A Neural Substrate for Rapid Timbre Recognition? Neural and Behavioral Discrimination of Very Brief Acoustic Vowels.

The timbre of a sound plays an important role in our ability to discriminate between behaviorally relevant auditory categories, such as different vowels in speech. Here, we investigated, in the primary auditory cortex (A1) of anesthetized guinea pigs, the neural representation of vowels with impoverished timbre cues. Five different vowels were presented with durations ranging from 2 to 128 ms. A psychophysical experiment involving human listeners showed that identification performance was near ceiling for the longer durations and degraded close to chance level for the shortest durations. This was likely due to spectral splatter, which reduced the contrast between the spectral profiles of the vowels at short durations. Effects of vowel duration on cortical responses were well predicted by the linear frequency responses of A1 neurons. Using mutual information, we found that auditory cortical neurons in the guinea pig could be used to reliably identify several vowels for all durations. Information carried by each cortical site was low on average, but the population code was accurate even for durations where human behavioral performance was poor. These results suggest that a place population code is available at the level of A1 to encode spectral profile cues for even very short sounds.

[1]  H. Helmholtz,et al.  On the Sensations of Tone as a Physiological Basis for the Theory of Music , 2005 .

[2]  Giles Wilkeson Gray Phonemic microtomy: The minimum duration of perceptible speech sounds , 1942 .

[3]  C. E. SHANNON,et al.  A mathematical theory of communication , 1948, MOCO.

[4]  Gunnar Fant,et al.  Acoustic Theory Of Speech Production , 1960 .

[5]  A. Liberman,et al.  The Identification and Discrimination of Synthetic Vowels , 1962 .

[6]  R. Plomp,et al.  Perceptual and physical space of vowel sounds. , 1969, The Journal of the Acoustical Society of America.

[7]  O. Tosi,et al.  Vowel recognition threshold as a function of temporal segmentations. , 1970, Journal of speech and hearing research.

[8]  Michael P. Beddoes,et al.  Discrimination of vowel sounds of very short duration , 1972 .

[9]  S. S. Stevens Frequency Analysis and Periodicity Detection in Hearing. , 1972 .

[10]  P. Welton,et al.  Backscattering of short ultrasonic pulses by solid elastic cylinders at large ka , 1979 .

[11]  M. Sachs,et al.  Encoding of steady-state vowels in the auditory nerve: representation in terms of discharge rate. , 1979, The Journal of the Acoustical Society of America.

[12]  Kuldip K. Paliwal,et al.  ON THE PERFORMANCE OF BURG'S METHOD OF MAXIMUM ENTROPY SPECTRAL ANALYSIS WHEN APPLIED TO VOICED SPEECH , 1982 .

[13]  C D Geisler,et al.  Responses of auditory-nerve fibers to consonant-vowel syllables. , 1981, The Journal of the Acoustical Society of America.

[14]  B. Delgutte,et al.  Speech coding in the auditory nerve: I. Vowel-like sounds. , 1984, The Journal of the Acoustical Society of America.

[15]  I. Winter,et al.  The representation of steady-state vowel sounds in the temporal discharge patterns of the guinea pig cochlear nerve and primarylike cochlear nucleus neurons. , 1986, The Journal of the Acoustical Society of America.

[16]  Joan M. Sinnott,et al.  Auditory frequency discrimination in primates: Species differences (Cercopithecus, Macaca, Homo). , 1987 .

[17]  The timbre of sung vowels. , 1988, The Journal of the Acoustical Society of America.

[18]  T. M. Nearey Static, dynamic, and relational properties in vowel perception. , 1989, The Journal of the Acoustical Society of America.

[19]  Donald Robertson,et al.  Plasticity of frequency organization in auditory cortex of guinea pigs with partial unilateral deafness , 1989, The Journal of comparative neurology.

