Skip to main content
Log in

Neuronal identification of signal periodicity by balanced inhibition

  • Letter to the Editor
  • Published:
Biological Cybernetics Aims and scope Submit manuscript

Abstract

Many animals, including men, use periodicity information, e.g., amplitude modulations of acoustic stimuli, as a vital cue to auditory object formation. The underlying neuronal mechanisms, however, still remain a matter of debate. Here, we mathematically analyze a model for periodicity identification that relies on the interplay of excitation and delayed inhibition. Our analytical results show how the maximal response of such a system varies systematically with the time constants of excitation and inhibition. The model reliably identifies signal periodicity in the range from about ten to several hundred Hertz. Importantly, the model relies on biologically plausible parameters only. It works best for excitatory and inhibitory neuronal couplings of equal strength, the so-called ‘balanced inhibition’ We show how balanced inhibition can serve to identify low-frequency signal periodicity and how variation of a single parameter, the inhibitory time constant, can tune the system to different frequencies.

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.

References

  • Anderson JS, Carandini M, Ferster D (2000) Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex. J Neurophysiol 84: 909–926

    CAS  PubMed  Google Scholar 

  • Barth F (1998) The vibrational sense of spiders. In: Hoy RR, Popper AN, Fay RR (eds) Comparative hearing: insects, chap. 7. Springer, New York, pp 228–278

    Google Scholar 

  • Bendor D, Wang X (2005) The neuronal representation of pitch in primate auditory cortex. Nature 436: 1161–1165

    Article  CAS  PubMed  Google Scholar 

  • Bleckmann H, Barth F (1984) Sensory ecology of a semi-equatic spider Dolomedes triton II. The release of predatory behavior by water surface waves. Behav Ecol Sociobiol 14: 303–312

    Article  Google Scholar 

  • Bregman A (1990) Auditory scene analysis. MIT Press, Cambridge

    Google Scholar 

  • Cherry EC (1953) Some experiments on the recognition of speech, with one and with two ears. J Acoust Soc Am 25(5): 975–979

    Article  Google Scholar 

  • Coombs S, Görner P, Münz H (eds) (1989) Themechanosensory lateral line: neurobiology and evolution. Springer, New York

    Google Scholar 

  • Elepfandt A (1984) Localization of water surface waves with the lateral line system in the clawed toad (Xenopus laevis daudin). In: Varjú D, Schnitzler H (eds) Localizatoin and orientation in biology and engineering. Springer, New York, pp 63–65

    Google Scholar 

  • Friedel P, Bürck M, van Hemmen JL (2007) Neuronal identification of acoustic signal periodicity. Biol Cybern 97: 247–260

    Article  PubMed  Google Scholar 

  • Gerstner W, Kistler W (2002) Spiking neuron models. Cambridge University Press, Cambridge

    Google Scholar 

  • Grothe B (1994) Interaction of excitation and inhibition in processing of pure tone and amplitude-modulated stimuli in the medial superior olive of the mustached bat. J Neurophysiol 71: 706–721

    CAS  PubMed  Google Scholar 

  • Highley MJ, Contreras D (2006) Balanced excitation and inhibition determine spike timing during frequency adaptation. J Neurosci 26(2): 448–457

    Article  Google Scholar 

  • Izhikevich EM (2001) Resonate-and-fire neurons. Neural Netw 14: 883–894

    Article  CAS  PubMed  Google Scholar 

  • Joris PX, Schreiner CE, Rees A (2004) Neural processing of amplitude-modulated sounds. Physiol Rev 84: 541–577

    Article  CAS  PubMed  Google Scholar 

  • Kalmijn A (1988) Hydrodynamic and acoustic field detection. In: Atema J, Fay R, Popper A, Tavolga W (eds) Sensory biology of aquatic animals, chap. 4. Springer, New York, pp 83–130

    Google Scholar 

  • Käse R., Bleckmann H (1987) Prey localization by surface wave ray-tracing: fish track bugs like oceanographers track storms. Experientia 43: 290–293

    Article  PubMed  Google Scholar 

  • Krishna B, Semple M (2000) Auditory temporal processing: response to sinusoidally amplitude-moulated tones in the inferior colliculus. J Neurophysiol 84: 255–273

    CAS  PubMed  Google Scholar 

  • Langner G (1992) Periodicity coding in the auditory system. Hear Res 60: 115–142

    Article  CAS  PubMed  Google Scholar 

  • Langner G, Schreiner C (1988) Periodicity coding in the inferior colliculus of the cat. I. Neuronal mechanisms. J Neurophysiol 60: 1799–1822

