Selective Subcortical Enhancement of Musical Intervals in Musicians

By measuring the auditory brainstem response to two musical intervals, the major sixth (E3 and G2) and the minor seventh (E3 and F#2), we found that musicians have a more specialized sensory system for processing behaviorally relevant aspects of sound. Musicians had heightened responses to the harmonics of the upper tone (E), as well as certain combination tones (sum tones) generated by nonlinear processing in the auditory system. In music, the upper note is typically carried by the upper voice, and the enhancement of the upper tone likely reflects musicians' extensive experience attending to the upper voice. Neural phase locking to the temporal periodicity of the amplitude-modulated envelope, which underlies the perception of musical harmony, was also more precise in musicians than nonmusicians. Neural enhancements were strongly correlated with years of musical training, and our findings, therefore, underscore the role that long-term experience with music plays in shaping auditory sensory encoding.

[1]  R. Eckhorn,et al.  Stimulus-dependent modulations of correlated high-frequency oscillations in cat visual cortex. , 1997, Cerebral cortex.

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

[3]  D O Kim,et al.  Cochlear mechanics: nonlinear behavior in two-tone responses as reflected in cochlear-nerve-fiber responses and in ear-canal sound pressure. , 1980, The Journal of the Acoustical Society of America.

[4]  S. H. Hulse,et al.  Auditory discrimination of chord-based spectral structures by European starlings ( Sturnus vulgaris ) , 1995 .

[5]  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.

[6]  F. de Ribaupierre,et al.  Phase-locked responses to low frequency tones in the medial geniculate body , 1979, Hearing Research.

[7]  M. Sams,et al.  Musicians have enhanced subcortical auditory and audiovisual processing of speech and music , 2007, Proceedings of the National Academy of Sciences.

[8]  J. Hall Auditory brainstem frequency following responses to waveform envelope periodicity. , 1979, Science.

[9]  S. Kuriki,et al.  Effects of Musical Experience on Different Components of MEG Responses Elicited by Sequential Piano-Tones and Chords , 2006, The Journal of Neuroscience.

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

[11]  Nobuo Suga,et al.  Plasticity and Corticofugal Modulation for Hearing in Adult Animals , 2002, Neuron.

[12]  J. Kaas,et al.  Tonotopic organization, architectonic fields, and connections of auditory cortex in macaque monkeys , 1993, The Journal of comparative neurology.

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

[14]  J. T. Marsh,et al.  Frequency-following (microphonic-like) neural responses evoked by sound. , 1968, Electroencephalography and clinical neurophysiology.

[15]  G Moushegian,et al.  Laboratory note. Scalp-recorded early responses in man to frequencies in the speech range. , 1973, Electroencephalography and clinical neurophysiology.

[16]  J. Rothwell,et al.  Motorcortical Excitability and Synaptic Plasticity Is Enhanced in Professional Musicians , 2007, The Journal of Neuroscience.

[17]  G. Schlaug,et al.  Brain Structures Differ between Musicians and Non-Musicians , 2003, The Journal of Neuroscience.

[18]  I. Peretz,et al.  Brain organization for music processing. , 2005, Annual review of psychology.

[19]  George Moushegian,et al.  Laboratory noteScalp-recorded early responses in man to frequencies in the speech rangeReponses precoces enregistrees sur le scalp chez l'homme a des frequences dans la gamme du langage , 1973 .

[20]  D. Kemp,et al.  Otoacoustic emissions, their origin in cochlear function, and use. , 2002, British medical bulletin.

[21]  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.

[22]  E. Knudsen Fundamental components of attention. , 2007, Annual review of neuroscience.

[23]  G C Galbraith,et al.  Two-channel brain-stem frequency-following responses to pure tone and missing fundamental stimuli. , 1994, Electroencephalography and clinical neurophysiology.

[24]  D. McAlpine Neural sensitivity to periodicity in the inferior colliculus: evidence for the role of cochlear distortions. , 2004, Journal of neurophysiology.

[25]  R. Goldstein,et al.  Auditory distortion products measured with averaged auditory evoked potentials. , 1992, Journal of speech and hearing research.

[26]  E. W. Large,et al.  A GENERIC NONLINEAR MODEL FOR AUDITORY PERCEPTION , 2006 .

[27]  S. S. Stevens,et al.  Critical Band Width in Loudness Summation , 1957 .

