Direct Recordings of Pitch Responses from Human Auditory Cortex

Summary Pitch is a fundamental percept with a complex relationship to the associated sound structure [1]. Pitch perception requires brain representation of both the structure of the stimulus and the pitch that is perceived. We describe direct recordings of local field potentials from human auditory cortex made while subjects perceived the transition between noise and a noise with a regular repetitive structure in the time domain at the millisecond level called regular-interval noise (RIN) [2]. RIN is perceived to have a pitch when the rate is above the lower limit of pitch [3], at approximately 30 Hz. Sustained time-locked responses are observed to be related to the temporal regularity of the stimulus, commonly emphasized as a relevant stimulus feature in models of pitch perception (e.g., [1]). Sustained oscillatory responses are also demonstrated in the high gamma range (80–120 Hz). The regularity responses occur irrespective of whether the response is associated with pitch perception. In contrast, the oscillatory responses only occur for pitch. Both responses occur in primary auditory cortex and adjacent nonprimary areas. The research suggests that two types of pitch-related activity occur in humans in early auditory cortex: time-locked neural correlates of stimulus regularity and an oscillatory response related to the pitch percept.

[1]  Karl J. Friston,et al.  Cortical circuits for perceptual inference , 2009, Neural Networks.

[2]  Birger Kollmeier,et al.  Dichotic pitch activates pitch processing centre in Heschl's gyrus , 2009, NeuroImage.

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

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

[5]  B Lütkenhöner,et al.  Neuromagnetic evidence for a pitch processing center in Heschl's gyrus. , 2003, Cerebral cortex.

[6]  Alain de Cheveigné,et al.  Pitch perception models , 2005 .

[7]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[8]  Mitchell Steinschneider,et al.  Spectrotemporal analysis of evoked and induced electroencephalographic responses in primary auditory cortex (A1) of the awake monkey. , 2008, Cerebral cortex.

[9]  D. M. Green,et al.  A panoramic code for sound location by cortical neurons. , 1994, Science.

[10]  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.

[11]  Matthias M. Müller,et al.  Human Gamma Band Activity and Perception of a Gestalt , 1999, The Journal of Neuroscience.

[12]  O. Bertrand,et al.  Oscillatory gamma activity in humans and its role in object representation , 1999, Trends in Cognitive Sciences.

[13]  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.

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

[15]  Joachim Gross,et al.  Gamma Oscillations in Human Primary Somatosensory Cortex Reflect Pain Perception , 2007, PLoS biology.

[16]  B. Gordon,et al.  Induced electrocorticographic gamma activity during auditory perception. Brazier Award-winning article, 2001. , 2001, Clinical neurophysiology : official journal of the International Federation of Clinical Neurophysiology.

[17]  Rajesh P. N. Rao,et al.  Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. , 1999 .

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

[19]  Ernst Mach,et al.  Sensations of tone. , 1897 .

[20]  M. Howard,et al.  A hybrid clinical-research depth electrode for acute and chronic in vivo microelectrode recording of human brain neurons. Technical note. , 1996, Journal of neurosurgery.

[21]  D. Hall,et al.  Pitch Processing Sites in the Human Auditory Brain , 2008, Cerebral cortex.

[22]  Nikos K Logothetis,et al.  Decoding a bistable percept with integrated time-frequency representation of single-trial local field potential. , 2008, Journal of neural engineering.

[23]  N. Logothetis,et al.  Phase-of-Firing Coding of Natural Visual Stimuli in Primary Visual Cortex , 2008, Current Biology.

[24]  T. Hackett,et al.  Organization and Correspondence of the Auditory Cortex of Humans and Nonhuman Primates , 2007 .

[25]  S. Shamma.  On the Emergence and Awareness of Auditory Objects , 2008, PLoS biology.

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

[27]  I. Fried,et al.  Coupling Between Neuronal Firing, Field Potentials, and fMRI in Human Auditory Cortex , 2005, Science.

[28]  Karl J. Friston,et al.  Auditory Object Analysis , 2012 .

[29]  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.

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

[31]  B. Gordon,et al.  Induced electrocorticographic gamma activity during auditory perception , 2001, Clinical Neurophysiology.

[32]  A. Pérez-Villalba.  Rhythms of the Brain, G. Buzsáki. Oxford University Press, Madison Avenue, New York (2006), Price: GB £42.00, p. 448, ISBN: 0-19-530106-4 , 2008 .

[33]  Lee M. Miller,et al.  Populations of auditory cortical neurons can accurately encode acoustic space across stimulus intensity , 2009, Proceedings of the National Academy of Sciences.

[34]  R. Patterson,et al.  The lower limit of melodic pitch. , 2001, The Journal of the Acoustical Society of America.