Processing of harmonics in the lateral belt of macaque auditory cortex

Many speech sounds and animal vocalizations contain components, referred to as complex tones, that consist of a fundamental frequency (F0) and higher harmonics. In this study we examined single-unit activity recorded in the core (A1) and lateral belt (LB) areas of auditory cortex in two rhesus monkeys as they listened to pure tones and pitch-shifted conspecific vocalizations (“coos”). The latter consisted of complex-tone segments in which F0 was matched to a corresponding pure-tone stimulus. In both animals, neuronal latencies to pure-tone stimuli at the best frequency (BF) were ~10 to 15 ms longer in LB than in A1. This might be expected, since LB is considered to be at a hierarchically higher level than A1. On the other hand, the latency of LB responses to coos was ~10 to 20 ms shorter than to the corresponding pure-tone BF, suggesting facilitation in LB by the harmonics. This latency reduction by coos was not observed in A1, resulting in similar coo latencies in A1 and LB. Multi-peaked neurons were present in both A1 and LB; however, harmonically-related peaks were observed in LB for both early and late response components, whereas in A1 they were observed only for late components. Our results suggest that harmonic features, such as relationships between specific frequency intervals of communication calls, are processed at relatively early stages of the auditory cortical pathway, but preferentially in LB.

[1]  N Suga,et al.  Harmonic-sensitive neurons in the auditory cortex of the mustache bat. , 1979, Science.

[2]  Jerome Kagan,et al.  Perception of music by infants , 1996, Nature.

[3]  G. Recanzone,et al.  Frequency and intensity response properties of single neurons in the auditory cortex of the behaving macaque monkey. , 2000, Journal of neurophysiology.

[4]  E. Terhardt Pitch, consonance, and harmony. , 1974, The Journal of the Acoustical Society of America.

[5]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

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

[7]  M Steinschneider,et al.  Consonance and dissonance of musical chords: neural correlates in auditory cortex of monkeys and humans. , 2001, Journal of neurophysiology.

[8]  Sterling C. Johnson,et al.  A population-average MRI-based atlas collection of the rhesus macaque , 2009, NeuroImage.

[9]  A. Izumi,et al.  Japanese monkeys perceive sensory consonance of chords. , 2000, The Journal of the Acoustical Society of America.

[10]  J. Rauschecker,et al.  Processing of band-passed noise in the lateral auditory belt cortex of the rhesus monkey. , 2004, Journal of neurophysiology.

[11]  Jos J. Eggermont,et al.  Correlated neural activity as the driving force for functional changes in auditory cortex , 2007, Hearing Research.

[12]  C E Schreiner,et al.  Topography of excitatory bandwidth in cat primary auditory cortex: single-neuron versus multiple-neuron recordings. , 1992, Journal of neurophysiology.

[13]  J. Rauschecker,et al.  Phoneme and word recognition in the auditory ventral stream , 2012, Proceedings of the National Academy of Sciences.

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

[15]  Charles E Schroeder,et al.  Timing of pure tone and noise-evoked responses in macaque auditory cortex , 2005, Neuroreport.

[16]  W. Fitch The biology and evolution of music: A comparative perspective , 2006, Cognition.

[17]  D. Schwarz,et al.  Perception of the missing fundamental in nonhuman primates. , 1988, The Journal of the Acoustical Society of America.

[18]  D. Margoliash,et al.  Temporal and harmonic combination-sensitive neurons in the zebra finch's HVc , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  Xiaoqin Wang,et al.  Spectral integration in A1 of awake primates: neurons with single- and multipeaked tuning characteristics. , 2003, Journal of neurophysiology.

[20]  H. Scheich,et al.  Processing of sound sequences in macaque auditory cortex: response enhancement. , 1999, Journal of neurophysiology.

[21]  Richard C Saunders,et al.  Differential Coding of Conspecific Vocalizations in the Ventral Auditory Cortical Stream , 2014, The Journal of Neuroscience.

