Neural coding of periodicity in marmoset auditory cortex.

Pitch, our perception of how high or low a sound is on a musical scale, crucially depends on a sound's periodicity. If an acoustic signal is temporally jittered so that it becomes aperiodic, the pitch will no longer be perceivable even though other acoustical features that normally covary with pitch are unchanged. Previous electrophysiological studies investigating pitch have typically used only periodic acoustic stimuli, and as such these studies cannot distinguish between a neural representation of pitch and an acoustical feature that only correlates with pitch. In this report, we examine in the auditory cortex of awake marmoset monkeys (Callithrix jacchus) the neural coding of a periodicity's repetition rate, an acoustic feature that covaries with pitch. We first examine if individual neurons show similar repetition rate tuning for different periodic acoustic signals. We next measure how sensitive these neural representations are to the temporal regularity of the acoustic signal. We find that neurons throughout auditory cortex covary their firing rate with the repetition rate of an acoustic signal. However, similar repetition rate tuning across acoustic stimuli and sensitivity to temporal regularity were generally only observed in a small group of neurons found near the anterolateral border of primary auditory cortex, the location of a previously identified putative pitch processing center. These results suggest that although the encoding of repetition rate is a general component of auditory cortical processing, the neural correlate of periodicity is confined to a special class of pitch-selective neurons within the putative pitch processing center of auditory cortex.

[1]  Daniel Bendor,et al.  Cortical representations of pitch in monkeys and humans , 2006, Current Opinion in Neurobiology.

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

[3]  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.

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

[5]  Doris Y. Tsao,et al.  A Cortical Region Consisting Entirely of Face-Selective Cells , 2006, Science.

[6]  C. M. Marin,et al.  Concurrent vowel identification II: Effects of phase, harmonicity and task , 1997 .

[7]  Israel Nelken,et al.  Responses of auditory cortex to complex stimuli: functional organization revealed using intrinsic optical signals. , 2008, Journal of neurophysiology.

[8]  R. Llinás,et al.  Human oscillatory brain activity near 40 Hz coexists with cognitive temporal binding. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[9]  R. Goebel,et al.  Mirror-Symmetric Tonotopic Maps in Human Primary Auditory Cortex , 2003, Neuron.

[10]  Ling Qin,et al.  Neural mechanisms of interstimulus interval-dependent responses in the primary auditory cortex of awake cats , 2009, BMC Neuroscience.

[11]  M. Kilgard,et al.  Anesthesia suppresses nonsynchronous responses to repetitive broadband stimuli , 2007, Neuroscience.

[12]  Christopher J. Plack,et al.  Differences in frequency modulation detection and fundamental frequency discrimination between complex tones consisting of resolved and unresolved harmonics , 1995 .

[13]  P. Müller-Preuss,et al.  Auditory responsive cortex in the squirrel monkey: neural responses to amplitude-modulated sounds , 1996, Experimental Brain Research.

[14]  C D Salzman,et al.  Neural mechanisms for forming a perceptual decision. , 1994, Science.

[15]  R. Ritsma Existence Region of the Tonal Residue. I , 1962 .

[16]  X Wang,et al.  Temporal discharge patterns evoked by rapid sequences of wide- and narrowband clicks in the primary auditory cortex of cat. , 2000, Journal of neurophysiology.

[17]  Sridhar Kalluri,et al.  Perception and cortical neural coding of harmonic fusion in ferrets. , 2008, The Journal of the Acoustical Society of America.

[18]  Roy D. Patterson,et al.  The relative strength of the tone and noise components in iterated rippled noise , 1996 .

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

[20]  I. Pollack Discrimination of mean temporal interval within jittered auditory pulse trains. , 1968, The Journal of the Acoustical Society of America.

[21]  I. Whitfield,et al.  RESPONSES OF AUDITORY CORTICAL NEURONS TO STIMULI OF CHANGING FREQUENCY. , 1965, Journal of neurophysiology.

[22]  Ranulfo Romo,et al.  Neural codes for perceptual discrimination of acoustic flutter in the primate auditory cortex , 2009, Proceedings of the National Academy of Sciences.

