Neuronal identification of acoustic signal periodicity

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.

[1]  J. Hemmen.  Chapter 18 Theory of synaptic plasticity , 2001 .

[2]  A. Hudspeth,et al.  Sensitivity, polarity, and conductance change in the response of vertebrate hair cells to controlled mechanical stimuli. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[3]  G. Schuller,et al.  Natural ultrasonic echoes from wing beating insects are encoded by collicular neurons in the CF-FM bat,Rhinolophus ferrumequinum , 2004, Journal of Comparative Physiology A.

[4]  Ray Meddis,et al.  Virtual pitch in a computational physiological model. , 2006, The Journal of the Acoustical Society of America.

[5]  H. Markl,et al.  Transmission of vibration in a spider's web , 1986 .

[6]  D. McAlpine,et al.  Spike-frequency adaptation in the inferior colliculus. , 2004, Journal of neurophysiology.

[7]  Ad Aertsen,et al.  Stable propagation of synchronous spiking in cortical neural networks , 1999, Nature.

[8]  I. Dean,et al.  Neural population coding of sound level adapts to stimulus statistics , 2005, Nature Neuroscience.

[9]  D. Oertel.  The role of timing in the brain stem auditory nuclei of vertebrates. , 1999, Annual review of physiology.

[10]  F. G. Barth,et al.  Vibrations in the orb web of the spider Nephila clavipes: cues for discrimination and orientation , 1996, Journal of Comparative Physiology A.

[11]  R. Meddis,et al.  A unitary model of pitch perception. , 1997, The Journal of the Acoustical Society of America.

[12]  M. Ferragamo,et al.  Periodicity extraction in the anuran auditory nerve , 1993, Journal of Comparative Physiology A.

[13]  M. Semple,et al.  Auditory temporal processing: responses to sinusoidally amplitude-modulated tones in the inferior colliculus. , 2000, Journal of neurophysiology.

[14]  R. Blickhan,et al.  The time course and frequency content of hydrodynamic events caused by moving fish, frogs, and crustaceans , 1991, Journal of Comparative Physiology A.

[15]  Friedrich G. Barth,et al.  Neuroethology of the Spider Vibration Sense , 1985 .

[16]  J. Culling,et al.  Perceptual separation of concurrent speech sounds: absence of across-frequency grouping by common interaural delay. , 1995, The Journal of the Acoustical Society of America.

[17]  H. Bleckmann,et al.  Prey localization by surface wave ray-tracing: Fish track bugs like oceanographers track storms , 1987, Experientia.

[18]  Horst H. Lang.  Surface wave discrimination between prey and nonprey by the back swimmerNotonecta glauca L. (Hemiptera, Heteroptera) , 1980, Behavioral Ecology and Sociobiology.

[19]  H. Bleckmann.  Reception of hydrodynamic stimuli in aquatic and semiaquatic animals , 1994 .

[20]  J. Zwislocki,et al.  Short-term adaptation and incremental responses of single auditory-nerve fibers , 1975, Biological Cybernetics.

[21]  T N Buell,et al.  Combination of binaural information across frequency bands. , 1991, The Journal of the Acoustical Society of America.

[22]  Jürgen Tautz,et al.  Vibrational communication in the fiddler crab, Uca pugilator , 1990, Journal of Comparative Physiology A.

[23]  Anthony N. Burkitt,et al.  Synchronization of the Neural Response to Noisy Periodic Synaptic Input , 2001, Neural Computation.

[24]  Sheryl Coombs,et al.  The Mechanosensory Lateral Line , 1989 .

[25]  Hynek Hermansky,et al.  The Analysis and Representation of Speech , 2004 .

[26]  André Longtin,et al.  The cellular basis for parallel neural transmission of a high-frequency stimulus and its low-frequency envelope , 2006, Proceedings of the National Academy of Sciences.

[27]  F. Barth,et al.  Tuning of vibration sensitive neurons in the central nervous system of a wandering spider,Cupiennius salei Keys , 1987, Journal of Comparative Physiology A.

[28]  J. Tautz,et al.  The role of leaf structure in vibration propagation. , 2000, The Journal of the Acoustical Society of America.

[29]  W. M. Masters,et al.  Vibrations in the orbwebs of Nuctenea sclopetaria (Araneidae) , 1984, Behavioral Ecology and Sociobiology.

[30]  C E Schreiner,et al.  Neural processing of amplitude-modulated sounds. , 2004, Physiological reviews.

[31]  C. Schreiner,et al.  Periodicity coding in the inferior colliculus of the cat. I. Neuronal mechanisms. , 1988, Journal of neurophysiology.

[32]  Israel Nelken,et al.  Responses of auditory-cortex neurons to structural features of natural sounds , 1999, Nature.

[33]  Diana Deutsch,et al.  Octave generalization of specific interference effects in memory for tonal pitch , 1973 .

[34]  Peter A. Cariani,et al.  Neural timing nets , 2001, Neural Networks.

[35]  Wulfram Gerstner,et al.  Extracting Oscillations: Neuronal Coincidence Detection with Noisy Periodic Spike Input , 1998, Neural Computation.

[36]  W. Yost.  Auditory image perception and analysis: The basis for hearing , 1991, Hearing Research.

