Skip to main content

Advertisement

Springer Nature Link
Log in

On population encoding and decoding of auditory information for bat echolocation

  • Original Paper
  • Published:
Biological Cybernetics Aims and scope Submit manuscript

Abstract

In this article, we study the neural encoding of acoustic information for FM-bats (such as Eptesicus fuscus) in simulation. In echolocation research, the frequency–time sound representation as expressed by the spectrogram is often considered as input. The rationale behind this is that a similar representation is present in the cochlea, i.e. the receptor potential of the inner hair cells (IHC) along the length of the cochlea, and hence similar acoustic information is relayed to the brain. In this article, we study to what extent the latter assumption is true. The receptor potential is converted into neural activity of the synapting auditory nerve cells (ANC), and information might be lost in this conversion process. Especially for FM-bats, this information transmission is not trivial: in contrast to other mammals, they detect short transient signals, and consequently neural activity can only be integrated over very limited time intervals. To quantify the amount of information transmitted we design a neural network-based algorithm to reconstruct the IHC receptor potentials from the spiking activity of the synapting auditory neurons. Both the receptor potential and the resulting neural activity are simulated using Meddis’ peripheral model. Comparing the reconstruction to the IHC receptor potential, we quantify the information transmission of the bat hearing system and investigate how this depends on the intensity of the incoming signal, the distribution of auditory neurons, and previous masking stimulation (adaptation). In addition, we show how this approach allows to inspect which spectral features survive neural encoding and hence can be relevant for echolocation.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Altes R (1980) Detection, estimation, and classification with spectrograms. J Acoust Soc Am 67(4): 1232–1246

    Article  Google Scholar 

  • Avissar M, Furman AC, Saunders JC, Parsons TD (2007) Adaptation reduces spike-count reliability, but not spike-timing precision, of auditory nerve responses. J Neurosci 27(24): 6461–6472

    Article  CAS  PubMed  Google Scholar 

  • Aytekin M, Grassi E, Sahota M, Moss CF (2004) The bat head-related transfer function reveals binaural cues for sound localization in azimuth and elevation. J Acoust Soc Am 116(6): 3594–3605

    Article  PubMed  Google Scholar 

  • Bialek W, Rieke F, de Ruyter van Steveninck RR, Warland D (1991) Reading a neural code. Science 252: 1854–1857

    Article  CAS  PubMed  Google Scholar 

  • Borst A, Theunissen FE (1999) Information theory and neural coding. Nature Neurosci 2(11): 947–957

    Article  CAS  PubMed  Google Scholar 

  • Burda H, Úlehelová L (1983) Cochlear hair-cell populations and limits of resolution of hearing in two vespertilionid bats, Nyctalus noctula and Eptesicus serotinus. J Morphol 176: 221–224

    Article  CAS  PubMed  Google Scholar 

  • Chase SM, Young ED (2006) Spike-timing codes enhance the representation of multiple simultaneous sound-localization cues in the inferior colliculus. J Neurosci 26(15): 3889–3898

    Article  CAS  PubMed  Google Scholar 

  • Chase SM, Young ED (2008) Cues for sound localization are encoded in multiple aspects of spike trains in the inferior colliculus. J Neurophysiol 99: 1672–1682

    Article  PubMed  Google Scholar 

  • Clague H, Theunissen F, Miller JP (1997) Effects of adaptation on neural coding by primary sensory interneurons in the cricket cercal system. J Neurophysiol 77: 07–220

    Google Scholar 

  • Dalland JI (1965) Hearing sensitivity in bats. Science 150: 1185–1186

    Article  CAS  PubMed  Google Scholar 

  • Eger M, Eckhorn R (2002) A model-based approach for the analysis of neuronal information transmission in multi-input and -output systems. J Comput Neurosci 12: 175–200

    Article  CAS  PubMed  Google Scholar 

  • Firzlaff U, Schuchmann M, Grunwald JE, Schuller G, Wiegrebe L (2007) Object-oriented echo perception and cortical representation in echolocation bats. PLoS Biol 5(5): 1174–1183

    Article  CAS  Google Scholar 

  • Fontaine B, Peremans H (2007) Tuning bat LSO neurons to interaural intensity differences through spike-timing dependent plasticity. Biol Cybern 97: 261–267

    Article  PubMed  Google Scholar 

  • Gaumond RP, Kim DO, Molnar CE (1983) Response of cochlear nerve fibers to brief acoustic stimuli: role of discharge-history effects. J Acoust Soc Am 74(5): 1392–1398

    Article  CAS  PubMed  Google Scholar 

  • Genzel D, Wiegrebe L (2008) Time-variant spectral peak and notch detection in echolocation-call sequences in bats. J Exp Biol 211: 9–14

    Article  PubMed  Google Scholar 

  • Givois V, Pollack GS (2000) Sensory habituation of auditory receptor neurons: implications for sound localization. J Exp Biol 203: 2529–2537

    CAS  PubMed  Google Scholar 

  • Griffin DR (1974) Listening in the dark: acoustic orientation of bats and men. Dover Publications, New York

    Google Scholar 

  • Haplea S, Covey E, Casseday JH (1994) Frequency tuning and response latencies at three levels in the brainstem of the echolocating bat, Eptesicus fuscus. J Comp Physiol A 174: 671–683

    Article  CAS  PubMed  Google Scholar 

  • Hiryu S, Hagino T, Riquimaroux H, Watanabe Y (2007) Echo-intensity compensation in echolocating bats (Pipistrellus abramus) during flight measured by a telemetry microphone. J Acoust Soc Am 121(3): 1749–1757

    Article  PubMed  Google Scholar 

  • Koay G, Heffner HE, Heffner RS (1996) Audiogram of the big brown bat (Eptesicus fuscus). Hear Res 105: 202–210

