Representation of spectrotemporal sound information in the ascending auditory pathway

Abstract.The representation of sound information in the central nervous system relies on the analysis of time-varying features in communication and other environmental sounds. How are auditory physiologists and theoreticians to choose an appropriate method for characterizing spectral and temporal acoustic feature representations in single neurons and neural populations? A brief survey of currently available scientific methods and their potential usefulness is given, with a focus on the strengths and weaknesses of using noise analysis techniques for approximating spectrotemporal response fields (STRFs). Noise analysis has been used to foster several conceptual advances in describing neural acoustic feature representation in a variety of species and auditory nuclei. STRFs have been used to quantitatively assess spectral and temporal transformations across mutually connected auditory nuclei, to identify neuronal interactions between spectral and temporal sound dimensions, and to compare linear vs. nonlinear response properties through state-dependent comparisons. We propose that noise analysis techniques used in combination with novel stimulus paradigms and parametric experiment designs will provide powerful means of exploring acoustic feature representations in the central nervous system.

[1]  C E Schreiner,et al.  Functional topography of cat primary auditory cortex: distribution of integrated excitation. , 1990, Journal of neurophysiology.

[2]  N Suga,et al.  Disproportionate tonotopic representation for processing CF-FM sonar signals in the mustache bat auditory cortex. , 1976, Science.

[3]  R. Reid,et al.  Rules of Connectivity between Geniculate Cells and Simple Cells in Cat Primary Visual Cortex , 2001, The Journal of Neuroscience.

[4]  S A Shamma,et al.  Spectro-temporal response field characterization with dynamic ripples in ferret primary auditory cortex. , 2001, Journal of neurophysiology.

[5]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

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

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

[8]  I. Nelken,et al.  Responses to linear and logarithmic frequency‐modulated sweeps in ferret primary auditory cortex , 2000, The European journal of neuroscience.

[9]  Jonathan Z. Simon,et al.  Robust Spectrotemporal Reverse Correlation for the Auditory System: Optimizing Stimulus Design , 2000, Journal of Computational Neuroscience.

[10]  K. Naka,et al.  Identification of multi-input biological systems. , 1974, IEEE transactions on bio-medical engineering.

[11]  R. Reid,et al.  Synaptic Integration in Striate Cortical Simple Cells , 1998, The Journal of Neuroscience.

[12]  Andrew J. King,et al.  Linear processing of spatial cues in primary auditory cortex , 2001, Nature.

[13]  Jeffrey J Wenstrup,et al.  Topographical distribution of delay-tuned responses in the mustached bat inferior colliculus , 2001, Hearing Research.

[14]  C. Schreiner,et al.  Gabor analysis of auditory midbrain receptive fields: spectro-temporal and binaural composition. , 2003, Journal of neurophysiology.

[15]  Barry J. Richmond,et al.  Information flow and temporal coding in primate pattern vision , 1995, Journal of Computational Neuroscience.

[16]  Victor A. F. Lamme,et al.  Feedforward, horizontal, and feedback processing in the visual cortex , 1998, Current Opinion in Neurobiology.

[17]  M. Merzenich,et al.  Changes of AI receptive fields with sound density. , 2002, Journal of neurophysiology.

[18]  C. Schreiner,et al.  Representation of amplitude modulation in the auditory cortex of the cat. II. Comparison between cortical fields , 1988, Hearing Research.

[19]  M M Merzenich,et al.  Representation of cochlea within primary auditory cortex in the cat. , 1975, Journal of neurophysiology.

[20]  J. P. Jones,et al.  An evaluation of the two-dimensional Gabor filter model of simple receptive fields in cat striate cortex. , 1987, Journal of neurophysiology.

[21]  D Margoliash,et al.  An introduction to birdsong and the avian song system. , 1997, Journal of neurobiology.

[22]  N Suga,et al.  Peripheral specialization for fine analysis of doppler-shifted echoes in the auditory system of the "CF-FM" bat Pteronotus parnellii. , 1975, The Journal of experimental biology.

[23]  K. Sen,et al.  Spectral-temporal Receptive Fields of Nonlinear Auditory Neurons Obtained Using Natural Sounds , 2022 .

[24]  E D Young,et al.  Linear and nonlinear spectral integration in type IV neurons of the dorsal cochlear nucleus. II. Predicting responses with the use of nonlinear models. , 1997, Journal of neurophysiology.

[25]  J. Eggermont.  Temporal modulation transfer functions for AM and FM stimuli in cat auditory cortex. Effects of carrier type, modulating waveform and intensity , 1994, Hearing Research.