[20]  A R Palmer,et al.  The representation of the spectra and fundamental frequencies of steady-state single- and double-vowel sounds in the temporal discharge patterns of guinea pig cochlear-nerve fibers. , 1990, The Journal of the Acoustical Society of America.

[21]  C. Schreiner,et al.  Physiology and topography of neurons with multipeaked tuning curves in cat primary auditory cortex. , 1991, Journal of neurophysiology.

[22]  J. Edeline,et al.  Receptive field plasticity in the auditory cortex during frequency discrimination training: selective retuning independent of task difficulty. , 1993, Behavioral neuroscience.

[23]  Bruno H. Repp,et al.  Speech Perception, Production and Linguistic Structure. , 1993 .

[24]  R. Patterson,et al.  The Duration Required to Identify the Instrument, the Octave, or the Pitch Chroma of a Musical Note , 1995 .

[25]  Roy D. Patterson,et al.  The stimulus duration required to identify vowels, their octave, and their pitch chroma , 1995 .

[26]  William Bialek,et al.  Entropy and Information in Neural Spike Trains , 1996, cond-mat/9603127.

[27]  S. Thorpe,et al.  Speed of processing in the human visual system , 1996, Nature.

[28]  E D Young,et al.  Effects of acoustic trauma on the representation of the vowel "eh" in cat auditory nerve fibers. , 1997, The Journal of the Acoustical Society of America.

[29]  A. Treves,et al.  The representational capacity of the distributed encoding of information provided by populations of neurons in primate temporal visual cortex , 1997, Experimental Brain Research.

[30]  B. May,et al.  Effects of bilateral olivocochlear lesions on vowel formant discrimination in cats , 1998, Hearing Research.

[31]  Alexander Borst,et al.  Information theory and neural coding , 1999, Nature Neuroscience.

[32]  J. Edeline,et al.  Effects of noradrenaline on frequency tuning of auditory cortex neurons during wakefulness and slow‐wave sleep , 1999, The European journal of neuroscience.

[33]  C E Schreiner,et al.  Correlations between neural discharges are related to receptive field properties in cat primary auditory cortex , 1999, The European journal of neuroscience.

[34]  Alan R. Palmer,et al.  Identification and localisation of auditory areas in guinea pig cortex , 2000, Experimental Brain Research.

[35]  Stefan Uppenkamp,et al.  The effects of temporal asymmetry on the detection and perception of short chirps 1 1 Parts of this study were presented during the 12th International Symposium on Hearing 2000 in Mierlo/NL (Uppenkamp et al., 2001). , 2001, Hearing Research.

[36]  Jean-Marc Edeline,et al.  Diversity of receptive field changes in auditory cortex during natural sleep , 2001, The European journal of neuroscience.

[37]  J. Victor Binless strategies for estimation of information from neural data. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[38]  T. Kitama,et al.  Critical spectral regions for vowel identification , 2002, Neuroscience Research.

[39]  Masataka Goto,et al.  RWC Music Database: Music genre database and musical instrument sound database , 2003, ISMIR.

[40]  William Bialek,et al.  Entropy and information in neural spike trains: progress on the sampling problem. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[41]  Matthew A. Wilson,et al.  Dynamic Analyses of Information Encoding in Neural Ensembles , 2004, Neural Computation.

[42]  Benjamin Halberstam,et al.  Vowel normalization: the role of fundamental frequency and upper formants , 2004, J. Phonetics.

[43]  Jos J. Eggermont,et al.  Neural connectivity only accounts for a small part of neural correlation in auditory cortex , 1996, Experimental Brain Research.

[44]  Gal Chechik,et al.  Encoding Stimulus Information by Spike Numbers and Mean Response Time in Primary Auditory Cortex , 2005, Journal of Computational Neuroscience.

[45]  Jan W. H. Schnupp,et al.  Plasticity of Temporal Pattern Codes for Vocalization Stimuli in Primary Auditory Cortex , 2006, The Journal of Neuroscience.

[46]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .

