Neural Correlates of Auditory Figure-Ground Segregation Based on Temporal Coherence

To make sense of natural acoustic environments, listeners must parse complex mixtures of sounds that vary in frequency, space, and time. Emerging work suggests that, in addition to the well-studied spectral cues for segregation, sensitivity to temporal coherence—the coincidence of sound elements in and across time—is also critical for the perceptual organization of acoustic scenes. Here, we examine pre-attentive, stimulus-driven neural processes underlying auditory figure-ground segregation using stimuli that capture the challenges of listening in complex scenes where segregation cannot be achieved based on spectral cues alone. Signals (“stochastic figure-ground”: SFG) comprised a sequence of brief broadband chords containing random pure tone components that vary from 1 chord to another. Occasional tone repetitions across chords are perceived as “figures” popping out of a stochastic “ground.” Magnetoencephalography (MEG) measurement in naïve, distracted, human subjects revealed robust evoked responses, commencing from about 150 ms after figure onset that reflect the emergence of the “figure” from the randomly varying “ground.” Neural sources underlying this bottom-up driven figure-ground segregation were localized to planum temporale, and the intraparietal sulcus, demonstrating that this area, outside the “classic” auditory system, is also involved in the early stages of auditory scene analysis.”

[1]  D. Pandya,et al.  Cortico-cortical connections in the rhesus monkey. , 1969, Brain research.

[2]  P. Rakić,et al.  Heterogeneous afferents to the inferior parietal lobule of the rhesus monkey revealed by the retrograde transport method , 1977, Brain Research.

[3]  Dr. Juhani Hyvärinen The Parietal Cortex of Monkey and Man , 1982, Studies of Brain Function.

[4]  B. Moore,et al.  Suggested formulae for calculating auditory-filter bandwidths and excitation patterns. , 1983, The Journal of the Acoustical Society of America.

[5]  L. Christophorou,et al.  5 – From Basic Research to Application , 1984 .

[6]  D. Pandya,et al.  Projections to the frontal cortex from the posterior parietal region in the rhesus monkey , 1984, The Journal of comparative neurology.

[7]  E. G. Jones Cerebral Cortex , 1987, Cerebral Cortex.

[8]  B. Moore,et al.  Temporal window shape as a function of frequency and level. , 1989, The Journal of the Acoustical Society of America.

[9]  H S Colburn,et al.  Reducing informational masking by sound segregation. , 1994, The Journal of the Acoustical Society of America.

[10]  Discriminating coherence in spectro-temporal patterns. , 1995, The Journal of the Acoustical Society of America.

[11]  M. Hallett Human Brain Function , 1998, Trends in Neurosciences.

[12]  M. Goldberg,et al.  The representation of visual salience in monkey parietal cortex , 1998, Nature.

[13]  D. Poeppel,et al.  Latency of the auditory evoked neuromagnetic field components: stimulus dependence and insights toward perception. , 2000, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[14]  C. Koch,et al.  Computational modelling of visual attention , 2001, Nature Reviews Neuroscience.

[15]  Mitchell Steinschneider,et al.  Neural correlates of auditory stream segregation in primary auditory cortex of the awake monkey , 2001, Hearing Research.

[16]  G. Nolte The magnetic lead field theorem in the quasi-static approximation and its use for magnetoencephalography forward calculation in realistic volume conductors. , 2003, Physics in medicine and biology.

[17]  Karl J. Friston,et al.  Comparing dynamic causal models , 2004, NeuroImage.

[18]  R. Carlyon How the brain separates sounds , 2004, Trends in Cognitive Sciences.

[19]  J. Arezzo,et al.  Auditory stream segregation in monkey auditory cortex: effects of frequency separation, presentation rate, and tone duration. , 2004, The Journal of the Acoustical Society of America.

[20]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[21]  I. Nelken,et al.  Functional organization of ferret auditory cortex. , 2005, Cerebral cortex.

[22]  Rhodri Cusack,et al.  The Intraparietal Sulcus and Perceptual Organization , 2005, Journal of Cognitive Neuroscience.

[23]  A. Schleicher,et al.  Cytoarchitectonic identification and probabilistic mapping of two distinct areas within the anterior ventral bank of the human intraparietal sulcus , 2006, The Journal of comparative neurology.

[24]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[25]  R. Ilmoniemi,et al.  Interpreting magnetic fields of the brain: minimum norm estimates , 2006, Medical and Biological Engineering and Computing.

[26]  Andrew J Oxenham,et al.  Cortical FMRI activation to sequences of tones alternating in frequency: relationship to perceived rate and streaming. , 2007, Journal of neurophysiology.

[27]  M. Kenward,et al.  An Introduction to the Bootstrap , 2007 .

[28]  Andrew J Oxenham,et al.  Human Cortical Activity during Streaming without Spectral Cues Suggests a General Neural Substrate for Auditory Stream Segregation , 2007, The Journal of Neuroscience.