[23]  Roy D. Patterson,et al.  Distortion products and the perceived pitch of harmonic complex tones , 2001 .

[24]  E. Owens,et al.  An Introduction to the Psychology of Hearing , 1997 .

[25]  J. Kaas,et al.  Architectonic identification of the core region in auditory cortex of macaques, chimpanzees, and humans , 2001, The Journal of comparative neurology.

[26]  Xiaoqin Wang,et al.  Cortical processing of temporal modulations , 2003, Speech Commun..

[27]  C. Schreiner,et al.  Thalamocortical transformation of responses to complex auditory stimuli , 2004, Experimental Brain Research.

[28]  Emilio Salinas,et al.  Cognitive neuroscience: Flutter Discrimination: neural codes, perception, memory and decision making , 2003, Nature Reviews Neuroscience.

[29]  R. Patterson,et al.  The Processing of Temporal Pitch and Melody Information in Auditory Cortex , 2002, Neuron.

[30]  D. H. Johnson,et al.  The relationship between spike rate and synchrony in responses of auditory-nerve fibers to single tones. , 1980, The Journal of the Acoustical Society of America.

[31]  Alan R Palmer,et al.  Phase-locked responses to pure tones in the primary auditory cortex , 2002, Hearing Research.

[32]  V B Mountcastle,et al.  Neuronal Coding by Cortical Cells of the Frequency of Oscillating Peripheral Stimuli , 1968, Science.

[33]  B. Moore An Introduction to the Psychology of Hearing , 1977 .

[34]  G. Recanzone,et al.  Single-neuron responses to rapidly presented temporal sequences in the primary auditory cortex of the awake macaque monkey. , 2007, Journal of neurophysiology.

[35]  M. Scherg,et al.  Structural and functional asymmetry of lateral Heschl's gyrus reflects pitch perception preference , 2005, Nature Neuroscience.

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

[37]  C Kaernbach,et al.  Psychophysical evidence against the autocorrelation theory of auditory temporal processing. , 1998, The Journal of the Acoustical Society of America.

[38]  S. R. Jammalamadaka,et al.  Directional Statistics, I , 2011 .

[39]  W A Yost,et al.  A time domain description for the pitch strength of iterated rippled noise. , 1996, The Journal of the Acoustical Society of America.

[40]  R. Plomp Rate of Decay of Auditory Sensation , 1964 .

[41]  J. Kaas,et al.  Subdivisions and connections of auditory cortex in owl monkeys , 1992, The Journal of comparative neurology.

[42]  Andrew J Oxenham,et al.  A Neural Representation of Pitch Salience in Nonprimary Human Auditory Cortex Revealed with Functional Magnetic Resonance Imaging , 2004, The Journal of Neuroscience.

[43]  Daniel Bendor,et al.  Differential neural coding of acoustic flutter within primate auditory cortex , 2007, Nature Neuroscience.

[44]  R. Fay,et al.  Pitch : neural coding and perception , 2005 .

[45]  R. L. Rennaker,et al.  Response to broadband repetitive stimuli in auditory cortex of the unanesthetized rat , 2006, Hearing Research.

[46]  J. Ostwald,et al.  Temporal Coding of Amplitude and Frequency Modulation in the Rat Auditory Cortex , 1995, The European journal of neuroscience.

[47]  Uwe Baumann,et al.  Pulse rate discrimination with deeply inserted electrode arrays , 2004, Hearing Research.

[48]  Christopher J Plack,et al.  The human ‘pitch center’ responds differently to iterated noise and Huggins pitch , 2007, Neuroreport.

[49]  Christopher DiMattina,et al.  Virtual vocalization stimuli for investigating neural representations of species-specific vocalizations. , 2006, Journal of neurophysiology.

[50]  N Suga,et al.  Functional properties of auditory neurones in the cortex of echo‐locating bats. , 1965, The Journal of physiology.

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

[52]  D. Bendor,et al.  Neural response properties of primary, rostral, and rostrotemporal core fields in the auditory cortex of marmoset monkeys. , 2008, Journal of neurophysiology.

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

[54]  Fan-Gang Zeng,et al.  Temporal pitch in electric hearing , 2002, Hearing Research.

