Neural spike-timing patterns vary with sound shape and periodicity in three auditory cortical fields.

Mammals perceive a wide range of temporal cues in natural sounds, and the auditory cortex is essential for their detection and discrimination. The rat primary (A1), ventral (VAF), and caudal suprarhinal (cSRAF) auditory cortical fields have separate thalamocortical pathways that may support unique temporal cue sensitivities. To explore this, we record responses of single neurons in the three fields to variations in envelope shape and modulation frequency of periodic noise sequences. Spike rate, relative synchrony, and first-spike latency metrics have previously been used to quantify neural sensitivities to temporal sound cues; however, such metrics do not measure absolute spike timing of sustained responses to sound shape. To address this, in this study we quantify two forms of spike-timing precision, jitter, and reliability. In all three fields, we find that jitter decreases logarithmically with increase in the basis spline (B-spline) cutoff frequency used to shape the sound envelope. In contrast, reliability decreases logarithmically with increase in sound envelope modulation frequency. In A1, jitter and reliability vary independently, whereas in ventral cortical fields, jitter and reliability covary. Jitter time scales increase (A1 < VAF < cSRAF) and modulation frequency upper cutoffs decrease (A1 > VAF > cSRAF) with ventral progression from A1. These results suggest a transition from independent encoding of shape and periodicity sound cues on short time scales in A1 to a joint encoding of these same cues on longer time scales in ventral nonprimary cortices.

[1]  R. Plomp Pitch of complex tones. , 1966, The Journal of the Acoustical Society of America.

[2]  I. Pollack Periodicity pitch for interrupted white noise--fact or artifact? , 1969, The Journal of the Acoustical Society of America.

[3]  E. Terhardt On the perception of periodic sound fluctuations (roughness) , 1974 .

[4]  E. M. Burns,et al.  Played-again SAM: Further observations on the pitch of amplitude-modulated noise , 1981 .

[5]  R. Plomp The Role of Modulation in Hearing , 1983 .

[6]  W. W. Clark,et al.  Detection of frequency and rate modulation by the chinchilla. , 1981, The Journal of the Acoustical Society of America.

[7]  J. Kelly,et al.  Organization of auditory cortex in the albino rat: sound frequency. , 1988, Journal of neurophysiology.

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

[9]  J. L. Hollett,et al.  Repetition rate and signal level effects on neuronal responses to brief tone pulses in cat auditory cortex. , 1989, The Journal of the Acoustical Society of America.

[10]  C. Cotman,et al.  The excitatory amino acid receptors: their classes, pharmacology, and distinct properties in the function of the central nervous system. , 1989, Annual review of pharmacology and toxicology.

[11]  D. P. Phillips,et al.  Response timing constraints on the cortical representation of sound time structure. , 1990, The Journal of the Acoustical Society of America.

[12]  Joseph E LeDoux,et al.  Information cascade from primary auditory cortex to the amygdala: corticocortical and corticoamygdaloid projections of temporal cortex in the rat. , 1993, Cerebral cortex.

[13]  D. P. Phillips Neural Representation of Stimulus Times in the Primary Auditory Cortex a , 1993, Annals of the New York Academy of Sciences.

[14]  F. Mascagni,et al.  Corticoamygdaloid and corticocortical projections of the rat temporal cortex: APhaseolus vulgaris leucoagglutinin study , 1993, Neuroscience.

[15]  C. Krumhansl,et al.  Isolating the dynamic attributes of musical timbre. , 1993, The Journal of the Acoustical Society of America.

[16]  R. Wilcox The percentage bend correlation coefficient , 1994 .

[17]  R. Plomp,et al.  Effect of reducing slow temporal modulations on speech reception. , 1994, The Journal of the Acoustical Society of America.

[18]  T. Sejnowski,et al.  Reliability of spike timing in neocortical neurons. , 1995, Science.

[19]  T. Irino,et al.  Temporal asymmetry in the auditory system. , 1996, The Journal of the Acoustical Society of America.

[20]  D. Irvine,et al.  First-spike timing of auditory-nerve fibers and comparison with auditory cortex. , 1997, Journal of neurophysiology.

[21]  John H. R. Maunsell,et al.  On the relationship between synaptic input and spike output jitter in individual neurons. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[22]  G. Langner,et al.  Periodicity coding in the primary auditory cortex of the Mongolian gerbil (Merionesunguiculatus ): two different coding strategies for pitch and rhythm? , 1997, Journal of Comparative Physiology A.

[23]  P. Heil,et al.  Auditory cortical onset responses revisited. I. First-spike timing. , 1997, Journal of neurophysiology.

[24]  M. Cassell,et al.  Cortical, thalamic, and amygdaloid projections of rat temporal cortex , 1997, The Journal of comparative neurology.

[25]  I. Peretz,et al.  Role of Familiarity in Auditory Discrimination of Musical Instrument: A Laterality Study , 1997, Cortex.

[26]  Idan Segev,et al.  Ion Channel Stochasticity May Be Critical in Determining the Reliability and Precision of Spike Timing , 1998, Neural Computation.