[26]  Lee M. Miller,et al.  Functional Convergence of Response Properties in the Auditory Thalamocortical System , 2001, Neuron.

[27]  N Suga,et al.  Facilitative responses to species-specific calls in cortical FM-FM neurons of the mustached bat. , 1996, Neuroreport.

[28]  L. Palmer,et al.  The retinotopic organization of area 17 (striate cortex) in the cat , 1978, The Journal of comparative neurology.

[29]  Li I. Zhang,et al.  Topography and synaptic shaping of direction selectivity in primary auditory cortex , 2003, Nature.

[30]  M M Merzenich,et al.  Representation of the cochlea within the inferior colliculus of the cat. , 1974, Brain research.

[31]  I. Ohzawa,et al.  Spatiotemporal organization of simple-cell receptive fields in the cat's striate cortex. II. Linearity of temporal and spatial summation. , 1993, Journal of neurophysiology.

[32]  V. Bringuier,et al.  Horizontal propagation of visual activity in the synaptic integration field of area 17 neurons. , 1999, Science.

[33]  C E Schreiner,et al.  Functional organization of squirrel monkey primary auditory cortex: responses to pure tones. , 2001, Journal of neurophysiology.

[34]  P. I. M. Johannesma,et al.  Spectro-temporal characteristics of single units in the auditory midbrain of the lightly anaesthetised grass frog (Rana temporaria L.) Investigated with noise stimuli , 1981, Hearing Research.

[35]  D. Irvine,et al.  Sensitivity of neurons in cat primary auditory cortex to tones and frequency-modulated stimuli. II: Organization of response properties along the ‘isofrequency’ dimension , 1992, Hearing Research.

[36]  G D Lewen,et al.  Reproducibility and Variability in Neural Spike Trains , 1997, Science.

[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]  Christoph E Schreiner,et al.  Spectrotemporal structure of receptive fields in areas AI and AAF of mouse auditory cortex. , 2003, Journal of neurophysiology.

[40]  K. Sen,et al.  Feature analysis of natural sounds in the songbird auditory forebrain. , 2001, Journal of neurophysiology.

[41]  A. Doupe.  Song- and Order-Selective Neurons in the Songbird Anterior Forebrain and their Emergence during Vocal Development , 1997, The Journal of Neuroscience.

[42]  M. Liberman.  The cochlear frequency map for the cat: labeling auditory-nerve fibers of known characteristic frequency. , 1982, The Journal of the Acoustical Society of America.

[43]  C. Schreiner,et al.  Representation of amplitude modulation in the auditory cortex of the cat. I. The anterior auditory field (AAF) , 1986, Hearing Research.

[44]  Lee M. Miller,et al.  Spectrotemporal receptive fields in the lemniscal auditory thalamus and cortex. , 2002, Journal of neurophysiology.

[45]  C. Schreiner,et al.  Nonlinear Spectrotemporal Sound Analysis by Neurons in the Auditory Midbrain , 2002, The Journal of Neuroscience.

[46]  M. Merzenich,et al.  Optimizing sound features for cortical neurons. , 1998, Science.

[47]  K A Razak,et al.  Single cortical neurons serve both echolocation and passive sound localization. , 1999, Journal of neurophysiology.

[48]  D. Ferster,et al.  Neural mechanisms of orientation selectivity in the visual cortex. , 2000, Annual review of neuroscience.

[49]  C. Schreiner,et al.  Functional topography of cat primary auditory cortex: responses to frequency-modulated sweeps , 2004, Experimental Brain Research.

[50]  C E Schreiner,et al.  Modular organization of intrinsic connections associated with spectral tuning in cat auditory cortex , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[51]  J. H. Casseday,et al.  Neural tuning for sound duration: role of inhibitory mechanisms in the inferior colliculus. , 1994, Science.

[52]  C. Schreiner,et al.  Time course of forward masking tuning curves in cat primary auditory cortex. , 1997, Journal of neurophysiology.

[53]  D. Ferster,et al.  The contribution of noise to contrast invariance of orientation tuning in cat visual cortex. , 2000, Science.

[54]  Alan R. Palmer,et al.  Spectrotemporal Receptive Field Properties of Single Units in the Primary, Dorsocaudal and Ventrorostral Auditory Cortex of the Guinea Pig , 2002, Audiology and Neurotology.

[55]  N. Suga,et al.  Combination-sensitive neurons in the primary auditory cortex of the mustached bat , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  Xiaoqin Wang,et al.  Temporal and rate representations of time-varying signals in the auditory cortex of awake primates , 2001, Nature Neuroscience.