Skip to main content
Log in

Side peak suppression in responses of an across-frequency integration model to stimuli of varying bandwidth as demonstrated analytically and by implementation

  • Published:
Journal of Computational Neuroscience Aims and scope Submit manuscript

Abstract

Multiplication-like sound localization models are subjected to phase ambiguities for high-frequency tonal stimuli as multiplication creates several equivalent response peaks in tuning curves. By increasing the bandwidth of the stimulus, phase ambiguities can be reduced, which is often referred to as side peak suppression. In this study we present a Jeffress-based sound localization model, and determine side peak suppression analytically. The results were verified with an implementation of the same model, and compared to physiological data of barn owls. Three types of stimuli were analyzed: pure-tone stimuli, two-tone complexes with varying frequency distances, and noise signals with variable bandwidths. As an additional parameter we also determined the half-width of the main response peak to examine the scaling of tuning curves in azimuth. Results showed that side peak suppression did not only depend on bandwidth, but also on the center frequency and the distance of the side peak to the main response peak. In particular, the analytical model predicted that side peak suppression is a function of relative bandwidth, whereas half-width is inversely proportional to center frequency, with a proportionality factor depending on relative bandwidth. The analytical approach and the implementation yielded equivalent tuning curves (deviation < 1 %). Moreover, the electrophysiological data recorded in barn owls closely matched the predicted tuning curves.

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. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Agmon-Snir, H., Carr, C.E., Rinzel, J. (1998). The role of dendrites in auditory coincidence detection. Nature, 393, 268–272.

    Article  CAS  PubMed  Google Scholar 

  • Ashida, G., & Carr, C.E. (2011). Sound localization: Jeffress and beyond. Current Opinion in Neurobiology, 21, 745–751.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bernstein, L.R., & Trahiotis, C. (2011). Lateralization produced by envelope-based interaural temporal disparities of high-frequency, raised-sine stimuli: empirical data and modeling. Journal of the Acoustical Society of America, 129(3), 1501–1508.

    Article  PubMed  Google Scholar 

  • Bernstein, L.R., & Trahiotis, C. (2012). Lateralization produced by interaural temporal and intensitive disparities of high-frequency, raised-sine stimuli: data and modeling. Journal of the Acoustical Society of America, 131(1), 409–415.

    Article  PubMed  Google Scholar 

  • Cai, H., Carney, L.H., Colburn, H.S. (1998). A model for binaural response properties of inferior colliculus neurons. i. a model with interaural time difference-sensitive excitatory and inhibitory inputs. Journal of the Acoustical Society of America, 103(1), 475–493.

    Article  CAS  PubMed  Google Scholar 

  • Calmes, L., Lakemeyer, G., Wagner, H. (2007). Azimuthal sound localization using coincidence of timing across frequency on a robotic platform. Journal of the Acoustical Society of America, 121(4), 2034–2048.

    Article  PubMed  Google Scholar 

  • Carr, C.E., & Boudreau, R.E. (1993). Organization of the nucleus magnocellularis and the nucleus laminaris in the barn owl: encoding and measuring interaural time differences. The Journal of Comparative Neurology, 334(3), 337–355.

    Article  CAS  PubMed  Google Scholar 

  • Carr, C.E., & Konishi, M. (1988). Axonal delay lines for time measurement in the owl’s brainstem. Proceedings of the National Academy of Sciences of the United States of America, 85, 8311–8315.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Carr, C.E., & Konishi, M. (1990). A circuit for detection of interaural time differences in the brain stem of the barn owl. Journal of Neuroscience, 10(10), 3227–3246.

    CAS  PubMed  Google Scholar 

  • Christianson, G.B., & Pena, J.L. (2006). Noise reduction of coincidence detector output by the inferior colliculus of the barn owl. The Journal of Neuroscience, 26(22), 5948–5954.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Colburn, H.S., Durlach, N., Carterette, E., Friedman, M. (1978). Models of binaural interaction. Handbook of Perception, 4, 467–518.

    Google Scholar 

  • Colburn, H.S., Han, Y., Culotta, C.P. (1990). Coincidence model of mso responses. Hearing Research, 49(1–3), 335–346.

    Article  CAS  PubMed  Google Scholar 

  • Faller, C., & Merimaa, J. (2004). Source localization in complex listening situations: selection of binaural cues based on interaural coherence. Journal of the Acoustical Society of America, 116(5), 3075–3089.

