Linking Cortical Spike Pattern Codes to Auditory Perception

Neurometric analysis has proven to be a powerful tool for studying links between neural activity and perception, especially in visual and somatosensory cortices, but conventional neurometrics are based on a simplistic rate-coding hypothesis that is clearly at odds with the rich and complex temporal spiking patterns evoked by many natural stimuli. In this study, we investigated the possible relationships between temporal spike pattern codes in the primary auditory cortex (A1) and the perceptual detection of subtle changes in the temporal structure of a natural sound. Using a two-alternative forced-choice oddity task, we measured the ability of human listeners to detect local time reversals in a marmoset twitter call. We also recorded responses of neurons in A1 of anesthetized and awake ferrets to these stimuli, and analyzed these responses using a novel neurometric approach that is sensitive to temporal discharge patterns. We found that although spike count-based neurometrics were inadequate to account for behavioral performance on this auditory task, neurometrics based on the temporal discharge patterns of populations of A1 units closely matched the psychometric performance curve, but only if the spiking patterns were resolved at temporal resolutions of 20 msec or better. These results demonstrate that neurometric discrimination curves can be calculated for temporal spiking patterns, and they suggest that such an extension of previous spike count-based approaches is likely to be essential for understanding the neural correlates of the perception of stimuli with a complex temporal structure.

[1]  M M Merzenich,et al.  Representation of a species-specific vocalization in the primary auditory cortex of the common marmoset: temporal and spectral characteristics. , 1995, Journal of neurophysiology.

[2]  L. Optican,et al.  Role of inferior temporal neurons in visual memory. I. Temporal encoding of information about visual images, recalled images, and behavioral context. , 1992, Journal of neurophysiology.

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

[4]  X. Wang,et al.  On cortical coding of vocal communication sounds in primates. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[5]  A. Zador,et al.  Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex , 2003, Nature.

[6]  G H Recanzone,et al.  Correlation between the activity of single auditory cortical neurons and sound-localization behavior in the macaque monkey. , 2000, Journal of neurophysiology.

[7]  S. Rosen Temporal information in speech: acoustic, auditory and linguistic aspects. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[8]  M. DeWeese,et al.  Binary Spiking in Auditory Cortex , 2003, The Journal of Neuroscience.

[9]  Ira J. Hirsh,et al.  Auditory Perception of Temporal Order , 1959 .

[10]  H. Barlow,et al.  Single Units and Sensation: A Neuron Doctrine for Perceptual Psychology? , 1972, Perception.

[11]  Xiaoqin Wang,et al.  Differential representation of species-specific primate vocalizations in the auditory cortices of marmoset and cat. , 2001, Journal of neurophysiology.

[12]  J. C. Middlebrooks,et al.  Coding of Sound-Source Location by Ensembles of Cortical Neurons , 2000, The Journal of Neuroscience.

[13]  J. C. Middlebrooks,et al.  Cortical representation of auditory space: information-bearing features of spike patterns. , 2002, Journal of neurophysiology.

[14]  Gert Stange,et al.  Temporal synchronization in the primary auditory response in the pigeon , 1989, Hearing Research.

[15]  Alan R Palmer,et al.  Responses to the purr call in three areas of the guinea pig auditory cortex , 2005, Neuroreport.

[16]  J. Arezzo,et al.  Representation of the voice onset time (VOT) speech parameter in population responses within primary auditory cortex of the awake monkey. , 2003, The Journal of the Acoustical Society of America.

[17]  J. Movshon,et al.  The statistical reliability of signals in single neurons in cat and monkey visual cortex , 1983, Vision Research.

[18]  D G Pelli,et al.  Probe tone thresholds in the auditory nerve measured by two-interval forced-choice procedures. , 1987, The Journal of the Acoustical Society of America.

[19]  B Masterton,et al.  Contribution of auditory cortex to sound localization in the monkey (Macaca mulatta). , 1975, Journal of neurophysiology.

[20]  W. Newsome,et al.  Correlation between Speed Perception and Neural Activity in the Middle Temporal Visual Area , 2005, The Journal of Neuroscience.

[21]  R E Pastore,et al.  Temporal order judgment of auditory stimulus offset , 1983, Perception & psychophysics.

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

[23]  D. Bradley,et al.  Neural population code for fine perceptual decisions in area MT , 2005, Nature Neuroscience.

[24]  R. Efron TEMPORAL PERCEPTION, APHASIA AND D'EJ'A VU. , 1963, Brain : a journal of neurology.