[28]  J. Eggermont,et al.  What's to lose and what's to learn: Development under auditory deprivation, cochlear implants and limits of cortical plasticity , 2007, Brain Research Reviews.

[29]  L. M. Kitzes,et al.  Intrinsic inter- and intralaminar connections and their relationship to the tonotopic map in cat primary auditory cortex , 2004, Experimental Brain Research.

[30]  Antoine J. Shahin,et al.  Enhancement of Neuroplastic P2 and N1c Auditory Evoked Potentials in Musicians , 2003, The Journal of Neuroscience.

[31]  A. Krishnan,et al.  Comparison of the acoustic and neural distortion product at 2f1-f2 in normal-hearing adults , 2008, International journal of audiology.

[32]  B. Delgutte,et al.  Neurobiological Foundations for the Theory of Harmony in Western Tonal Music , 2001, Annals of the New York Academy of Sciences.

[33]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. I. Alpha and beta event-related desynchronization. , 1998, Brain : a journal of neurology.

[34]  R. Plomp,et al.  Tonal consonance and critical bandwidth. , 1965, The Journal of the Acoustical Society of America.

[35]  D T Kemp,et al.  Indications of different distortion product otoacoustic emission mechanisms from a detailed f1,f2 area study. , 2000, The Journal of the Acoustical Society of America.

[36]  Antoine J. Shahin,et al.  Effects of Musical Training on the Auditory Cortex in Children , 2003, Annals of the New York Academy of Sciences.

[37]  I. Peretz,et al.  Contribution of different cortical areas in the temporal lobes to music processing. , 1998, Brain : a journal of neurology.

[38]  H J Steeneken,et al.  Interference between two simple tones. , 1968, The Journal of the Acoustical Society of America.

[39]  Alan C. Evans,et al.  Emotional responses to pleasant and unpleasant music correlate with activity in paralimbic brain regions , 1999, Nature Neuroscience.

[40]  J. E. Hind,et al.  Auditory cortex on the human posterior superior temporal gyrus , 2000, The Journal of comparative neurology.

[41]  C. Schroeder,et al.  Speech-evoked activity in primary auditory cortex: effects of voice onset time. , 1994, Electroencephalography and clinical neurophysiology.

[42]  W Goebl,et al.  Melody lead in piano performance: expressive device or artifact? , 2001, The Journal of the Acoustical Society of America.

[43]  Sibylle C. Herholz,et al.  Cortical Plasticity Induced by Short-Term Unimodal and Multimodal Musical Training , 2008, The Journal of Neuroscience.

[44]  E. Terhardt Psychoacoustic evaluation of musical sounds , 1978, Perception & psychophysics.

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

[46]  L. Hood,et al.  Clinical Applications of the Auditory Brainstem Response , 1998 .

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

[48]  K E Hecox,et al.  Auditory nonlinearities measured with auditory-evoked potentials. , 1990, The Journal of the Acoustical Society of America.

[49]  P. Cariani,et al.  Encoding of pitch in the human brainstem is sensitive to language experience. , 2005, Brain research. Cognitive brain research.

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

[51]  N. Kraus,et al.  Exploring the relationship between physiological measures of cochlear and brainstem function , 2009, Clinical Neurophysiology.

[52]  N. Kraus,et al.  The scalp-recorded brainstem response to speech: neural origins and plasticity. , 2010, Psychophysiology.

[53]  J. Winer Decoding the auditory corticofugal systems , 2005, Hearing Research.

[54]  J. Saffran,et al.  The Infant's Auditory World: Hearing, Speech, and the Beginnings of Language , 2007 .

[55]  D T Kemp,et al.  Wave and place fixed DPOAE maps of the human ear. , 2001, The Journal of the Acoustical Society of America.

[56]  J. Fritz,et al.  Adaptive changes in cortical receptive fields induced by attention to complex sounds. , 2007, Journal of neurophysiology.

[57]  Isabelle Peretz,et al.  Functional dissociations following bilateral lesions of auditory cortex. , 1994 .

[58]  M. N. Wallace,et al.  Chemoarchitectonic organization of the cat primary auditory cortex , 2004, Experimental Brain Research.

[59]  A. Kameoka,et al.  Consonance theory part II: consonance of complex tones and its calculation method. , 1969, The Journal of the Acoustical Society of America.

[60]  Jun Yan,et al.  Corticofugal Modulation of Initial Sound Processing in the Brain , 2008, The Journal of Neuroscience.