    Article  PubMed  Google Scholar 

  • Fischer, B.J., Anderson, C.H., Pena, J.L. (2009). Multiplicative auditory spatial receptive fields created by a hierarchy of population codes. PLoS One, 4(11), 1–15.

    Article  Google Scholar 

  • Grau-Serrat, V., Carr, C.E., Simon, J.Z. (2003). Modeling coincidence detection in nucleus laminaris. Biological Cybernetics, 89, 388–396.

    Article  PubMed Central  PubMed  Google Scholar 

  • Han, Y.A., & Colburn, H.S. (1993). Point-neuron model for binaural interaction in MSO. Hearing Research, 68(1), 115–130.

    Article  CAS  PubMed  Google Scholar 

  • Hancock, K.E., & Delgutte, B. (2004). A physiologically based model of interaural time difference discrimination. The Journal of Neuroscience, 24(32), 7110–7117.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hausmann, L., von Campenhausen, M., Endler, F., Singheiser, M., Wagner, H. (2009). Improvements of sound localization abilities by the facial ruff of the barn owl (tyto alba) as demonstrated by virtual ruff removal. PLoS One, 4(11), 11.

    Article  Google Scholar 

  • Hausmann, L., von Campenhausen, M., Wagner, H. (2010). Properties of low-frequency head-related transfer functions in the barn owl (tyto alba). Journal of Comparative Physiology: A Neuroethology, Sensory, Neural, and Behavioral Physiology, 196(9), 601–612.

    Article  Google Scholar 

  • Hummersone, C., Mason, R., Brookes, T. (2010). Dynamic precedence effect modeling for source separation in reverberant environments. IEEE Transactions on Acoustics, Speech and Signal Processing, 18(7), 1867–1871.

    Google Scholar 

  • Jeffress, L.A. (1948). A place theory of sound localization. Journal of Comparative and Physiological Psychology, 41, 35–39.

    Article  CAS  PubMed  Google Scholar 

  • Jercog, P.E., Svirskis, G., Kotak, V.C., Sanes, D.H., Rinzel, J. (2010). Asymmetric excitatory synaptic dynamics underlie interaural time difference processing in the auditory system. PLoS Biology, 8(6), e1000406.

    Article  PubMed Central  PubMed  Google Scholar 

  • Joris, P.X., & Yin, T.C.T. (2006). A matter of time: internal delays in binaural processing. Trends in Neurosciences, 30(2), 70–78.

    Article  PubMed  Google Scholar 

  • Joris, P.X., Smith, P.H., Yin, T.C.T. (1998). Coincidence detection in the auditory system: 50 years after Jeffress. Neuron, 21, 1235–1238.

    Article  CAS  PubMed  Google Scholar 

  • Köppl, C. (1997). Phase locking to high frequencies in the auditory nerve and cochlear nucleus magnocellularis of the barn owl, tyto alba. The Journal of Neuroscience, 17(9), 3312–3321.

    PubMed  Google Scholar 

  • Leibold, C. (2010). Influence of inhibitory synaptic kinetics on the interaural time difference sensitivity in a linear model of binaural coincidence detection. Journal of the Acoustical Society of America, 127(2), 931–942.

    Article  PubMed  Google Scholar 

  • Liu, C., Wheeler, B.C., O’Brien, W.D.J., Bilger, R.C., Lansing, C.R., Feng, A.S. (2000). Localization of multiple sound sources with two microphones. Journal of the Acoustical Society of America, 108(4), 1888–1905.

    Article  CAS  PubMed  Google Scholar 

  • Lüling, H., Siveke, I., Grothe, B., Leibold, C. (2011). Frequency-invariant representation of interaural time differences in mammals. PLoS Computational Biology, 7(3), e1002013.

    Article  PubMed Central  PubMed  Google Scholar 

  • Mazer, J.A. (1998). How the owl resolves auditory coding ambiguity. Proceedings of the National Academy of Sciences of the United States of America, 95, 10932–10937.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Peña, J.L., & Konishi, M. (2000). Cellular mechanisms for resolving phase ambiguity in the owl’s inferior colliculus. Proceedings of the National Academy of Sciences, 97(22), 11787–11792.

    Article  Google Scholar 

  • Peña, J.L., & Konishi, M. (2001). Auditory spatial receptive fields created by multiplication. Science, 292, 249–252.

    Article  PubMed  Google Scholar 

  • Saberi, K., Farahbod, H., Konishi, M. (1998). How do owls localize interaurally phase-ambiguous signals? Proceedings of the National Academy of Sciences, 95(11), 6465–6468.