[37]  C. Schreiner,et al.  Periodicity coding in the inferior colliculus of the cat. II. Topographical organization. , 1988, Journal of neurophysiology.

[38]  A. Rees,et al.  Neuronal responses to amplitude-modulated and pure-tone stimuli in the guinea pig inferior colliculus, and their modification by broadband noise. , 1989, The Journal of the Acoustical Society of America.

[39]  Günther Palm,et al.  A biologically motivated neural network for phase extraction from complex sounds , 2004, Biological cybernetics.

[40]  Gerald Langner,et al.  Periodicity coding in the auditory system , 1992, Hearing Research.

[41]  E. C. Cmm,et al.  on the Recognition of Speech, with , 2008 .

[42]  Horst Bleckmann,et al.  Prey Identification and Prey Localization in Surface-feeding Fish and Fishing Spiders , 1988 .

[43]  R. Kempter,et al.  How the threshold of a neuron determines its capacity for coincidence detection. , 1998, Bio Systems.

[44]  Wulfram Gerstner,et al.  Spiking Neuron Models , 2002 .

[45]  Jelle Atema,et al.  Sensory Biology of Aquatic Animals , 1988, Springer New York.

[46]  L. A. Westerman,et al.  Rapid and short-term adaptation in auditory nerve responses , 1984, Hearing Research.

[47]  Anthony N. Burkitt,et al.  A review of the integrate-and-fire neuron model: II. Inhomogeneous synaptic input and network properties , 2006, Biological Cybernetics.

[48]  Horst Bleckmann,et al.  Frequency discrimination of the surface-feeding fishAplocheilus lineatus — A prerequisite for prey localization? , 1981, Journal of comparative physiology.

[49]  A. Elepfandt.  Wave frequency recognition and absolute pitch for water waves in the clawed frog,Xenopus laevis , 1986, Journal of Comparative Physiology A.

[50]  P. Brownell,et al.  Compressional and Surface Waves in Sand: Used by Desert Scorpions to Locate Prey , 1977, Science.

[51]  F. Barth,et al.  The release of attack and escape behavior by vibratory stimuli in a wandering spider (Cupiennim salei keys.) , 1983, Journal of comparative physiology.

[52]  J. Licklider,et al.  A duplex theory of pitch perception , 1951, Experientia.

[53]  L. Demany,et al.  Dichotic fusion of two tones one octave apart: evidence for internal octave templates. , 1988, The Journal of the Acoustical Society of America.

[54]  A. Bregman.  Auditory Scene Analysis , 2008 .

[55]  L. Humphreys.  Generalization as a function of method of reinforcement. , 1939 .

[56]  Ad. J. Kalmijn,et al.  Hydrodynamic and Acoustic Field Detection , 1988 .

[57]  Anthony N. Burkitt,et al.  A Review of the Integrate-and-fire Neuron Model: I. Homogeneous Synaptic Input , 2006, Biological Cybernetics.

[58]  Zachary M. Smith,et al.  Chimaeric sounds reveal dichotomies in auditory perception , 2002, Nature.

[59]  Gregoire Nicolis,et al.  Stochastic resonance , 2007, Scholarpedia.

[60]  D. Bendor,et al.  The neuronal representation of pitch in primate auditory cortex , 2005, Nature.

[61]  R V Shannon,et al.  Speech Recognition with Primarily Temporal Cues , 1995, Science.

[62]  H. Bleckmann,et al.  Stimulus discrimination and wave source localization in fishing spiders (Dolomedes triton and D. okefinokensis) , 1994, Journal of Comparative Physiology A.

[63]  J. T. Marsh,et al.  Human auditory frequency-following responses to a missing fundamental. , 1978, Science.

[64]  P. Cariani.  Recurrent timing nets for auditory scene analysis , 2003, Proceedings of the International Joint Conference on Neural Networks, 2003..

[65]  F. Huntingford.  The Mechanosensory Lateral Line: Neurobiology and Evolution, S. Coombs, P. Görner, H. Münz (Eds.). Springer-Verlag, New York ((1989)), xvii , 1990 .

[66]  Adrian Rees,et al.  Stimulus properties influencing the responses of inferior colliculus neurons to amplitude-modulated sounds , 1987, Hearing Research.

[67]  Adrian Rees,et al.  Responses of neurons in the inferior colliculus of the rat to AM and FM tones , 1983, Hearing Research.

[68]  B. Grothe,et al.  Temporal processing in sensory systems , 2000, Current Opinion in Neurobiology.

[69]  L. Trussell,et al.  Synaptic mechanisms for coding timing in auditory neurons. , 1999, Annual review of physiology.

[70]  F. Barth,et al.  Spider vibration receptors: Threshold curves of individual slits in the metatarsal lyriform organ , 1982, Journal of comparative physiology.

[71]  Daniel P. W. Ellis,et al.  The auditory organization of speech and other sources in listeners and computational models , 2001, Speech Commun..

[72]  L. Trussell,et al.  A characterization of excitatory postsynaptic potentials in the avian nucleus magnocellularis. , 1994, Journal of neurophysiology.

[73]  Friedrich G. Barth,et al.  The Vibrational Sense of Spiders , 1998 .