[29]  Karl J. Friston,et al.  Canonical Source Reconstruction for MEG , 2007, Comput. Intell. Neurosci..

[30]  J. Rauschecker,et al.  The role of auditory cortex in the formation of auditory streams , 2007, Hearing Research.

[31]  J. F. Kalaska,et al.  Attention in hierarchical models of object recognition , 2007 .

[32]  K. Amunts,et al.  Probabilistic maps, morphometry, and variability of cytoarchitectonic areas in the human superior parietal cortex. , 2008, Cerebral cortex.

[33]  A. Oxenham,et al.  Neural Correlates of Auditory Perceptual Awareness under Informational Masking , 2008, PLoS biology.

[34]  S. Shamma,et al.  Temporal Coherence in the Perceptual Organization and Cortical Representation of Auditory Scenes , 2009, Neuron.

[35]  S. Shamma,et al.  Interaction between Attention and Bottom-Up Saliency Mediates the Representation of Foreground and Background in an Auditory Scene , 2009, PLoS biology.

[36]  George R. Mangun,et al.  Anterior Intraparietal Sulcus is Sensitive to Bottom–Up Attention Driven by Stimulus Salience , 2009, Journal of Cognitive Neuroscience.

[37]  A. Gutschalk,et al.  Functional dissociation of transient and sustained fMRI BOLD components in human auditory cortex revealed with a streaming paradigm based on interaural time differences , 2010, The European journal of neuroscience.

[38]  S. David,et al.  Adaptive, behaviorally-gated, persistent encoding of task-relevant auditory information in ferret frontal cortex , 2010, Nature Neuroscience.

[39]  Mitchell Steinschneider,et al.  Formation of auditory streams , 2010 .

[40]  Alexander Gutschalk,et al.  Activity associated with stream segregation in human auditory cortex is similar for spatial and pitch cues. , 2010, Cerebral cortex.

[41]  S. Shamma,et al.  Behind the scenes of auditory perception , 2010, Current Opinion in Neurobiology.

[42]  S. Shamma,et al.  Temporal coherence and attention in auditory scene analysis , 2011, Trends in Neurosciences.

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

[44]  M. Chait,et al.  Brain Bases for Auditory Stimulus-Driven Figure–Ground Segregation , 2011, The Journal of Neuroscience.

[45]  Gerald Kidd,et al.  Contextual effects in the identification of nonspeech auditory patterns. , 2011, The Journal of the Acoustical Society of America.

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

[47]  Karl J. Friston,et al.  EEG and MEG Data Analysis in SPM8 , 2011, Comput. Intell. Neurosci..

[48]  Melissa K. Gregg,et al.  Attention, Awareness, and the Perception of Auditory Scenes , 2011, Front. Psychology.

[49]  Brian C J Moore,et al.  Properties of auditory stream formation , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[50]  Shihab Shamma,et al.  Temporal coherence versus harmonicity in auditory stream formation. , 2013, The Journal of the Acoustical Society of America.

[51]  Shihab Shamma,et al.  Auditory stream segregation for alternating and synchronous tones. , 2013, Journal of experimental psychology. Human perception and performance.

[52]  S. Shamma,et al.  Segregation of complex acoustic scenes based on temporal coherence , 2013, eLife.

[53]  Morten Løve Jepsen,et al.  Effects of tonotopicity, adaptation, modulation tuning, and temporal coherence in "primitive" auditory stream segregation. , 2014, The Journal of the Acoustical Society of America.

[54]  M. Malmierca,et al.  Adaptation in the auditory system: an overview , 2014, Front. Integr. Neurosci..

[55]  Karl J. Friston,et al.  Algorithmic procedures for Bayesian MEG/EEG source reconstruction in SPM , 2014, NeuroImage.

[56]  Karl J. Friston,et al.  EEG andMEGData Analysis in SPM 8 , 2014 .

[57]  Israel Nelken Stimulus-specific adaptation and deviance detection in the auditory system: experiments and models , 2014, Biological Cybernetics.

[58]  Lucas C. Parra,et al.  Joint decorrelation, a versatile tool for multichannel data analysis , 2014, NeuroImage.

[59]  Mounya Elhilali,et al.  Segregating Complex Sound Sources through Temporal Coherence , 2014, PLoS Comput. Biol..

[60]  S. David,et al.  Emergent Selectivity for Task-Relevant Stimuli in Higher-Order Auditory Cortex , 2014, Neuron.

[61]  Paul A. Fuchs The Oxford handbook of auditory science , 2015 .

[62]  James A. O'Sullivan,et al.  Evidence for Neural Computations of Temporal Coherence in an Auditory Scene and Their Enhancement during Active Listening , 2015, The Journal of Neuroscience.

[63]  Sukhbinder Kumar,et al.  Large-Scale Analysis of Auditory Segregation Behavior Crowdsourced via a Smartphone App , 2016, PloS one.