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.
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
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
Bendor D, Wang X (2005) The neuronal representation of pitch in primate auditory cortex. Nature 436: 1161–1165
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
Bregman A (1990) Auditory scene analysis. MIT Press, Cambridge
Cherry EC (1953) Some experiments on the recognition of speech, with one and with two ears. J Acoust Soc Am 25(5): 975–979
Coombs S, Görner P, Münz H (eds) (1989) Themechanosensory lateral line: neurobiology and evolution. Springer, New York
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
Friedel P, Bürck M, van Hemmen JL (2007) Neuronal identification of acoustic signal periodicity. Biol Cybern 97: 247–260
Gerstner W, Kistler W (2002) Spiking neuron models. Cambridge University Press, Cambridge
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
Highley MJ, Contreras D (2006) Balanced excitation and inhibition determine spike timing during frequency adaptation. J Neurosci 26(2): 448–457
Izhikevich EM (2001) Resonate-and-fire neurons. Neural Netw 14: 883–894
Joris PX, Schreiner CE, Rees A (2004) Neural processing of amplitude-modulated sounds. Physiol Rev 84: 541–577
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
Käse R., Bleckmann H (1987) Prey localization by surface wave ray-tracing: fish track bugs like oceanographers track storms. Experientia 43: 290–293
Krishna B, Semple M (2000) Auditory temporal processing: response to sinusoidally amplitude-moulated tones in the inferior colliculus. J Neurophysiol 84: 255–273
Langner G (1992) Periodicity coding in the auditory system. Hear Res 60: 115–142
Langner G, Schreiner C (1988) Periodicity coding in the inferior colliculus of the cat. I. Neuronal mechanisms. J Neurophysiol 60: 1799–1822
Large EW, Crawford JD (2002) Auditory temporal computation: interval selectivity based on post-inhibitory rebound. J Comput Neurosci 13: 125–142
Las L, Stern EA, Nelken I (2005) Representation of tone in fluctuating maskers in the ascending auditory system. J Neurosci 25(6): 1503–1513
Licklider J (1951) A duplex theory of pitch perception. Experientia 7: 128–134
Meddis R, O’Mard L (2006) Virtual pitch in a computational physiological model. J Acoust Soc. Am. 120(6): 3861–3869
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
Nelken I, Rotman Y, Bar Yosef O (1999) Responses of auditory-cortex neurons to structural features of natural sounds. Nature 397: 154–157
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
Okun M, Lampl I (2008) Instantaneous correlation of excitation and inhibition during ongoing and sensory-evoked activities. Nat Neurosci 11(5): 535–537
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
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
Rees A, Møller A (1987) Stimulus properties influencing the repsonses of inferior colliculus neurons to amplitude-modulated sounds. Hear Res 27: 129–143
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
Schreiner C, Langner G (1988) Periodicity coding in the inferior colliculus of the cat. II. Topograhical organization. J Neurophysiol 60: 1823–1840
Shannon R, Zeng FG, Kamath V, Wygonski J, Ekelid M (1995) Speech recognition with primarily temporal cues. Science 270: 303–304
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
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
Wehr M, Zador AM (2003) Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426: 442–446
Wickesberg RE (1996) Rapid inhibition in the cochlear nuclear complex of the chinchilla. J Acoust Soc Am 100(3): 1691–1702
Yost W (1994) Fundamentals of Hearing: an introduction, 3rd edn. Academic, San Diego
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
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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
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DOI: https://doi.org/10.1007/s00422-009-0302-0