[27]  J. Eggermont Representation of spectral and temporal sound features in three cortical fields of the cat. Similarities outweigh differences. , 1998, Journal of neurophysiology.

[28]  J. Risset,et al.  Exploration of timbre by analysis and synthesis , 1999 .

[29]  Kenneth D. Miller,et al.  Cross-channel correlations in tetrode recordings: implications for spike-sorting , 1999, Neurocomputing.

[30]  J. Csicsvari,et al.  Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements. , 2000, Journal of neurophysiology.

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

[32]  P. Heil Representation of Sound Onsets in the Auditory System , 2001, Audiology and Neurotology.

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

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

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

[36]  Ralph M. Siegel,et al.  Deterministic dynamics emerging from a cortical functional architecture , 2001, Neural Networks.

[37]  Joseph E LeDoux,et al.  Redefining the tonotopic core of rat auditory cortex: Physiological evidence for a posterior field , 2002, The Journal of comparative neurology.

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

[39]  Xiaoqin Wang,et al.  Neural representations of sinusoidal amplitude and frequency modulations in the primary auditory cortex of awake primates. , 2002, Journal of neurophysiology.

[40]  Jufang He OFF responses in the auditory thalamus of the guinea pig. , 2002, Journal of neurophysiology.

[41]  Monty A. Escabí,et al.  Representation of spectrotemporal sound information in the ascending auditory pathway , 2003, Biological Cybernetics.

[42]  Peter Heil,et al.  Coding of temporal onset envelope in the auditory system , 2003, Speech Commun..

[43]  Michael P. Stryker,et al.  New Paradigm for Optical Imaging Temporally Encoded Maps of Intrinsic Signal , 2003, Neuron.

[44]  D. Copenhagen,et al.  Vesicular Glutamate Transporters 1 and 2 Target to Functionally Distinct Synaptic Release Sites , 2004, Science.

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

[46]  John P. Miller,et al.  Temporal encoding in nervous systems: A rigorous definition , 1995, Journal of Computational Neuroscience.

[47]  Christian Rosenmund,et al.  An essential role for vesicular glutamate transporter 1 (VGLUT1) in postnatal development and control of quantal size. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[48]  Xiaoqin Wang,et al.  Information content of auditory cortical responses to time-varying acoustic stimuli. , 2004, Journal of neurophysiology.

[49]  P. Heil First-spike latency of auditory neurons revisited , 2004, Current Opinion in Neurobiology.

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

[51]  M. Stryker,et al.  Fine functional organization of auditory cortex revealed by Fourier optical imaging. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[52]  Kelvin E. Jones,et al.  Neuronal variability: noise or part of the signal? , 2005, Nature Reviews Neuroscience.

[53]  T. Hromádka,et al.  Reliability and Representational Bandwidth in the Auditory Cortex , 2005, Neuron.

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

[55]  Nathan R. Wilson,et al.  Presynaptic Regulation of Quantal Size by the Vesicular Glutamate Transporter VGLUT1 , 2005, The Journal of Neuroscience.

[56]  D. Butts,et al.  Tuning Curves, Neuronal Variability, and Sensory Coding , 2006, PLoS biology.

[57]  Cyrus P. Billimoria,et al.  Neuromodulation of Spike-Timing Precision in Sensory Neurons , 2006, The Journal of Neuroscience.

[58]  S. Kuwada,et al.  Optimizing the Stimuli to Evoke the Amplitude Modulation Following Response (AMFR) in Neonates , 2006, Ear and hearing.

[59]  J. Kelly,et al.  Behavioral limits of auditory temporal resolution in the rat: amplitude modulation and duration discrimination. , 2006, Journal of comparative psychology.

[60]  Brian H Scott,et al.  Dynamic amplitude coding in the auditory cortex of awake rhesus macaques. , 2007, Journal of neurophysiology.

[61]  H. Read,et al.  Multiparametric auditory receptive field organization across five cortical fields in the albino rat. , 2007, Journal of neurophysiology.

[62]  M. Semple,et al.  Transformation of Temporal Properties between Auditory Midbrain and Cortex in the Awake Mongolian Gerbil , 2007, The Journal of Neuroscience.

[63]  M. Escabí,et al.  Early cortical damage in rat somatosensory cortex alters acoustic feature representation in primary auditory cortex , 2007, Neuroscience.

[64]  Edward L. Bartlett,et al.  Neural representations of temporally modulated signals in the auditory thalamus of awake primates. , 2007, Journal of neurophysiology.

[65]  S. Lomber,et al.  Double dissociation of 'what' and 'where' processing in auditory cortex , 2008, Nature Neuroscience.

[66]  G. Rosen,et al.  Detection of silent gaps in white noise following cortical deactivation in rats , 2008, Neuroreport.

[67]  Nathan C Higgins,et al.  Spectral processing deficits in belt auditory cortex following early postnatal lesions of somatosensory cortex , 2008, Neuroscience.

[68]  M. Escabí,et al.  Distinct Roles for Onset and Sustained Activity in the Neuronal Code for Temporal Periodicity and Acoustic Envelope Shape , 2008, The Journal of Neuroscience.

