Abstract
Acoustic signals transmit information by temporal characteristics and envelope periodicity as well as by their frequency content. Many animals can extract the frequency content of a signal by means of specialized organs such as the cochlea but for the detection and identification of higher-order periodicity, e.g., amplitude modulations, this type of organ is useless. In addition, many animals do not have a cochlea but still depend on a reliable identification of different frequencies in the vast variety of acoustic signals they perceive in their natural environment. Hence, neural mechanisms to decode periodicity information must exist. We present a detailed mathematical analysis of a recurrent and a feedforward model of neuronal periodicity extraction and discuss basic constraints for neuronal circuitry performing such a task in a biological system. Both the recurrent and the feedforward model perform well using neuronal parameters typical for the auditory system. Performance is limited mainly by the temporal precision of the connections between the neurons.
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References
Aicher B, Tautz J (1990) Signal transmission through the substrate. J Comp Physiol A 166:345
Avendaño C, Deng L, Hermansky H, Gold B (2004) The analysis and representation of speech. In: Greenberg S, Ainsworth W, Popper A, Fay R (eds) Speech processing in the auditory system, chap. 2. Springer, New York, p. 63
Barth F (1985) Neuroethology of the spider vibration sense. In: Barth F (ed) Neurobiology of arachnids, chap. 11. Springer, New York, p 203
Barth F (1998) The vibrational sense of spiders. In: Hoy R, Popper A, Fay R (eds) Comparative hearing: insects, chap. 7. Springer, New York, p 228
Barth F, Geethabali (1982) Spider vibration receptors: threshold curves of individual slits in the metatarsal lyriform organ. J Comp Physiol A 148:175
Bendor D, Wang X (2005) The neuronal representation of pitch in primate auditory cortex. Nature 436:1161
Bleckmann H (1994) Reception of hydrodynamic stimuli in aquatic and semiaquatic animals. Gustav Fisher, Stuttgart
Bleckmann H (1998) Prey identification and prey localization in surface-feeding fish and fishing spiders. In: Atema J, Fay R, Popper A, Tavolga W (eds) Sensory biology of aquatic animals, chap. 24. Springer, New York, p 619
Bleckmann H, Waldner I, Schwartz E (1981) Frequency discrimination in the surface-feeding fish Aplocheilus lineatus—a prerequisite for prey localization?. J Comp Physiol A 143:485
Bleckmann H, Breithaubt T, Blickhan RJT (1991) The time course and frequency content of hydrodynamic events caused by moving fish, frogs and crustaceans. J Comp Physiol A 168:749
Bleckmann H, Borchard M, Horn P, Görner P (1994) Stimulus discrimination and wave source localization in fishing spiders (Dolomedes triton and D. okefinokensis). J Comp Physiol A 174:305
Borst M, Langner G, Palm G (2004) A biologically motivated network for phase extraction from complex sounds. Biol Cybern 90:98
Bregman A (1990) Auditory scene analysis. MIT Press, Cambridge, MA
Brownell P (1977) Compressional and surface waves in sand: used by desert scorpions to locate prey. Science 197:479
Buell T, Hafter E (1991) Combination of binaural information across frequency bands. J Acoust Soc Am 90:1894
Burkitt A (2006a) A review of the integrate-and-fire neuron model: I. Homogeneous synaptic input. Biol Cybern 95:1
Burkitt A (2006b) A review of the integrate-and-fire neuron model: II. Inhomogeneous synaptic input and network properties. Biol Cybern 95:97
Burkitt A, Clark G (2001) Synchronization of the neural response to noise periodic synaptic input. Neural Comp 13:2639
Cariani P (2001) Neural timing nets. Neur Netw 14:737
Cariani P (2003) Recurrent timing nets for auditory speech analysis. Proc Int Joint Conf Neural Netw 2:1575
Cherry E (1953) Some experiments on the recognition of speech, with one and with two ears. J Acoust Soc Am 25:975
Cooke M, Ellis D (2001) The auditory organization of speech and other sources in listeners and computational models. Speech Commun 35:141
Coombs S, Görner P, Münz He (1989) The mechanosensory lateral line: neurobiology and evolution. Springer, New York
Culling J, Summerfield Q (1995) Perceptual separation of concurrent speech sounds: absence of across-frequency grouping by common interaural delay. J Acoust Soc Am 98:785
Dean I, Harper N, McAlpine D (2005) Neural population coding of sound level adapts to stimulus statistics. Nat Neurosci 8:1684
Demany L, Semal C (1988) Dichotic fusion of 2 tones one octave apart: evidence for internal octave templates. J Acoust Soc Am 83:687
Deutsch D (1973) Octave generalization of specific interference effects in memory for tonal pitch. Percept Phychophys 13:271
Diesmann M, Gewaltig MO, Aertsen A (1999) Stable propagation of synchronous spiking in cortical neural networks. Nature 402:529
Elepfandt A (1986) Wave frequency recognition and absolute pitch for water waves in the clawed frog Xenopus laevis. J Comp Physiol A 158:235
Gammaitoni L, Hänggi P, Jung P, Marchesoni F (1998) Stochastic resonance. Rev Mod Phys 70:223
Gerstner W, Kistler W (2002) Spiking neuron models. Cambridge University Press, Cambridge