[61]  G. Long,et al.  The effect of stimulus-frequency ratio on distortion product otoacoustic emission components. , 2005, The Journal of the Acoustical Society of America.

[62]  A Lewis,et al.  THE SCIENCE OF SOUND , 1997 .

[63]  Guido F. Smoorenburg,et al.  Combination Tones and Their Origin , 1972 .

[64]  C. Nicholson,et al.  Experimental optimization of current source-density technique for anuran cerebellum. , 1975, Journal of neurophysiology.

[65]  Terence W. Picton,et al.  Envelope and spectral frequency-following responses to vowel sounds , 2008, Hearing Research.

[66]  C. Palmer Music performance. , 1997, Annual review of psychology.

[67]  Shawn A. Weil,et al.  Change detection in multi-voice music: the role of musical structure, musical training, and task demands. , 2002, Journal of experimental psychology. Human perception and performance.

[68]  E. Rouiller,et al.  Auditory corticocortical interconnections in the cat: evidence for parallel and hierarchical arrangement of the auditory cortical areas , 2004, Experimental Brain Research.

[69]  Nicole M. Russo,et al.  Musical experience shapes human brainstem encoding of linguistic pitch patterns , 2007, Nature Neuroscience.

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

[71]  B. Delgutte,et al.  Neural correlates of the pitch of complex tones. II. Pitch shift, pitch ambiguity, phase invariance, pitch circularity, rate pitch, and the dominance region for pitch. , 1996, Journal of neurophysiology.

[72]  Paul J. Abbas,et al.  A chronic microelectrode investigation of the tonotopic organization of human auditory cortex , 1996, Brain Research.

[73]  Patrick C M Wong,et al.  Selective neurophysiologic responses to music in instrumentalists with different listening biographies , 2009, Human brain mapping.

[74]  P. Pandya,et al.  Human frequency-following response correlates of the distortion product at 2F1-F2. , 2004, Journal of the American Academy of Audiology.

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

[76]  N. Kraus,et al.  Reading and subcortical auditory function. , 2009, Cerebral cortex.

[77]  R. Eckhorn,et al.  High frequency (60-90 Hz) oscillations in primary visual cortex of awake monkey. , 1993, Neuroreport.

[78]  J. L. Goldstein Auditory nonlinearity. , 1967, The Journal of the Acoustical Society of America.

[79]  M Steinschneider,et al.  Complex tone processing in primary auditory cortex of the awake monkey. II. Pitch versus critical band representation. , 2000, The Journal of the Acoustical Society of America.

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

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

[82]  E. Rouiller,et al.  Neurons sensitive to narrow ranges of repetitive acoustic transients in the medial geniculate body of the cat , 2004, Experimental Brain Research.

[83]  C Palmer,et al.  Harmonic, melodic, and frequency height influences in the perception of multivoiced music , 1994, Perception & psychophysics.

[84]  N. Kraus,et al.  Musical experience and neural efficiency – effects of training on subcortical processing of vocal expressions of emotion , 2009, The European journal of neuroscience.

[85]  A. Krishnan,et al.  Human Frequency-Following Responses to Two-Tone Approximations of Steady-State Vowels , 1999, Audiology and Neurotology.

[86]  Erika Skoe,et al.  Experience‐induced Malleability in Neural Encoding of Pitch, Timbre, and Timing , 2009, Annals of the New York Academy of Sciences.

[87]  J. T. Marsh,et al.  Far-field recorded frequency-following responses: evidence for the locus of brainstem sources. , 1975, Electroencephalography and clinical neurophysiology.

[88]  N. Mizuno,et al.  Morphology and laminar organization of electrophysiologically identified neurons in the primary auditory cortex in the cat , 1985, The Journal of comparative neurology.

[89]  B. Ross,et al.  COGNITIVE NEUROSCIENCE AND NEUROPSYCHOLOGY: Timbre-specific enhancement of auditory cortical representations in musicians , 2022 .

[90]  D. Kemp,et al.  Relationships between DPOAE and TEOAE amplitude and phase characteristics , 1999 .

[91]  M Steinschneider,et al.  Temporal encoding of the voice onset time phonetic parameter by field potentials recorded directly from human auditory cortex. , 1999, Journal of neurophysiology.

[92]  J. Saffran,et al.  Musical Learning and Language Development , 2003, Annals of the New York Academy of Sciences.

