Neural representation of three-dimensional acoustic space in the human temporal lobe

Sound localization is an important function of the human brain, but the underlying cortical mechanisms remain unclear. In this study, we recorded auditory stimuli in three-dimensional space and then replayed the stimuli through earphones during functional magnetic resonance imaging (fMRI). By employing a machine learning algorithm, we successfully decoded sound location from the blood oxygenation level-dependent signals in the temporal lobe. Analysis of the data revealed that different cortical patterns were evoked by sounds from different locations. Specifically, discrimination of sound location along the abscissa axis evoked robust responses in the left posterior superior temporal gyrus (STG) and right mid-STG, discrimination along the elevation (EL) axis evoked robust responses in the left posterior middle temporal lobe (MTL) and right STG, and discrimination along the ordinate axis evoked robust responses in the left mid-MTL and right mid-STG. These results support a distributed representation of acoustic space in human cortex.

[1]  G L Romani,et al.  Human brain activation during passive listening to sounds from different locations: An fMRI and MEG study , 2005, Human brain mapping.

[2]  Talia Shrem,et al.  Spatial Localization of Auditory Stimuli in Human Auditory Cortex is Based on Both Head-Independent and Head-Centered Coordinate Systems , 2012, The Journal of Neuroscience.

[3]  J. Blauert Spatial Hearing: The Psychophysics of Human Sound Localization , 1983 .

[4]  K. Jambrosic,et al.  Sound localization , 2004, Proceedings. Elmar-2004. 46th International Symposium on Electronics in Marine.

[5]  J. Rauschecker,et al.  Evidence for distinct human auditory cortex regions for sound location versus identity processing , 2013, Nature Communications.

[6]  J. Rauschecker,et al.  A PET study of human auditory spatial processing , 1999, Neuroscience Letters.

[7]  Barbara G Shinn-Cunningham,et al.  Cerebral Cortex doi:10.1093/cercor/bhs359 Auditory Spatial Attention Representations in the Human Cerebral Cortex , 2012 .

[8]  Xiaoqin Wang,et al.  Level dependence of spatial processing in the primate auditory cortex. , 2012, Journal of neurophysiology.

[9]  Jochen Kaiser,et al.  Effects of feature-selective attention on auditory pattern and location processing , 2008, NeuroImage.

[10]  Jörg Lewald,et al.  Processing of sound location in human cortex , 2008, The European journal of neuroscience.

[11]  J. Thiran,et al.  Distinct Pathways Involved in Sound Recognition and Localization: A Human fMRI Study , 2000, NeuroImage.

[12]  Glenn C. Thompson,et al.  The inability of squirrel monkeys to localize sound after unilateral ablation of auditory cortex , 1983, Behavioural Brain Research.

[13]  Robert A. A. Campbell,et al.  Physiological and behavioral studies of spatial coding in the auditory cortex , 2007, Hearing Research.

[14]  Alan R Palmer,et al.  Descending projections from auditory cortex modulate sensitivity in the midbrain to cues for spatial position. , 2008, Journal of neurophysiology.

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

[16]  J. Rauschecker,et al.  Hierarchical Organization of the Human Auditory Cortex Revealed by Functional Magnetic Resonance Imaging , 2001, Journal of Cognitive Neuroscience.

[17]  John C. Middlebrooks,et al.  Auditory space processing: here, there or everywhere? , 2002, Nature Neuroscience.

[18]  John C. Middlebrooks,et al.  Auditory Cortex Spatial Sensitivity Sharpens During Task Performance , 2010, Nature Neuroscience.

[19]  Peter Bremen,et al.  Rat primary auditory cortex is tuned exclusively to the contralateral hemifield. , 2013, Journal of neurophysiology.

[20]  Giancarlo Valente,et al.  Multivariate analysis of fMRI time series: classification and regression of brain responses using machine learning. , 2008, Magnetic resonance imaging.

[21]  J. C. Middlebrooks Sound localization. , 2015, Handbook of clinical neurology.

[22]  E. Macaluso,et al.  A Common Cortical Substrate Activated by Horizontal and Vertical Sound Movement in the Human Brain , 2002, Current Biology.

[23]  R. Zatorre,et al.  Where is 'where' in the human auditory cortex? , 2002, Nature Neuroscience.

[24]  Lee M. Miller,et al.  Populations of auditory cortical neurons can accurately encode acoustic space across stimulus intensity , 2009, Proceedings of the National Academy of Sciences.

[25]  D. Irvine,et al.  Topographic organization of interaural intensity difference sensitivity in deep layers of cat superior colliculus: implications for auditory spatial representation. , 1985, Journal of neurophysiology.

[26]  W R Thurlow,et al.  Effect of induced head movements on localization of direction of sounds. , 1967, The Journal of the Acoustical Society of America.

