You can't stop the music: Reduced auditory alpha power and coupling between auditory and memory regions facilitate the illusory perception of music during noise

Our brain has the capacity of providing an experience of hearing even in the absence of auditory stimulation. This can be seen as illusory conscious perception. While increasing evidence postulates that conscious perception requires specific brain states that systematically relate to specific patterns of oscillatory activity, the relationship between auditory illusions and oscillatory activity remains mostly unexplained. To investigate this we recorded brain activity with magnetoencephalography and collected intracranial data from epilepsy patients while participants listened to familiar as well as unknown music that was partly replaced by sections of pink noise. We hypothesized that participants have a stronger experience of hearing music throughout noise when the noise sections are embedded in familiar compared to unfamiliar music. This was supported by the behavioral results showing that participants rated the perception of music during noise as stronger when noise was presented in a familiar context. Time-frequency data show that the illusory perception of music is associated with a decrease in auditory alpha power pointing to increased auditory cortex excitability. Furthermore, the right auditory cortex is concurrently synchronized with the medial temporal lobe, putatively mediating memory aspects associated with the music illusion. We thus assume that neuronal activity in the highly excitable auditory cortex is shaped through extensive communication between the auditory cortex and the medial temporal lobe, thereby generating the illusion of hearing music during noise.

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

[2]  John P. Aggleton,et al.  Interleaving brain systems for episodic and recognition memory , 2006, Trends in Cognitive Sciences.

[3]  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 .

[4]  Ana Navarro Cebrián,et al.  Electrophysiological correlates of accurate mental image formation in auditory perception and imagery tasks , 2010, Brain Research.

[5]  M. Kahana,et al.  Human hippocampal theta oscillations and the formation of episodic memories , 2012, Hippocampus.

[6]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

[7]  W. Klimesch,et al.  Theta synchronization during episodic retrieval: neural correlates of conscious awareness. , 2001, Brain research. Cognitive brain research.

[8]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[9]  Simon Hanslmayr,et al.  Prestimulus oscillations predict visual perception performance between and within subjects , 2007, NeuroImage.

[10]  Matthew Flatt,et al.  PsyScope: An interactive graphic system for designing and controlling experiments in the psychology laboratory using Macintosh computers , 1993 .

[11]  W. Penny,et al.  Theta-Coupled Periodic Replay in Working Memory , 2010, Current Biology.

[12]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[13]  Á. Pascual-Leone,et al.  α-Band Electroencephalographic Activity over Occipital Cortex Indexes Visuospatial Attention Bias and Predicts Visual Target Detection , 2006, The Journal of Neuroscience.

[14]  J Gross,et al.  REPRINTS , 1962, The Lancet.

[15]  Alan C. Evans,et al.  Hearing in the Mind's Ear: A PET Investigation of Musical Imagery and Perception , 1996, Journal of Cognitive Neuroscience.

[16]  W. Singer,et al.  Modulation of Neuronal Interactions Through Neuronal Synchronization , 2007, Science.

[17]  K. O’Connor,et al.  Encoding of Illusory Continuity in Primary Auditory Cortex , 2007, Neuron.

[18]  W. Klimesch,et al.  EEG alpha oscillations: The inhibition–timing hypothesis , 2007, Brain Research Reviews.

[19]  Jonas Obleser,et al.  Alpha Rhythms in Audition: Cognitive and Clinical Perspectives , 2011, Front. Psychology.

[20]  Thomas Elbert,et al.  Tinnitus Perception and Distress Is Related to Abnormal Spontaneous Brain Activity as Measured by Magnetoencephalography , 2005, PLoS medicine.

[21]  Niels Birbaumer,et al.  Cross-frequency phase synchronization: A brain mechanism of memory matching and attention , 2008, NeuroImage.

[22]  Christo Pantev,et al.  Imagery Mismatch Negativity in Musicians , 2009, Annals of the New York Academy of Sciences.

[23]  Ingrid S. Johnsrude,et al.  Illusory Vowels Resulting from Perceptual Continuity: A Functional Magnetic Resonance Imaging Study , 2008, Journal of Cognitive Neuroscience.

[24]  O. Jensen,et al.  Shaping Functional Architecture by Oscillatory Alpha Activity: Gating by Inhibition , 2010, Front. Hum. Neurosci..