Grothe B, Klump G (2000) Temporal processing in sensory systems. Curr Opin Neurobiol 10:467
Hergenröder R, Barth F (1983) The release of attack and escape behavior by vibratory stimuli in a wandering spider (Cupiennius salei Keys). J Comp Physiol A 152:347
Hudspeth A, Corey D (1977) Sensitivity, polarity, and conductance change in the response of vertebrate hair cells to controlled mechanical stimuli. Proc Natl Acad Sci USA 74:2407
Humphreys L (1939) Generalization as a function of method of reinforcement. J Exp Psych 25:361
Ingham N, McAlpine D (2004) Spike-frequency adaptation in the inferior colliculus. J Neurophysiol 91:632
Joris P, Schreiner C, Rees A (2004) Neural processing of amplitude-modulated sounds. Physiol Rev 84:541
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, p 83
Käse R, Bleckmann H (1987) Prey localization by surface ray-tracing: fish track bugs like oceanographers track storms. Experientia 43:290
Kempter R, Gerstner W, Van Hemmen J, Wagner H (1998a) Extracting oscillations: Neural coincidence detection with noise periodic spike input. Neural Comp 10:1987
Kempter R, Gerstner W, Van Hemmen J (1998b) How the threshold of a neuron determines its capacity for coincidence detection. BioSys 48:105
Krishna B, Semple M (2000) Auditory temporal processing: response to sinusoidally amplitude-moulated tones in the inferior colliculus. J Neurophysiol 84:255
Landolfa M, Barth F (1996) Vibrations in the orb web of the spider Nephilia clavipes: Cues for discrimination and orientation. J Comp Physiol A 179:493
Lang H (1980) Surface wave discrimination between prey and nonprey by the backswimmer Notonecta glauca L. (Hemiptera, Heteroptera). Beh Ecol Sociobiol 6:233
Langner G (1992) Periodicity coding in the auditory system. Hear Res 60:115
Langner G, Schreiner C (1988) Periodicity coding in the inferior colliculus of the cat. i. neuronal mechanisms. J Neurophysiol 60:1799
Licklider J (1951) A duplex theory of pitch perception. Experientia 7:128
Magal C, Schöller M, Tautz J, Casas J (2000) The role of leaf structure in vibration propagation. J Acoust Soc Am 108:2412
Masters W (1984) Vibrations in the orbwebs of Nuctenea sclopetaria (Araneidae). Beh Ecol Sociobiol 15:217
Masters W, Markl H, Moffat A (1986) Transmission of vibration in a spider’s web. In: Shear W (ed) Spiders: Webs, Behavior, and Evolution, Chap. 3. Stanford University Press, Stanford, p 49
Meddis R, O’Mard L (1997) A unitary model of pitch perception. J Acoust Soc Am 102:1811
Meddis R, O’Mard L (2006) Virtual pitch in a computational physiological model. J Acoust Soc Am 120:3861
Megela Simmons A, Ferragamo M (1993) Periodicity extraction in the anuran auditory nerve. J Comp Physiol A 172:57
Middleton J, Longtin A, Benda J, Maler L (2006) The cellular basis for parallel neural transmission of a high-frequency stimulus and its low-frequency envelope. Proc Natl Acad Sci USA 103:14596
Nelken I, Rotman Y, Bar Yosef O (1999) Responses of auditory-cortex neurons to structural features of natural sounds. Nature 397:154
Oertel D (1999) The role of timing in the brain stem auditory nuclei of vertebrates. Ann Rev Physiol 61:497
Rees A, Møller A (1983) Responses of neurons in the inferior colliculus of the rat to am and fm tones. Hear Res 10:301
Rees A, Møller A (1987) Stimulus properties influencing the repsonses of inferior colliculus neurons to amplitude-modulated sounds. Hear Res 27:129
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
Schuller G (1984) Natural ultrasonic echoes from wing beating insects are encoded by collicular neurons in the CF-FM bat, Rhinolophus ferrumequinum. J Comp Physiol A 155:121
Schreiner C, Langner G (1988) Periodicity coding in the inferior colliculus of the cat. II. Topographical organization. J Neurophysiol 60:1823
Shannon R, Zeng FG, Kamath V, Wygonski J, Ekelid M (1995) Speech recognition with primarily temporal cues. Science 270:303
Smith R, Zwislocki J (1975) Short-term adaptation and incremental responses of single auditory-nerve fibers. Biol Cybern 17:169
Smith J, Marsh J, Greenberg S, Brown W (1978) Human auditory frequency-following responses to a missing fundamental. Science 201:639
Smith Z, Delgutte B, Oxenham A (2002) Chimaeric sounds reveal dichotomies in auditory perception. Nature 416:87
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
Trussell L (1999) Synaptic mechanisms for coding timing in auditory neurons. Ann Rev Physiol 61:477
Van Hemmen J (2001) Theory of synaptic plasticity. In: Moss F, Gielen S (eds) Handbook of biophysics, vol 4, Neuro-informatics and neural modelling, Chap. 18. Elsevier, Amsterdam, p 771
Westerman L, Smith R (1984) Rapid and short-term adaptation in auditory nerve responses. Hear Res 15:249
Yost W (1991) Auditory image perception and analysis: The basis for hearing. Hear Res 56:8
Zhang S, Trussell L (1994) A characterization of excitatory postsynaptic potentials in the avian nucleus magnocellularis. J Neurophysiol 72:705
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Friedel, P., Bürck, M. & Leo van Hemmen, J. Neuronal identification of acoustic signal periodicity. Biol Cybern 97, 247–260 (2007). https://doi.org/10.1007/s00422-007-0173-1
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DOI: https://doi.org/10.1007/s00422-007-0173-1