[27]  Robert T. Knight,et al.  Cerebral Responses to Change in Spatial Location of Unattended Sounds , 2007, Neuron.

[28]  J. Gallant,et al.  Identifying natural images from human brain activity , 2008, Nature.

[29]  J. Fell,et al.  Lateralized auditory spatial perception and the contralaterality of cortical processing as studied with functional magnetic resonance imaging and magnetoencephalography , 1999, Human brain mapping.

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

[31]  John C. Middlebrooks,et al.  Distributed coding of sound locations in the auditory cortex , 2003, Biological Cybernetics.

[32]  Michael Erb,et al.  Processing of auditory spatial cues in human cortex: An fMRI study , 2006, Neuropsychologia.

[33]  V R Algazi,et al.  Elevation localization and head-related transfer function analysis at low frequencies. , 2001, The Journal of the Acoustical Society of America.

[34]  Chris Rorden,et al.  Spatial Attention Evokes Similar Activation Patterns for Visual and Auditory Stimuli , 2010, Journal of Cognitive Neuroscience.

[35]  Jochen Kaiser,et al.  Processing of Auditory Location Changes after Horizontal Head Rotation , 2009, The Journal of Neuroscience.

[36]  J. C. Middlebrooks,et al.  Location Coding by Opponent Neural Populations in the Auditory Cortex , 2005, PLoS biology.

[37]  B. Grothe,et al.  Mechanisms of sound localization in mammals. , 2010, Physiological reviews.

[38]  R. Bowtell,et al.  “sparse” temporal sampling in auditory fMRI , 1999, Human brain mapping.

[39]  Bruce D. McCandliss,et al.  Brain mechanisms implicated in the preattentive categorization of speech sounds revealed using FMRI and a short-interval habituation trial paradigm. , 2007, Cerebral cortex.

[40]  M M Merzenich,et al.  Representation of cochlea within primary auditory cortex in the cat. , 1975, Journal of neurophysiology.

[41]  Hanna Damasio,et al.  Predicting visual stimuli on the basis of activity in auditory cortices , 2010, Nature Neuroscience.

[42]  D. Hubel,et al.  Receptive fields of single neurones in the cat's striate cortex , 1959, The Journal of physiology.

[43]  P. Alku,et al.  Asymmetrical representation of auditory space in human cortex , 2010, Brain Research.

[44]  J. C. Middlebrooks,et al.  Two-dimensional sound localization by human listeners. , 1990, The Journal of the Acoustical Society of America.

[45]  J. Rauschecker,et al.  Functional Specialization in Rhesus Monkey Auditory Cortex , 2001, Science.

[46]  Jörg Lewald,et al.  When and Where of Auditory Spatial Processing in Cortex: A Novel Approach Using Electrotomography , 2011, PloS one.

[47]  C. Rorden,et al.  Stereotaxic display of brain lesions. , 2000, Behavioural neurology.

[48]  Karl J. Friston,et al.  Statistical parametric mapping , 2013 .

[49]  Doug J. K. Barrett,et al.  Response preferences for “what” and “where” in human non-primary auditory cortex , 2006, NeuroImage.

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

[51]  Simon Carlile,et al.  The nature and distribution of errors in sound localization by human listeners , 1997, Hearing Research.

[52]  G H Recanzone,et al.  Spatial processing in the auditory cortex of the macaque monkey. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[53]  E. Macaluso,et al.  High Binaural Coherence Determines Successful Sound Localization and Increased Activity in Posterior Auditory Areas , 2005, Neuron.

[54]  Andrea Bergmann,et al.  Statistical Parametric Mapping The Analysis Of Functional Brain Images , 2016 .

[55]  J. Kaas,et al.  Subdivisions of auditory cortex and processing streams in primates. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[56]  Tom M. Mitchell,et al.  Machine learning classifiers and fMRI: A tutorial overview , 2009, NeuroImage.

[57]  Eric I. Knudsen,et al.  Maps versus clusters: different representations of auditory space in the midbrain and forebrain , 1999, Trends in Neurosciences.

[58]  John C. Middlebrooks,et al.  Directional sensitivity of neurons in the primary auditory (AI) cortex: effects of sound-source intensity level. , 2003, Journal of neurophysiology.

[59]  Jörg Lewald,et al.  Sound localization with eccentric head position , 2000, Behavioural Brain Research.

[60]  L A JEFFRESS,et al.  A place theory of sound localization. , 1948, Journal of comparative and physiological psychology.

[61]  Henrik Møller Fundamentals of binaural technology , 1991 .

[62]  Tom Michael Mitchell,et al.  Predicting Human Brain Activity Associated with the Meanings of Nouns , 2008, Science.