[25]  R M Leahy,et al.  A sensor-weighted overlapping-sphere head model and exhaustive head model comparison for MEG. , 1999, Physics in medicine and biology.

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

[27]  P. Fries A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[28]  N. Weisz,et al.  rTMS Induced Tinnitus Relief Is Related to an Increase in Auditory Cortical Alpha Activity , 2013, PloS one.

[29]  Timothy L Hubbard,et al.  Auditory imagery: empirical findings. , 2010, Psychological bulletin.

[30]  A. Walden,et al.  Spectral analysis for physical applications : multitaper and conventional univariate techniques , 1996 .

[31]  Wolf Singer,et al.  Neuronal Synchrony: A Versatile Code for the Definition of Relations? , 1999, Neuron.

[32]  Takamitsu Watanabe,et al.  Memory of music: Roles of right hippocampus and left inferior frontal gyrus , 2008, NeuroImage.

[33]  T. Elbert,et al.  The relevance of spontaneous activity for the coding of the tinnitus sensation. , 2007, Progress in brain research.

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

[35]  F. Varela,et al.  Measuring phase synchrony in brain signals , 1999, Human brain mapping.

[36]  B. Staresina,et al.  Perirhinal and Parahippocampal Cortices Differentially Contribute to Later Recollection of Object- and Scene-Related Event Details , 2011, The Journal of Neuroscience.

[37]  C. Schroeder,et al.  Low-frequency neuronal oscillations as instruments of sensory selection , 2009, Trends in Neurosciences.

[38]  R. Zatorre,et al.  Effect of unilateral temporal-lobe excision on perception and imagery of songs , 1993, Neuropsychologia.

[39]  D. Kovalev,et al.  Rapid and fully automated visualization of subdural electrodes in the presurgical evaluation of epilepsy patients. , 2005, AJNR. American journal of neuroradiology.

[40]  G. Buzsáki Rhythms of the brain , 2006 .

[41]  A. Halpern,et al.  Cerebral Substrates of Musical Imagery , 2001, Annals of the New York Academy of Sciences.

[42]  P. Janata Brain Networks That Track Musical Structure , 2005, Annals of the New York Academy of Sciences.

[43]  Isabelle Peretz,et al.  Morphometry of the amusic brain: a two-site study. , 2006, Brain : a journal of neurology.

[44]  J. Karhu,et al.  Theta oscillations index human hippocampal activation during a working memory task. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[45]  Riitta Hari,et al.  Mind's Ear in a Musician: Where and When in the Brain , 2002, NeuroImage.

[46]  Rutger Goekoop,et al.  Deactivation of the parahippocampal gyrus preceding auditory hallucinations in schizophrenia. , 2010, The American journal of psychiatry.

[47]  Ole Jensen,et al.  Reading the hippocampal code by theta phase-locking , 2005, Trends in Cognitive Sciences.

[48]  Robert J. Zatorre,et al.  Mental Concerts: Musical Imagery and Auditory Cortex , 2005, Neuron.

[49]  Nathan Weisz,et al.  Lateralized auditory cortical alpha band activity and interregional connectivity pattern reflect anticipation of target sounds. , 2012, Cerebral cortex.

[50]  J. Gross,et al.  On the Role of Prestimulus Alpha Rhythms over Occipito-Parietal Areas in Visual Input Regulation: Correlation or Causation? , 2010, The Journal of Neuroscience.

[51]  Carmena Jose,et al.  Oscillatory phase coupling coordinates anatomically-dispersed functional cell assemblies , 2011 .

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

[53]  Renaud Jardri,et al.  Cortical activations during auditory verbal hallucinations in schizophrenia: a coordinate-based meta-analysis. , 2011, The American journal of psychiatry.

[54]  J. Rauschecker,et al.  Brain Activation during Anticipation of Sound Sequences , 2009, The Journal of Neuroscience.

[55]  V. Calhoun,et al.  An Update on Neurocognitive Impairment in Schizophrenia and Depression , 2010, Frontiers in human neuroscience.

[56]  M. Bar,et al.  Cortical Analysis of Visual Context , 2003, Neuron.

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

[58]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[59]  Riitta Salmelin,et al.  Evidence for reactive magnetic 10-Hz rhythm in the human auditory cortex , 1997, Neuroscience Letters.