[25]  J. Fritz,et al.  Dynamics of Precise Spike Timing in Primary Auditory Cortex , 2004, The Journal of Neuroscience.

[26]  J. Fritz,et al.  Rapid task-related plasticity of spectrotemporal receptive fields in primary auditory cortex , 2003, Nature Neuroscience.

[27]  Jos J Eggermont,et al.  Neuronal responses in cat primary auditory cortex to natural and altered species-specific calls , 2000, Hearing Research.

[28]  Mitchell Steinschneider,et al.  Intracortical responses in human and monkey primary auditory cortex support a temporal processing mechanism for encoding of the voice onset time phonetic parameter. , 2004, Cerebral cortex.

[29]  R. Romo,et al.  Neuronal correlates of sensory discrimination in the somatosensory cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[30]  K. Saberi,et al.  Cognitive restoration of reversed speech , 1999, Nature.

[31]  G. P. Moore,et al.  Statistical analysis and functional interpretation of neuronal spike data. , 1966, Annual review of physiology.

[32]  E. B. Wilson Probable Inference, the Law of Succession, and Statistical Inference , 1927 .

[33]  E. Javel,et al.  Stochastic properties of cat auditory nerve responses to electric and acoustic stimuli and application to intensity discrimination. , 2000, The Journal of the Acoustical Society of America.

[34]  R. Fay,et al.  Psychometric functions for level discrimination and the effects of signal duration in the goldfish (Carassius auratus): psychophysics and neurophysiology. , 1992, The Journal of the Acoustical Society of America.

[35]  Laurence O Trussell,et al.  Modulation of transmitter release at giant synapses of the auditory system , 2002, Current Opinion in Neurobiology.

[36]  M F Dorman,et al.  Relationship between N1 evoked potential morphology and the perception of voicing. , 2000, The Journal of the Acoustical Society of America.

[37]  Xiaoqin Wang,et al.  Neural representations of temporally asymmetric stimuli in the auditory cortex of awake primates. , 2001, Journal of neurophysiology.

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

[39]  J. Hanley,et al.  The meaning and use of the area under a receiver operating characteristic (ROC) curve. , 1982, Radiology.

[40]  R. Romo,et al.  Functional properties of primate putamen neurons during the categorization of tactile stimuli. , 1997, Journal of neurophysiology.

[41]  J. Rauschecker Cortical processing of complex sounds , 1998, Current Opinion in Neurobiology.

[42]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[43]  A. Parker,et al.  Sense and the single neuron: probing the physiology of perception. , 1998, Annual review of neuroscience.

[44]  P. Cariani Temporal Coding of Periodicity Pitch in the Auditory System: An Overview , 1999, Neural plasticity.

[45]  A. Stevens,et al.  Auditory perceptual consolidation in early-onset blindness , 2005, Neuropsychologia.

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

[47]  A. Parker,et al.  Neuronal activity and its links with the perception of multi-stable figures. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[48]  Alan Cowey,et al.  “Deaf Hearing”: Unacknowledged Detection of Auditory Stimuli in a Patient with Cerebral Deafness * * This paper was presented at the 3rd Annual Meeting on Towards a Science of Consciousness in Tucson, Arizona, USA, 1998. , 2000, Cortex.

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

[50]  H. Funkenstein,et al.  The effect of species-specific vocalization on the discharge of auditory cortical cells in the awake squirrel monkey (Saimiri sciureus) , 1973, Experimental Brain Research.

[51]  Rajiv Narayan,et al.  Distinct time scales in cortical discrimination of natural sounds in songbirds. , 2006, Journal of neurophysiology.

[52]  A. Parker,et al.  Comparing perceptual signals of single V5/MT neurons in two binocular depth tasks. , 2004, Journal of neurophysiology.

[53]  Angel R. Martinez,et al.  : Exploratory data analysis with MATLAB ® , 2007 .

[54]  John F. Brugge,et al.  The Structure of Spatial Receptive Fields of Neurons in Primary Auditory Cortex of the Cat , 1996, The Journal of Neuroscience.

[55]  R. Romo,et al.  Neural codes for perceptual discrimination in primary somatosensory cortex , 2005, Nature Neuroscience.

[56]  H B Barlow,et al.  Single units and sensation: a neuron doctrine for perceptual psychology? , 1972, Perception.

[57]  J. Eggermont Representation of a voice onset time continuum in primary auditory cortex of the cat. , 1995, Journal of the Acoustical Society of America.

[58]  J. Movshon,et al.  The analysis of visual motion: a comparison of neuronal and psychophysical performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.