A brain basis for musical hallucinations☆

The physiological basis for musical hallucinations (MH) is not understood. One obstacle to understanding has been the lack of a method to manipulate the intensity of hallucination during the course of experiment. Residual inhibition, transient suppression of a phantom percept after the offset of a masking stimulus, has been used in the study of tinnitus. We report here a human subject whose MH were residually inhibited by short periods of music. Magnetoencephalography (MEG) allowed us to examine variation in the underlying oscillatory brain activity in different states. Source-space analysis capable of single-subject inference defined left-lateralised power increases, associated with stronger hallucinations, in the gamma band in left anterior superior temporal gyrus, and in the beta band in motor cortex and posteromedial cortex. The data indicate that these areas form a crucial network in the generation of MH, and are consistent with a model in which MH are generated by persistent reciprocal communication in a predictive coding hierarchy.

[1]  Werner Lutzenberger,et al.  Gamma-band activity over early sensory areas predicts detection of changes in audiovisual speech stimuli , 2006, NeuroImage.

[2]  V. Menon,et al.  Musical rhythm spectra from Bach to Joplin obey a 1/f power law , 2012, Proceedings of the National Academy of Sciences.

[3]  J. Blom,et al.  [Musical hallucinations]. , 2009, Nederlands tijdschrift voor geneeskunde.

[4]  A. Borst Seeing smells: imaging olfactory learning in bees , 1999, Nature Neuroscience.

[5]  Luis-Manuel Garcia On and On: Repetition as Process and Pleasure in Electronic Dance Music , 2005 .

[6]  J. Kaltenbach Tinnitus: Models and mechanisms , 2011, Hearing Research.

[7]  M. Keshavan,et al.  Musical hallucinations and musical imagery: prevalence and phenomenology in schizophrenic inpatients. , 1997, Psychopathology.

[8]  Raymond J. Dolan,et al.  Dynamic causal models of steady-state responses , 2009, NeuroImage.

[9]  M. Congedo,et al.  Tinnitus Intensity Dependent Gamma Oscillations of the Contralateral Auditory Cortex , 2009, PloS one.

[10]  Gareth R. Barnes,et al.  Gamma band pitch responses in human auditory cortex measured with magnetoencephalography , 2012, NeuroImage.

[11]  Karl J. Friston,et al.  Attention, Uncertainty, and Free-Energy , 2010, Front. Hum. Neurosci..

[12]  Karl J. Friston,et al.  Canonical Microcircuits for Predictive Coding , 2012, Neuron.

[13]  M. Cunningham,et al.  Do cortical gamma oscillations promote or suppress perception? An under-asked question with an over-assumed answer , 2013, Front. Hum. Neurosci..

[14]  M. S. Keshner 1/f noise , 1982, Proceedings of the IEEE.

[15]  G. Schott,et al.  Musical hallucinations in a musician , 2006, Journal of Neurology.

[16]  D. Robertson,et al.  Progressive centralization of midbrain hyperactivity after acoustic trauma , 2011, Neuroscience.

[17]  R. Zatorre,et al.  Listening to musical rhythms recruits motor regions of the brain. , 2008, Cerebral cortex.

[18]  Seung-Schik Yoo,et al.  Human brain mapping of auditory imagery: event-related functional MRI study , 2001, Neuroreport.

[19]  Peter R. Johnson Dichotically-Stimulated Ear Differences in Musicians and Nonmusicians , 1977, Cortex.

[20]  David Mumford,et al.  On the computational architecture of the neocortex , 2004, Biological Cybernetics.

[21]  Clyde Witchard Residual Inhibition , 2013 .

[22]  Christopher K. Kovach,et al.  Temporal Envelope of Time-Compressed Speech Represented in the Human Auditory Cortex , 2009, The Journal of Neuroscience.

[23]  A. Norena An integrative model of tinnitus based on a central gain controlling neural sensitivity , 2011, Neuroscience & Biobehavioral Reviews.

[24]  Desynchronization in the right auditory cortex during musical hallucinations: A MEG study , 2003 .

[25]  D. De Ridder,et al.  Disentangling Depression and Distress Networks in the Tinnitus Brain , 2012, PloS one.

[26]  D. Baguley,et al.  Is musical hallucination an otological phenomenon? a review of the literature , 2009, Clinical otolaryngology : official journal of ENT-UK ; official journal of Netherlands Society for Oto-Rhino-Laryngology & Cervico-Facial Surgery.