[22]  R. Goebel,et al.  Processing of Natural Sounds: Characterization of Multipeak Spectral Tuning in Human Auditory Cortex , 2013, The Journal of Neuroscience.

[23]  N. Logothetis,et al.  A combined MRI and histology atlas of the rhesus monkey brain in stereotaxic coordinates , 2007 .

[24]  C. Schroeder,et al.  Somatosensory input to auditory association cortex in the macaque monkey. , 2001, Journal of neurophysiology.

[25]  Xiaoqin Wang,et al.  Correlation of neural response properties with auditory thalamus subdivisions in the awake marmoset. , 2011, Journal of neurophysiology.

[26]  Mitchell Steinschneider,et al.  Neural Correlates of Auditory Scene Analysis Based on Inharmonicity in Monkey Primary Auditory Cortex , 2010, The Journal of Neuroscience.

[27]  Yukiko Kikuchi,et al.  Hierarchical Auditory Processing Directed Rostrally along the Monkey's Supratemporal Plane , 2010, The Journal of Neuroscience.

[28]  J. Rauschecker,et al.  Processing of complex sounds in the macaque nonprimary auditory cortex. , 1995, Science.

[29]  H. Heffner,et al.  Free-field audiogram of the Japanese macaque (Macaca fuscata). , 1999, The Journal of the Acoustical Society of America.

[30]  Jeffrey S. Johnson,et al.  Activity Related to Perceptual Judgment and Action in Primary Auditory Cortex , 2012, The Journal of Neuroscience.

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

[32]  J. Eggermont,et al.  Increasing Spectrotemporal Sound Density Reveals an Octave-Based Organization in Cat Primary Auditory Cortex , 2008, The Journal of Neuroscience.

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

[34]  J. Kagan,et al.  INFANTS' PERCEPTION OF CONSONANCE AND DISSONANCE IN MUSIC , 1998 .

[35]  Shinjiro Oonishi,et al.  FUNCTIONAL ORGANIZATION AND INTEGRATIVE MECHANISM ON THE AUDITORY CORTEX OF THE CAT , 1965 .

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

[37]  N. Suga,et al.  Facilitatory and inhibitory frequency tuning of combination-sensitive neurons in the primary auditory cortex of mustached bats. , 1999, Journal of neurophysiology.

[38]  J. Rauschecker,et al.  Functional Specialization in Rhesus Monkey Auditory Cortex , 2001, Science.

[39]  S. Shamma,et al.  The Relationship of Auditory Cortical Activity to Perception and Behavior , 2011 .

[40]  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.

[41]  Ankoor S. Shah,et al.  Timing and laminar profile of eye-position effects on auditory responses in primate auditory cortex. , 2004, Journal of neurophysiology.

[42]  Jacquelyne J. Rivera,et al.  Music perception and octave generalization in rhesus monkeys. , 2000, Journal of experimental psychology. General.

[43]  E. Schellenberg,et al.  Sensory consonance and the perceptual similarity of complex-tone harmonic intervals: tests of adult and infant listeners. , 1996, The Journal of the Acoustical Society of America.

[44]  C. Camalier,et al.  Neural latencies across auditory cortex of macaque support a dorsal stream supramodal timing advantage in primates , 2012, Proceedings of the National Academy of Sciences.

[45]  J. Rauschecker,et al.  Functional specialization of medial auditory belt cortex in the alert rhesus monkey. , 2009, Journal of neurophysiology.

[46]  Sterling C. Johnson,et al.  Rhesus macaque brain morphometry: a methodological comparison of voxel-wise approaches. , 2010, Methods.

[47]  Brian H Scott,et al.  Effect of Behavioral Context on Representation of a Spatial Cue in Core Auditory Cortex of Awake Macaques , 2007, The Journal of Neuroscience.

[48]  Biao Tian,et al.  Processing of frequency-modulated sounds in the lateral auditory belt cortex of the rhesus monkey. , 2004, Journal of neurophysiology.