[55]  G. A. Miller,et al.  The Perception of Repeated Bursts of Noise , 1948 .

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

[57]  F B Simmons,et al.  Electrical stimulation of the auditory nerve in man. , 1966, Archives of otolaryngology.

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

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

[60]  Brian E. Russ,et al.  Prefrontal Neurons Predict Choices during an Auditory Same-Different Task , 2008, Current Biology.

[61]  W. Shofner,et al.  Responses of ventral cochlear nucleus units in the chinchilla to amplitude modulation by low-frequency, two-tone complexes. , 1996, The Journal of the Acoustical Society of America.

[62]  D. Bendor,et al.  Neural coding of temporal information in auditory thalamus and cortex , 2008, Neuroscience.

[63]  William A Yost,et al.  Pitch strength of regular-interval click trains with different length "runs" of regular intervals. , 2005, The Journal of the Acoustical Society of America.

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

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

[66]  I. Pollack Asynchrony: the perception of temporal gaps within periodic auditory pulse patterns. , 1967, The Journal of the Acoustical Society of America.

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

[68]  D. A. Ronken,et al.  Monaural detection of a phase difference between clicks. , 1970, The Journal of the Acoustical Society of America.

[69]  Robert J. Zatorre,et al.  Depth electrode recordings show double dissociation between pitch processing in lateral Heschl’s gyrus and sound onset processing in medial Heschl’s gyrus , 2008, Experimental Brain Research.

[70]  R. Shannon Multichannel electrical stimulation of the auditory nerve in man. I. Basic psychophysics , 1983, Hearing Research.

[71]  S. Shamma,et al.  Organization of response areas in ferret primary auditory cortex. , 1993, Journal of neurophysiology.

[72]  J. Kaas,et al.  Subdivisions of auditory cortex and processing streams in primates. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[75]  Hideki Kawahara,et al.  Concurrent vowel identification. I. Effects of relative amplitude and F0 difference , 1997, The Journal of the Acoustical Society of America.

[76]  Xiaoqin Wang,et al.  Sustained firing in auditory cortex evoked by preferred stimuli , 2005, Nature.

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

[78]  W. Newsome,et al.  Neuronal and psychophysical sensitivity to motion signals in extrastriate area MST of the macaque monkey , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[79]  I. Pollack Asynchrony II: Perception of temporal gaps within periodic and jittered pulse patterns. , 1968, The Journal of the Acoustical Society of America.

[80]  N. Logothetis,et al.  Functional Imaging Reveals Numerous Fields in the Monkey Auditory Cortex , 2006, PLoS biology.

[81]  A. King,et al.  Encoding of virtual acoustic space stimuli by neurons in ferret primary auditory cortex. , 2005, Journal of neurophysiology.

[82]  Andrew J Oxenham,et al.  Correct tonotopic representation is necessary for complex pitch perception. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[83]  G. M. BESSER,et al.  Some Physiological Characteristics of Auditory Flutter Fusion in Man , 1967, Nature.

[84]  Mitchell Steinschneider,et al.  Phase-locked cortical responses to a human speech sound and low-frequency tones in the monkey , 1980, Brain Research.

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

[86]  R. Patterson,et al.  The lower limit of pitch as determined by rate discrimination. , 2000, The Journal of the Acoustical Society of America.

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

[88]  M R Schroeder,et al.  Flat-spectrum speech. , 1986, The Journal of the Acoustical Society of America.

[89]  J. C. Middlebrooks,et al.  Codes for sound-source location in nontonotopic auditory cortex. , 1998, Journal of neurophysiology.

[90]  N. C. Singh,et al.  Modulation spectra of natural sounds and ethological theories of auditory processing. , 2003, The Journal of the Acoustical Society of America.

[91]  Maoz Shamir,et al.  Cortical Discrimination of Complex Natural Stimuli: Can Single Neurons Match Behavior? , 2007, The Journal of Neuroscience.

[92]  M. Merzenich,et al.  Covariation of latency and temporal resolution in the inferior colliculus of the cat , 1987, Hearing Research.

[93]  M. Goldstein,et al.  Cortical coding of repetitive acoustic pulses. , 1972, Brain research.