[27]  S. Petersen,et al.  Functional Anatomic Studies of Memory Retrieval for Auditory Words and Visual Pictures , 1996, The Journal of Neuroscience.

[28]  Doris-Eva Bamiou,et al.  Single-subject oscillatory gamma responses in tinnitus , 2012, Brain : a journal of neurology.

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

[30]  K. Kasai,et al.  Evidence for functional abnormality in the right auditory cortex during musical hallucinations , 1999, The Lancet.

[31]  R. Oostenveld,et al.  Reduced Occipital Alpha Power Indexes Enhanced Excitability Rather than Improved Visual Perception , 2013, The Journal of Neuroscience.

[32]  G. Turrigiano The Self-Tuning Neuron: Synaptic Scaling of Excitatory Synapses , 2008, Cell.

[33]  Aniruddh D. Patel,et al.  Top‐Down Control of Rhythm Perception Modulates Early Auditory Responses , 2009, Annals of the New York Academy of Sciences.

[34]  H. Feldmann Homolateral and contralateral masking of tinnitus. , 1981, The Journal of laryngology and otology. Supplement.

[35]  N. Weisz,et al.  Transient reduction of tinnitus intensity is marked by concomitant reductions of delta band power , 2008, BMC Biology.

[36]  A Thron,et al.  Playing piano in the mind--an fMRI study on music imagery and performance in pianists. , 2004, Brain research. Cognitive brain research.

[37]  Karl J. Friston The free-energy principle: a unified brain theory? , 2010, Nature Reviews Neuroscience.

[38]  M. Keshavan,et al.  Musical hallucinations: A review and synthesis. , 1992 .

[39]  G. Schlaug,et al.  In vivo evidence of structural brain asymmetry in musicians , 1995, Science.

[40]  Evan Balaban,et al.  β- And γ-band EEG power predicts illusory auditory continuity perception. , 2012, Journal of neurophysiology.

[41]  Stefan Koelsch,et al.  The Role of Harmonic Expectancy Violations in Musical Emotions: Evidence from Subjective, Physiological, and Neural Responses , 2006, Journal of Cognitive Neuroscience.

[42]  Joshua B. Mailman,et al.  Repetition in Music: Theoretical and Metatheoretical Perspectives , 2007 .

[43]  P. Janata The Neural Architecture of Music-Evoked Autobiographical Memories , 2009, Cerebral cortex.

[44]  R. Voss,et al.  ‘1/fnoise’ in music and speech , 1975, Nature.

[45]  T. Griffiths,et al.  Musical hallucinosis in acquired deafness. Phenomenology and brain substrate. , 2000, Brain : a journal of neurology.

[46]  Karl J. Friston,et al.  Free Energy, Precision and Learning: The Role of Cholinergic Neuromodulation , 2013, The Journal of Neuroscience.

[47]  Shinsuke Shimojo,et al.  Sound-induced illusory flash perception: role of gamma band responses , 2002, Neuroreport.

[48]  Angela J. Yu,et al.  Uncertainty, Neuromodulation, and Attention , 2005, Neuron.

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

[50]  K. Shinosaki,et al.  Evaluation of regional cerebral blood flow in a patient with musical hallucinations , 2010, Neurocase.

[51]  Werner Lutzenberger,et al.  Magnetoencephalographic gamma-band responses to illusory triangles in humans , 2004, NeuroImage.

[52]  A. Caramazza,et al.  Brain Regions That Represent Amodal Conceptual Knowledge , 2013, The Journal of Neuroscience.

[53]  S. M. Daselaar,et al.  Explaining the encoding/retrieval flip: Memory-related deactivations and activations in the posteromedial cortex , 2012, Neuropsychologia.

[54]  T. Elbert,et al.  Neuromagnetic indicators of auditory cortical reorganization of tinnitus. , 2005, Brain : a journal of neurology.

[55]  Lassi A. Liikkanen Musical activities predispose to involuntary musical imagery , 2012 .

[56]  J. Kaltenbach,et al.  Comparison and contrast of noise-induced hyperactivity in the dorsal cochlear nucleus and inferior colliculus , 2013, Hearing Research.

[57]  M. Imaizumi,et al.  Neural mechanism of residual inhibition of tinnitus in cochlear implant users , 2005, Neuroreport.