[47]  Gal Chechik,et al.  Reduction of Information Redundancy in the Ascending Auditory Pathway , 2006, Neuron.

[48]  A. Pouget,et al.  Neural correlations, population coding and computation , 2006, Nature Reviews Neuroscience.

[49]  A. R. Palmer,et al.  Laminar differences in the response properties of cells in the primary auditory cortex , 2007, Experimental Brain Research.

[50]  Gal Chechik,et al.  Information theory in auditory research , 2007, Hearing Research.

[51]  Rainer Goebel,et al.  "Who" Is Saying "What"? Brain-Based Decoding of Human Voice and Speech , 2008, Science.

[52]  Kerry M. M. Walker,et al.  Linking cortical spike pattern codes to auditory perception , 2008 .

[53]  Kerry M. M. Walker,et al.  Linking Cortical Spike Pattern Codes to Auditory Perception , 2008, Journal of Cognitive Neuroscience.

[54]  M. Kilgard,et al.  Cortical activity patterns predict speech discrimination ability , 2008, Nature Neuroscience.

[55]  Nima Mesgarani,et al.  Phoneme representation and classification in primary auditory cortex. , 2008, The Journal of the Acoustical Society of America.

[56]  Peter F Assmann,et al.  Identification of frequency-shifted vowels. , 2008, The Journal of the Acoustical Society of America.

[57]  Jean-Marc Edeline,et al.  A Spike-Timing Code for Discriminating Conspecific Vocalizations in the Thalamocortical System of Anesthetized and Awake Guinea Pigs , 2009, The Journal of Neuroscience.

[58]  Kerry M. M. Walker,et al.  Interdependent Encoding of Pitch, Timbre, and Spatial Location in Auditory Cortex , 2009, The Journal of Neuroscience.

[59]  J. Rauschecker,et al.  Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing , 2009, Nature Neuroscience.

[60]  Boris Gourévitch,et al.  Follow-up of latency and threshold shifts of auditory brainstem responses after single and interrupted acoustic trauma in guinea pig , 2009, Brain Research.

[61]  Kerry M. M. Walker,et al.  Multiplexed and Robust Representations of Sound Features in Auditory Cortex , 2011, The Journal of Neuroscience.

[62]  C. ten Cate,et al.  Zebra finches and Dutch adults exhibit the same cue weighting bias in vowel perception , 2011, Animal Cognition.

[63]  Boris Gourévitch,et al.  Age‐related changes in the guinea pig auditory cortex: relationship with brainstem changes and comparison with tone‐induced hearing loss , 2011, The European journal of neuroscience.

[64]  Boris Gourévitch,et al.  How different are the local field potentials and spiking activities? Insights from multi-electrodes arrays , 2012, Journal of Physiology-Paris.

[65]  M. Kilgard,et al.  Different timescales for the neural coding of consonant and vowel sounds. , 2013, Cerebral cortex.

[66]  J. Edeline,et al.  Cortical Inhibition Reduces Information Redundancy at Presentation of Communication Sounds in the Primary Auditory Cortex , 2013, The Journal of Neuroscience.

[67]  Yu Sato,et al.  Comparison of Neural Responses to Cat Meows and Human Vowels in the Anterior and Posterior Auditory Field of Awake Cats , 2013, PloS one.

[68]  J. Bizley,et al.  Neural and behavioral investigations into timbre perception , 2013, Front. Syst. Neurosci..

[69]  Kerry M. M. Walker,et al.  Spectral timbre perception in ferrets: discrimination of artificial vowels under different listening conditions. , 2013, The Journal of the Acoustical Society of America.

[70]  E. Hiebert Sensations of Tone as the Physiological Basis for the Theory of Music , 2014 .

[71]  Clara Suied,et al.  Auditory gist: recognition of very short sounds from timbre cues. , 2014, The Journal of the Acoustical Society of America.

[72]  Keith Johnson,et al.  Phonetic Feature Encoding in Human Superior Temporal Gyrus , 2014, Science.