[93]  M Steinschneider,et al.  Click train encoding in primary auditory cortex of the awake monkey: evidence for two mechanisms subserving pitch perception. , 1998, The Journal of the Acoustical Society of America.

[94]  D. Contreras,et al.  Synchronization of fast (30-40 Hz) spontaneous cortical rhythms during brain activation , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[95]  Laurel J. Trainor,et al.  Automatic Encoding of Polyphonic Melodies in Musicians and Nonmusicians , 2005, Journal of Cognitive Neuroscience.

[96]  J. Hohnsbein,et al.  The human frequency-following response (FFR): Normal variability and relation to the click-evoked brainstem response , 1992, Hearing Research.

[97]  W. Singer,et al.  Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[98]  J M Badier,et al.  Evoked potentials recorded from the auditory cortex in man: evaluation and topography of the middle latency components. , 1994, Electroencephalography and clinical neurophysiology.

[99]  William S. Rhode,et al.  Two-tone suppression and distortion production on the basilar membrane in the hook region of cat and guinea pig cochleae , 1993, Hearing Research.

[100]  Nobuo Suga,et al.  Multiparametric corticofugal modulation and plasticity in the auditory system , 2003, Nature Reviews Neuroscience.

[101]  C. Berlin,et al.  Olivocochlear efferent suppression in classical musicians. , 2003, Journal of the American Academy of Audiology.

[102]  J. Kaas,et al.  Subdivisions of auditory cortex and ipsilateral cortical connections of the parabelt auditory cortex in macaque monkeys , 1998, The Journal of comparative neurology.

[103]  B. Ross,et al.  Simultaneous pitches are encoded separately in auditory cortex: an MMNm study , 2008, Neuroreport.

[104]  N. Kraus,et al.  Relationships between behavior, brainstem and cortical encoding of seen and heard speech in musicians and non-musicians , 2008, Hearing Research.

[105]  C. Micheyl,et al.  Stronger bilateral efferent influences on cochlear biomechanical activity in musicians than in non-musicians , 1999, Neuroscience Letters.

[106]  Bernd Lütkenhöner,et al.  High-Precision Neuromagnetic Study of the Functional Organization of the Human Auditory Cortex , 1998, Audiology and Neurotology.

[107]  A. Galaburda,et al.  Cytoarchitectonic organization of the human auditory cortex , 1980, The Journal of comparative neurology.

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

[109]  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.

[110]  Christoph E. Schreiner,et al.  Auditory Cortex Mapmaking: Principles, Projections, and Plasticity , 2007, Neuron.

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

[112]  M Steinschneider,et al.  Complex tone processing in primary auditory cortex of the awake monkey. I. Neural ensemble correlates of roughness. , 2000, The Journal of the Acoustical Society of America.

[113]  Mario A. Ruggero,et al.  Two-tone distortion in the basilar membrane of the cochlea , 1991, Nature.

[114]  C. Schreiner,et al.  Periodicity coding in the inferior colliculus of the cat. I. Neuronal mechanisms. , 1988, Journal of neurophysiology.

[115]  K E Hecox,et al.  Electrophysiological evidence of nonlinear distortion products to two-tone stimuli. , 1991, The Journal of the Acoustical Society of America.

[116]  J. Bharucha,et al.  Music Perception and Cognition Following Bilateral Lesions of Auditory Cortex , 1990, Journal of Cognitive Neuroscience.

[117]  Nina Kraus,et al.  Brainstem responses to speech syllables , 2004, Clinical Neurophysiology.

[118]  B. Delgutte,et al.  Pitch representations in the auditory nerve: two concurrent complex tones. , 2008, Journal of neurophysiology.

[119]  I. Peretz,et al.  Cortical deafness to dissonance. , 2001, Brain : a journal of neurology.

[120]  G. V. Simpson,et al.  Cellular generators of the cortical auditory evoked potential initial component. , 1992, Electroencephalography and clinical neurophysiology.

[121]  E. G. Jones,et al.  Patterns of axon collateralization of identified supragranular pyramidal neurons in the cat auditory cortex. , 1991, Cerebral cortex.

[122]  Steven Greenberg,et al.  Neural temporal coding of low pitch. I. Human frequency-following responses to complex tones , 1987, Hearing Research.

[123]  L. Demany,et al.  The perceptual reality of tone chroma in early infancy , 1982 .