    Article  CAS  Google Scholar 

  • Saberi, K., Takahashi, Y., Farahbod, H., Konishi, M. (1999). Neural bases of an auditory illusion and its elimination in owls. Nature Neuroscience, 2(7), 656–659.

    Article  CAS  PubMed  Google Scholar 

  • Singheiser, M., Plachta, D.T., Brill, S., Bremen, P., van der Willigen, R.F., Wagner, H. (2010). Target-approaching behavior of barn owls (tyto alba): influence of sound frequency. Journal of Comparative Physiology, A Neuroethology, Sensory, Neural, and Behavioral Physiology, 196(3), 227–240.

    Article  Google Scholar 

  • Singheiser, M., Gutfreund, Y., Wagner, H. (2012). The representation of sound localization cues in the barn owl’s inferior colliculus. Front Neural Circuits, 6, 1–15.

    Article  Google Scholar 

  • Sullivan, W., & Konishi, M. (1986). Neural map of interaural phase difference in the owl’s brainstem. Proceedings of the National Academy of Sciences of the United States of America, 83(21), 8400–8404.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Supper, B., Brookes, T., Rumsey, F. (2006). An auditory onset detection algorithm for improved automatic source localization. IEEE Transactions On Audio, Speech and Language Processing, 14(3), 1008–1016.

    Article  Google Scholar 

  • Takahashi, T., & Konishi, M. (1986). Selectivity for interaural time difference in the owl’s midbrain. The Journal of Neuroscience, 6(12), 3413–3455.

    CAS  PubMed  Google Scholar 

  • Thompson, S.K., von Kriegstein, K., Deane-Pratt, A., Marquardt, T., Deichmann, R., Griffiths, T.D., McAlpine D. (2006). Representation of interaural time delay in the human auditory midbrain. Nature Neuroscience, 9(9), 1096–1098.

    Article  CAS  PubMed  Google Scholar 

  • Trahiotis, C., Bernstein, L.R., Akeroyd, M.A. (2001). Manipulating the ”straightness” and ”curvature” of patterns of interaural cross correlation affects listeners’ sensitivity to changes in interaural delay. Journal of the Acoustical Society of America, 109(1), 321–330.

    Article  CAS  PubMed  Google Scholar 

  • Vieira, J., & Almeida, L. (2003). A sound localizer robust to reverberation. Audio Engineering Society Convention, 115, 5973.

    Google Scholar 

  • von Campenhausen, M., & Wagner, H. (2006). Influence of the facial ruff on the sound-receiving characteristics of the barn owl’s ears. Journal of Comparative Physiology, 192(10), 1073–1082.

    Article  Google Scholar 

  • Wagner, H., Takahashi, T.T., Konishi, M. (1987). Representation of interaural time difference in the central nucleus of the barn owl’s inferior colliculus. Journal of Neuroscience, 7(10), 3105–3116.

    CAS  PubMed  Google Scholar 

  • Wagner, H., Asadollahi, A., Bremen, P., Endler, F., Vonderschen, K., von Campenhausen, M. (2007). Distribution of interaural time difference in the barn owl’s inferior colliculus in the low - and high-frequency ranges. The Journal of Neuroscience, 27(15), 4191–4200.

    Article  CAS  PubMed  Google Scholar 

  • Willert, V., Eggert, J., Adamy, J., Stahl, R., Körner, E. (2006). A probabilistic model for binaural sound localization. IEEE Transactions on Systems, Man and Cybernetics - Part B: Cybernetics, 36(5), 982–994.

    Article  Google Scholar 

  • Zhou, Y., Carney, L.H., Colburn, H.S. (2005). A model for interaural time difference sensitivity in the medial superior olive: interaction of excitatory and inhibitory synaptic inputs, channel dynamics, and cellular morphology. The Journal of Neuroscience, 12, 3046–3058.

    Article  Google Scholar 

Download references

Acknowledgment

The present project is supported by the National Research Fund, Luxembourg.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tom Goeckel.

Additional information

Action Editor: Catherine E. Carr

Rights and permissions

Reprints and permissions

About this article

Cite this article

Goeckel, T., Führ, H., Lakemeyer, G. et al. Side peak suppression in responses of an across-frequency integration model to stimuli of varying bandwidth as demonstrated analytically and by implementation. J Comput Neurosci 36, 1–17 (2014). https://doi.org/10.1007/s10827-013-0460-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10827-013-0460-x

Keywords

Navigation