[58]  R. Zatorre,et al.  When that tune runs through your head: a PET investigation of auditory imagery for familiar melodies. , 1999, Cerebral cortex.

[59]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[60]  Lassi A. Liikkanen Music in Everymind: Commonality of Involuntary Musical Imagery , 2008 .

[61]  Roy D. Patterson,et al.  Direct Recordings of Pitch Responses from Human Auditory Cortex , 2010, Current Biology.

[62]  S. Evers,et al.  The clinical spectrum of musical hallucinations , 2004, Journal of the Neurological Sciences.

[63]  Eleanor A. Maguire,et al.  Retrosplenial Cortex Codes for Permanent Landmarks , 2012, PloS one.

[64]  Daren Zhang,et al.  Early induced beta/gamma activity during illusory contour perception , 2009, Neuroscience Letters.

[65]  C Philip Beaman,et al.  Earworms (stuck song syndrome): towards a natural history of intrusive thoughts. , 2010, British journal of psychology.

[66]  Jae-Jin Song,et al.  Tinnitus and musical hallucinosis: The same but more , 2013, NeuroImage.

[67]  G. Berríos Musical Hallucinations , 1990, British Journal of Psychiatry.

[68]  Richard S. J. Frackowiak,et al.  Analysis of temporal structure in sound by the human brain , 1998, Nature Neuroscience.

[69]  T. Bever,et al.  Cerebral Dominance in Musicians and Nonmusicians , 1974, Science.

[70]  Roy D. Patterson,et al.  Predictive Coding and Pitch Processing in the Auditory Cortex , 2011, Journal of Cognitive Neuroscience.

[71]  Gary G. R. Green,et al.  Representations of the temporal envelope of sounds in human auditory cortex: Can the results from invasive intracortical “depth” electrode recordings be replicated using non-invasive MEG “virtual electrodes”? , 2013, NeuroImage.

[72]  W. Drongelen,et al.  Localization of brain electrical activity via linearly constrained minimum variance spatial filtering , 1997, IEEE Transactions on Biomedical Engineering.

[73]  Jens Haueisen,et al.  Involuntary Motor Activity in Pianists Evoked by Music Perception , 2001, Journal of Cognitive Neuroscience.

[74]  K. Diederen,et al.  Healthy individuals with auditory verbal hallucinations; who are they? Psychiatric assessments of a selected sample of 103 subjects. , 2010, Schizophrenia bulletin.

[75]  D. Robertson,et al.  Hyperactivity in the auditory midbrain after acoustic trauma: dependence on cochlear activity , 2009, Neuroscience.

[76]  Xiao-Jing Wang Neurophysiological and computational principles of cortical rhythms in cognition. , 2010, Physiological reviews.

[77]  Karl J. Friston,et al.  Dynamic causal modelling of induced responses , 2008, NeuroImage.

[78]  Diana Deutsch,et al.  Illusory transformation from speech to song. , 2011, The Journal of the Acoustical Society of America.

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

[80]  T. Bever,et al.  Cerebral dominance in musicians and nonmusicians. 1974. , 2009, The Journal of neuropsychiatry and clinical neurosciences.

[81]  F. Bailes The prevalence and nature of imagined music in the everyday lives of music students , 2007 .

[82]  R. Desimone,et al.  The Effects of Visual Stimulation and Selective Visual Attention on Rhythmic Neuronal Synchronization in Macaque Area V4 , 2008, The Journal of Neuroscience.

[83]  David J. M. Kraemer,et al.  Musical imagery: Sound of silence activates auditory cortex , 2005, Nature.

[84]  E. Brattico,et al.  Music and Emotions in the Brain: Familiarity Matters , 2011, PloS one.

[85]  E. Perry,et al.  Why people see things that are not there: A novel Perception and Attention Deficit model for recurrent complex visual hallucinations , 2005, Behavioral and Brain Sciences.

[86]  Paul Iverson,et al.  Name that tune: Identifying popular recordings from brief excerpts , 1999, Psychonomic bulletin & review.

[87]  Luc H. Arnal,et al.  Transitions in neural oscillations reflect prediction errors generated in audiovisual speech , 2011, Nature Neuroscience.

[88]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[89]  T. Ohnishi,et al.  Functional anatomy of musical perception in musicians , 2001, NeuroImage.