google Scholar 

  • Henning GB (1974) Detectability of interaural delay in high-frequency complex waveforms. J Acoust Soc Am 55:84–90

    Article  PubMed  CAS  Google Scholar 

  • Holderied MW, von Helversen O (2006) ‘Binaural echo disparity’ as a potential indicator of object orientation and cue for object recognition in echolocating nectar-feeding bats. J Exp Biol 209:3457–3468

    Article  PubMed  Google Scholar 

  • Irvine DR, Park VN, Mattingley JB (1995) Responses of neurons in the superior collilulus of the rat to interaural time- and intensity differences in transient stimuli: implications for the latency hypothesis. Hear Res 85:127–141

    Article  PubMed  CAS  Google Scholar 

  • Irving R, Harrison JM (1967) The superior olivary complex and audition: a comparative study. J Comp Neurol 130:77–86

    Article  PubMed  CAS  Google Scholar 

  • Jeffress LA (1948) A place theory of sound localisation. J Comp Physiol Psychol 41:35–39

    Article  PubMed  CAS  Google Scholar 

  • Joris PX, Yin TC (1995) Envelope coding in the lateral superior olive. I. Sensitivity to interaural time differences. J Neurophysiol 73:1043–1062

    PubMed  CAS  Google Scholar 

  • Le Beau FE, Rees A, Malmierca MS (1996) Contribution of GABA- and glycine-mediated inhibition to the monaural temporal response properties of neurons in the inferior colliculus. J Neurophysiol 75:902–919

    PubMed  CAS  Google Scholar 

  • Lohuis T, Fuzessery Z (2000) Neuronal sensitivity to interaural time differences in the sound envelope in the auditory cortex of the pallid bat. Hear Res 143:43–57

    Article  PubMed  CAS  Google Scholar 

  • Masterton B (1974) Adaptation for sound localization in the ear and brainstem of mammals. Fed Proc 33:1904–1910

    PubMed  CAS  Google Scholar 

  • Mueller R, Kuc R (2000) Foliage echoes: a probe into the ecological acoustics of bat echolocation. J Acoust Soc Am 108:836–845

    Article  Google Scholar 

  • Park TJ, Pollak GD (1993) GABA shapes sensitivity to interaural intensity disparities in the mustache bat’s inferior colliculus: implications for encoding sound location. J Neurosci 13:2050–2067

    PubMed  CAS  Google Scholar 

  • Pollak G (1988) Time is traded for intensity in the bat’s auditory system. Hear Res 36:107–124

    Article  PubMed  CAS  Google Scholar 

  • Rayleigh L (1907) On our perception of sound direction. Philos Mag 13:214–232

    Google Scholar 

  • Schuller G (1997) A cheap earphone for small animals with good frequency response in the ultrasonic frequency range. J Neurosci Methods 71:187–190

    Article  PubMed  CAS  Google Scholar 

  • Schuller G, Radtke-Schuller S, Betz M (1986) A stereotaxic method for small animals using experimentally determined reference profiles. J Neurosci Methods 18:339–350

    Article  PubMed  CAS  Google Scholar 

  • Schuller G, O’Neill W, Radtke-Schuller S (1991) Facilitation and delay sensitivity of auditory cortex neurons in CF -FM bats, Rhinolophus rouxi and Pteronotus p. parnellii. Eur J Neurosci 3:1165–1181

    Article  PubMed  Google Scholar 

  • Thompson S (1882) On the function of the two ears in the perception of space. Philos Mag 13:406–416

    Google Scholar 

  • van de Par S, Kohlrausch A (1997) A new approach to comparing binaural masking level differences at low and high frequencies. J Acoust Soc Am 101:1671–1680

    Article  PubMed  Google Scholar 

  • Wenstrup JJ, Ross LS, Pollak GD (1986) Binaural response organization within a frequency-band representation of the inferior colliculus. Implication for sound localization. J Neurosci 6:962–973

    PubMed  CAS  Google Scholar 

  • Yin TC, Hirsch TA, Chan JC (1985) Responses of neurons in the cat’s superior colliculus to acoustic stimuli. II. A model of interaural intensity sensitivity. J Neurophysiol 53:746–758

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Gerd Schuller and Benedikt Grothe for lively discussions on the topic. This work was supported by the ‘Volkswagenstiftung’ I79 780 to L.W. All experiments were conducted under the principles of laboratory animal care and the regulations of the current version of the German Law on Animal Protection (approval 209.1/211-2531-68/03, Reg. Oberbayern).

Author information

Author notes

  1. Uwe Firzlaff

    Present address: Lehrstuhl f. Zoologie, Technische Universität München, Liesel-Beckmann-Str. 4, 85350, Freising-Weihenstephan, Germany

Authors and Affiliations

  1. Division of Neurobiology, Department Biologie II, Ludwig-Maximilians-Universität München, Großhadernerstr. 2, 82152, Planegg-Martinsried, Germany

    Frank Borina, Uwe Firzlaff & Lutz Wiegrebe

Authors
  1. Frank Borina
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Uwe Firzlaff
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lutz Wiegrebe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Uwe Firzlaff.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Borina, F., Firzlaff, U. & Wiegrebe, L. Neural coding of echo-envelope disparities in echolocating bats. J Comp Physiol A 197, 561–569 (2011). https://doi.org/10.1007/s00359-010-0571-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-010-0571-z

Keywords

Search

Navigation