[69]  N. Lesica,et al.  The representation of amplitude modulations in the mammalian auditory midbrain. , 2008, Journal of neurophysiology.

[70]  S. Kuwada,et al.  Processing Temporal Modulations in Binaural and Monaural Auditory Stimuli by Neurons in the Inferior Colliculus and Auditory Cortex , 2009, Journal of the Association for Research in Otolaryngology.

[71]  M. Escabí,et al.  Spectral and temporal modulation tradeoff in the inferior colliculus. , 2010, Journal of neurophysiology.

[72]  Christopher I. Petkov,et al.  Complex Spectral Interactions Encoded by Auditory Cortical Neurons: Relationship Between Bandwidth and Pattern , 2010, Front. Syst. Neurosci..

[73]  Nathan C Higgins,et al.  Specialization of Binaural Responses in Ventral Auditory Cortices , 2010, The Journal of Neuroscience.

[74]  Sam R. Johnson,et al.  Temporal dynamics of sinusoidal and non‐sinusoidal amplitude modulation , 2010, The European journal of neuroscience.

[75]  N. Logothetis,et al.  Millisecond encoding precision of auditory cortex neurons , 2010, Proceedings of the National Academy of Sciences.

[76]  Nathan C Higgins,et al.  Thalamic label patterns suggest primary and ventral auditory fields are distinct core regions , 2010, The Journal of comparative neurology.

[77]  M. Wehr,et al.  Nonoverlapping Sets of Synapses Drive On Responses and Off Responses in Auditory Cortex , 2010, Neuron.

[78]  E. Gundelfinger,et al.  Onset Coding Is Degraded in Auditory Nerve Fibers from Mutant Mice Lacking Synaptic Ribbons , 2010, The Journal of Neuroscience.

[79]  A. Reyes Synaptic short-term plasticity in auditory cortical circuits , 2011, Hearing Research.

[80]  Nathan C Higgins,et al.  Thalamocortical pathway specialization for sound frequency resolution , 2011, The Journal of comparative neurology.

[81]  Edward L. Bartlett,et al.  A Computational Model of Cellular Mechanisms of Temporal Coding in the Medial Geniculate Body (MGB) , 2011, PloS one.

[82]  Judit Gervain,et al.  Auditory Perception of Self-Similarity in Water Sounds , 2011, Front. Integr. Neurosci..

[83]  Brian H Scott,et al.  Transformation of temporal processing across auditory cortex of awake macaques. , 2011, Journal of neurophysiology.

[84]  T. Hackett Information flow in the auditory cortical network , 2011, Hearing Research.

[85]  Kerry M. M. Walker,et al.  Cortical encoding of pitch: Recent results and open questions , 2011, Hearing Research.

[86]  Jeffrey S. Johnson,et al.  Amplitude modulation detection as a function of modulation frequency and stimulus duration: Comparisons between macaques and humans , 2011, Hearing Research.

[87]  R. Felix,et al.  Effects of ketamine on response properties of neurons in the superior paraolivary nucleus of the mouse , 2012, Neuroscience.

[88]  C. Pernet,et al.  The Role of Pitch and Timbre in Voice Gender Categorization , 2012, Front. Psychology.

[89]  Chen Chen,et al.  Precise Feature Based Time Scales and Frequency Decorrelation Lead to a Sparse Auditory Code , 2012, The Journal of Neuroscience.

[90]  Nathan C Higgins,et al.  Gene Expression Identifies Distinct Ascending Glutamatergic Pathways to Frequency-Organized Auditory Cortex in the Rat Brain , 2012, The Journal of Neuroscience.

[91]  Stephanie M. Gardner,et al.  A Computational Model of Inferior Colliculus Responses to Amplitude Modulated Sounds in Young and Aged Rats , 2012, Front. Neural Circuits.

[92]  R. Kanzaki,et al.  Pre-Attentive, Context-Specific Representation of Fear Memory in the Auditory Cortex of Rat , 2013, PloS one.

[93]  Mark D. McDonnell,et al.  Interaction of short-term depression and firing dynamics in shaping single neuron encoding , 2013, Front. Comput. Neurosci..

[94]  M. Kilgard,et al.  Cortical speech-evoked response patterns in multiple auditory fields are correlated with behavioral discrimination ability. , 2013, Journal of neurophysiology.

[95]  Guillaume A. Rousselet,et al.  Robust Correlation Analyses: False Positive and Power Validation Using a New Open Source Matlab Toolbox , 2012, Front. Psychology.

[96]  Y Zheng,et al.  Proportional spike-timing precision and firing reliability underlie efficient temporal processing of periodicity and envelope shape cues. , 2013, Journal of neurophysiology.

[97]  Jeffrey S. Johnson,et al.  Differences between Primary Auditory Cortex and Auditory Belt Related to Encoding and Choice for AM Sounds , 2013, The Journal of Neuroscience.

[98]  H. Helmholtz Die Lehre Von Den Tonempfindungen ALS Physiologische Grundlage Fur Die Theorie Der Musik , 2013 .

[99]  Yonggang Huang,et al.  A high-density, high-channel count, multiplexed μECoG array for auditory-cortex recordings. , 2014, Journal of neurophysiology.