    Article  Google Scholar 

  • Lopez-Poveda EA (2005) Spectral processing by the peripheral auditory system, facts and models. Int Rev Neurobiol 70: 7–48

    Article  PubMed  Google Scholar 

  • Manley GA, Irvine DRF, Johnstone BM (1972) Frequency response of bat tympanic membrane. Nature 237: 112–113

    Article  Google Scholar 

  • Matsuo I, Yano M (2004) An echolocation model for the restoration of an acoustic image from a single-emission echo. J Acoust Soc Am 116(6): 3782–3788

    Article  PubMed  Google Scholar 

  • Meddis R (2006) Auditory-nerve first-spike latency and auditory absolute threshold: a computer model. J Acoust Soc Am 119(1): 406–417

    Article  PubMed  Google Scholar 

  • Mogdans J, Schnitzler H-U (1990) Range resolution and the possible use of spectral information in the echolocating bat, Eptesicus fuscus. J Acoust Soc Am 88(2): 754–757

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Müller R (2003) A computational theory for the classification of natural biosonar targets based on a spike code. Netw Comput Neural Syst 14: 595–612

    Article  Google Scholar 

  • Nerettia N, Sanderson MI, Intrator N, Simmons JA (2003) Time–frequency model for echo-delay resolution in wideband biosonar. J Acoust Soc Am 113(4): 2137–2145

    Article  Google Scholar 

  • Obrist MK, Brock Fenton M, Eger JL, Schlegel PA (1993) What ears do for bats: a comparative study of pinna sound pressure transformation in chiroptera. J Exp Biol 180: 119–152

    CAS  PubMed  Google Scholar 

  • Palakal MJ, Wong D (1999) Cortical representation of spatiotemporal pattern of firing evoked by echolocation signals: population encoding of target features in real time. J Acoust Soc Am 106(1): 479–490

    Article  CAS  PubMed  Google Scholar 

  • Patterson RD (2000) Auditory images: how complex sounds are represented in the auditory system. J Acoust Soc Jpn E 21: 183–190

    Article  Google Scholar 

  • Ramprashad F, Money KE, Landolt JP, Laufer J (1978) A neuroanatomical study of the cochlea of the little brown bat (Myotis lucifugus). J Comp Neurol 178: 347–364

    Article  CAS  PubMed  Google Scholar 

  • Reijniers J, Peremans H (2007) Biomimetic sonar system performing spectrum-based localization. IEEE Trans Robot 23(6): 1151–1159

    Article  Google Scholar 

  • Rieke, F, Warland, D, de Ruyter van Steveninck, RR, Bialek, W (eds) (1997) Spikes: exploring the neural code. MIT Press, Cambridge

    Google Scholar 

  • Rodriguez A, Mora EC (2006) The echolocation repertoire of Eptesicus fuscus (Chiroptera: Vespertilionidae) in Cuba. Caribb J Sci 42: 121–128

    Google Scholar 

  • Saillant PA, Simmons JA, Dear SP, McMullen TA (1993) A computational model of echo processing and acoustic imaging in FM echolocating bats: the SCAT receiver. J Acoust Soc Am 94(5): 2691–2712

    Article  CAS  PubMed  Google Scholar 

  • Saillant PA, Simmons JA, Bouffard FH, Lee DN, Dear SP (2007) Biosonar signals impinging on the target during interception by big brown bats, Eptesicus fuscus. J Acoust Soc Am 121(5): 3001–3010

    Article  PubMed  Google Scholar 

  • Sanderson MI, Simmons JA (2000) Neural responses to overlapping FM sounds in the inferior colliculus of echolocating bats. J Neurophysiol 83: 1840–1855

    CAS  PubMed  Google Scholar 

  • Simmons JA, Saillant PA, Wotton JM, Haresign T, Ferragamo MJ, Moss CF (1995) Composition of biosonar images for target recognition by echolocating bats. Neural Netw 8: 1239–1261

    Article  Google Scholar 

  • Simmons JA, Wotton JM, Ferragamo MJ, Moss CF (2002) Transformation of external-ear spectral cues into perceived delays by the big brown bat, Eptesicus fuscus. J Acoust Soc Am 111(6): 2771–2782

    Article  PubMed  Google Scholar 

  • Sumner CJ, Lopez-Poveda EA, O’Mard LP, Meddis R (2002) A revised model of the inner-hair cell and auditory-nerve complex. J Acoust Soc Am 111(5): 2178–2188

    Article  PubMed  Google Scholar 

  • Victor JD (2006) Approaches to information-theoretic analysis of neural activity. Biol Theory 1(3): 302–316

    Article  PubMed  Google Scholar 

  • Warland DK, Reinagel P, Meister M (1997) Decoding visual information from a population of retinal ganglion cells. J Neurophysiol 78(5): 2336–2350

    CAS  PubMed  Google Scholar 

  • Wiegrebe L (2008) An autocorrelation model of bat sonar. Biol Cybern 98: 587–595

    Article  PubMed  Google Scholar 

  • Yovel Y, Franz MO, Stiltz P, Schnitzler HU (2008) Plant classification from bat-like echolocation signals. PLoS Comput Biol 4(3): e1000032

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Active Perception Laboratory, University of Antwerp, 2000, Antwerp, Belgium

    Jonas Reijniers & H. Peremans

Authors
  1. Jonas Reijniers
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. H. Peremans
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to Jonas Reijniers.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Reijniers, J., Peremans, H. On population encoding and decoding of auditory information for bat echolocation. Biol Cybern 102, 311–326 (2010). https://doi.org/10.1007/s00422-010-0368-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00422-010-0368-8

Keywords