    CAS  PubMed  Google Scholar 

  • Large EW, Crawford JD (2002) Auditory temporal computation: interval selectivity based on post-inhibitory rebound. J Comput Neurosci 13: 125–142

    Article  PubMed  Google Scholar 

  • Las L, Stern EA, Nelken I (2005) Representation of tone in fluctuating maskers in the ascending auditory system. J Neurosci 25(6): 1503–1513

    Article  CAS  PubMed  Google Scholar 

  • Licklider J (1951) A duplex theory of pitch perception. Experientia 7: 128–134

    Article  CAS  PubMed  Google Scholar 

  • Meddis R, O’Mard L (2006) Virtual pitch in a computational physiological model. J Acoust Soc. Am. 120(6): 3861–3869

    Article  PubMed  Google Scholar 

  • Monier C, Chavane F, Baudot P, Graham LJ, Frégnac Y (2003) Orientation and direction selectivity of synaptic inputs in visual cortical neurons: a diversity of combinations produces spike tuning. Neuron 37: 663–680

    Article  CAS  PubMed  Google Scholar 

  • Nelken I, Rotman Y, Bar Yosef O (1999) Responses of auditory-cortex neurons to structural features of natural sounds. Nature 397: 154–157

    Article  CAS  PubMed  Google Scholar 

  • Nelson PC, Carney LH (2004) A phenomenological model of peripheral and central neural responses to amplitude-modulated tones. J Acoust Soc Am 116(4): 2173–2186

    Article  PubMed  Google Scholar 

  • Okun M, Lampl I (2008) Instantaneous correlation of excitation and inhibition during ongoing and sensory-evoked activities. Nat Neurosci 11(5): 535–537

    Article  CAS  PubMed  Google Scholar 

  • Paolini AG, Clarey JC, Needham K, Clark GM (2005) Balanced inhibition and excitation underlies spike firing regularity in ventral cochlear nucleus chopper neurons. Eur J Neurosci 21: 1236–1248

    Article  PubMed  Google Scholar 

  • Rees A, Møller A (1983) Responses of neurons in the inferior colliculus of the rat to AM and FM tones. Hear Res 10: 301–330

    Article  CAS  PubMed  Google Scholar 

  • Rees A, Møller A (1987) Stimulus properties influencing the repsonses of inferior colliculus neurons to amplitude-modulated sounds. Hear Res 27: 129–143

    Article  CAS  PubMed  Google Scholar 

  • Rees A, Palmer A (1989) Neuronal responses to amplitude-modulated and pure-tone stimuli in the guinea pig inferior colliculus, and their modification by broadband noise. J Acoust Soc Am 85: 1978–1994

    Article  CAS  PubMed  Google Scholar 

  • Schreiner C, Langner G (1988) Periodicity coding in the inferior colliculus of the cat. II. Topograhical organization. J Neurophysiol 60: 1823–1840

    CAS  PubMed  Google Scholar 

  • Shannon R, Zeng FG, Kamath V, Wygonski J, Ekelid M (1995) Speech recognition with primarily temporal cues. Science 270: 303–304

    Article  CAS  PubMed  Google Scholar 

  • Speck-Hergenröder J, Barth F (1987) Tuning of vibration sensitive neurons in the central nervous system of a wandering spider, Cupiennius salei Keys. J Comp Physiol A 160: 467–475

    Article  Google Scholar 

  • van Hemmen JL (2001) Theory of synaptic plasticity. In: Moss F, Gielen S (eds) Handbook of biological physics, neuro-informatics, neural modelling, vol 4. Elsevier, Amsterdam, pp 771–823

    Google Scholar 

  • Wehr M, Zador AM (2003) Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426: 442–446

    Article  CAS  PubMed  Google Scholar 

  • Wickesberg RE (1996) Rapid inhibition in the cochlear nuclear complex of the chinchilla. J Acoust Soc Am 100(3): 1691–1702

    Article  CAS  PubMed  Google Scholar 

  • Yost W (1994) Fundamentals of Hearing: an introduction, 3rd edn. Academic, San Diego

    Google Scholar 

  • Zhang LI, Tan AYY, Schreiner CE, Merzenich MM (2003) Topography and synaptic shaping of direction selectivity in primary auditory cortex. Nature 424(10): 201–205

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Moritz Bürck.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bürck, M., van Hemmen, J.L. Neuronal identification of signal periodicity by balanced inhibition. Biol Cybern 100, 261–270 (2009). https://doi.org/10.1007/s00422-009-0302-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00422-009-0302-0

Keywords

Navigation