Auditory Cortex Encodes the Perceptual Interpretation of Ambiguous Sound

The confounding of physical stimulus characteristics and perceptual interpretations of stimuli poses a problem for most neuroscientific studies of perception. In the auditory domain, this pertains to the entanglement of acoustics and percept. Traditionally, most study designs have relied on cognitive subtraction logic, which demands the use of one or more comparisons between stimulus types. This does not allow for a differentiation between effects due to acoustic differences (i.e., sensation) and those due to conscious perception. To overcome this problem, we used functional magnetic resonance imaging (fMRI) in humans and pattern-recognition analysis to identify activation patterns that encode the perceptual interpretation of physically identical, ambiguous sounds. We show that it is possible to retrieve the perceptual interpretation of ambiguous phonemes—information that is fully subjective to the listener—from fMRI measurements of brain activity in auditory areas in the superior temporal cortex, most prominently on the posterior bank of the left Heschl's gyrus and sulcus and in the adjoining left planum temporale. These findings suggest that, beyond the basic acoustic analysis of sounds, constructive perceptual processes take place in these relatively early cortical auditory networks. This disagrees with hierarchical models of auditory processing, which generally conceive of these areas as sets of feature detectors, whose task is restricted to the analysis of physical characteristics and the structure of sounds.

[1]  R. Turner,et al.  Event-Related fMRI: Characterizing Differential Responses , 1998, NeuroImage.

[2]  Vladimir N. Vapnik,et al.  The Nature of Statistical Learning Theory , 2000, Statistics for Engineering and Information Science.

[3]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

[4]  P. Morosan,et al.  Probabilistic Mapping and Volume Measurement of Human Primary Auditory Cortex , 2001, NeuroImage.

[5]  P. Morosan,et al.  Human Primary Auditory Cortex: Cytoarchitectonic Subdivisions and Mapping into a Spatial Reference System , 2001, NeuroImage.

[6]  H. Scheich,et al.  Phonetic Perception and the Temporal Cortex , 2002, NeuroImage.

[7]  S. Hochstein,et al.  View from the Top Hierarchies and Reverse Hierarchies in the Visual System , 2002, Neuron.

[8]  T. Griffiths,et al.  The planum temporale as a computational hub , 2002, Trends in Neurosciences.

[9]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[10]  R. Goebel,et al.  Mirror-Symmetric Tonotopic Maps in Human Primary Auditory Cortex , 2003, Neuron.

[11]  P. Bertelson,et al.  Visual Recalibration of Auditory Speech Identification , 2003, Psychological science.

[12]  S. Scott,et al.  The neuroanatomical and functional organization of speech perception , 2003, Trends in Neurosciences.

[13]  Matthew H. Davis,et al.  Hierarchical Processing in Spoken Language Comprehension , 2003, The Journal of Neuroscience.

[14]  R. Goebel,et al.  Integration of Letters and Speech Sounds in the Human Brain , 2004, Neuron.

[15]  M. Scherg,et al.  Neuromagnetic Correlates of Streaming in Human Auditory Cortex , 2005, The Journal of Neuroscience.

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

[17]  J. Rauschecker,et al.  Perceptual Organization of Tone Sequences in the Auditory Cortex of Awake Macaques , 2005, Neuron.

[18]  G. Rees,et al.  Predicting the orientation of invisible stimuli from activity in human primary visual cortex , 2005, Nature Neuroscience.

[19]  David A. Medler,et al.  Cerebral Cortex doi:10.1093/cercor/bhi040 Cerebral Cortex Advance Access published February 9, 2005 , 2022 .

[20]  Rainer Goebel,et al.  Analysis of functional image analysis contest (FIAC) data with brainvoyager QX: From single‐subject to cortically aligned group general linear model analysis and self‐organizing group independent component analysis , 2006, Human brain mapping.

[21]  Cheng Cheng,et al.  Robust estimation of the false discovery rate , 2006, Bioinform..

[22]  Rajeev D. S. Raizada,et al.  Selective Amplification of Stimulus Differences during Categorical Processing of Speech , 2007, Neuron.

[23]  Israel Nelken,et al.  The Effects of Background Noise on the Neural Responses to Natural Sounds in Cat Primary Auditory Cortex , 2007, Frontiers Comput. Neurosci..

[24]  Rainer Goebel,et al.  The effect of temporal asynchrony on the multisensory integration of letters and speech sounds. , 2006, Cerebral cortex.

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

[26]  D. Poeppel,et al.  The cortical organization of speech processing , 2007, Nature Reviews Neuroscience.

[27]  Rainer Goebel,et al.  "Who" Is Saying "What"? Brain-Based Decoding of Human Voice and Speech , 2008, Science.

[28]  Rainer Goebel,et al.  Combining multivariate voxel selection and support vector machines for mapping and classification of fMRI spatial patterns , 2008, NeuroImage.

[29]  I. Nelken,et al.  Neurons and Objects: The Case of Auditory Cortex , 2008, Front. Neurosci..

[30]  Hans-Jochen Heinze,et al.  Predicting the recognition of natural scenes from single trial MEG recordings of brain activity , 2000, NeuroImage.

[31]  Jeffrey R. Binder,et al.  Left Posterior Temporal Regions are Sensitive to Auditory Categorization , 2008, Journal of Cognitive Neuroscience.

[32]  S. Hochstein,et al.  Reverse hierarchies and sensory learning , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[33]  Kayoko Okada,et al.  Area Spt in the Human Planum Temporale Supports Sensory-motor Integration for Speech Processing Establishing the Existence of Distinct Sen- Sory versus Motor Activation Patterns Would Establish That , 2022 .

[34]  Lars Riecke,et al.  Hearing Illusory Sounds in Noise: The Timing of Sensory-Perceptual Transformations in Auditory Cortex , 2009, Neuron.

[35]  J. Rauschecker,et al.  Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing , 2009, Nature Neuroscience.

[36]  G. Rees,et al.  The Neural Bases of Multistable Perception , 2022 .

[37]  L. Fadiga,et al.  The Motor Somatotopy of Speech Perception , 2009, Current Biology.

[38]  Noël Staeren,et al.  Sound Categories Are Represented as Distributed Patterns in the Human Auditory Cortex , 2009, Current Biology.

[39]  J. Obleser,et al.  Pre-lexical abstraction of speech in the auditory cortex , 2009, Trends in Cognitive Sciences.