Evaluating the Columnar Stability of Acoustic Processing in the Human Auditory Cortex

Using ultra-high field fMRI, we explored the cortical depth-dependent stability of acoustic feature preference in human auditory cortex. We collected responses from human auditory cortex (subjects from either sex) to a large number of natural sounds at submillimeter spatial resolution, and observed that these responses were well explained by a model that assumes neuronal population tuning to frequency-specific spectrotemporal modulations. We observed a relatively stable (columnar) tuning to frequency and temporal modulations. However, spectral modulation tuning was variable throughout the cortical depth. This difference in columnar stability between feature maps could not be explained by a difference in map smoothness, as the preference along the cortical sheet varied in a similar manner for the different feature maps. Furthermore, tuning to all three features was more columnar in primary than nonprimary auditory cortex. The observed overall lack of overlapping columnar regions across acoustic feature maps suggests, especially for primary auditory cortex, a coding strategy in which across cortical depths tuning to some features is kept stable, whereas tuning to other features systematically varies. SIGNIFICANCE STATEMENT In the human auditory cortex, sound aspects are processed in large-scale maps. Invasive animal studies show that an additional processing organization may be implemented orthogonal to the cortical sheet (i.e., in the columnar direction), but it is unknown whether observed organizational principles apply to the human auditory cortex. Combining ultra-high field fMRI with natural sounds, we explore the columnar organization of various sound aspects. Our results suggest that the human auditory cortex contains a modular coding strategy, where, for each module, several sound aspects act as an anchor along which computations are performed while the processing of another sound aspect undergoes a transformation. This strategy may serve to optimally represent the content of our complex acoustic natural environment.

[1]  R. Goebel,et al.  Mapping the Organization of Axis of Motion Selective Features in Human Area MT Using High-Field fMRI , 2011, PloS one.

[2]  Essa Yacoub,et al.  High-field fMRI unveils orientation columns in humans , 2008, Proceedings of the National Academy of Sciences.

[3]  Ravi S. Menon,et al.  Ocular dominance in human V1 demonstrated by functional magnetic resonance imaging. , 1997, Journal of neurophysiology.

[4]  Shahin Nasr,et al.  Interdigitated Color- and Disparity-Selective Columns within Human Visual Cortical Areas V2 and V3 , 2016, The Journal of Neuroscience.

[5]  P. van Dijk,et al.  Mapping the Tonotopic Organization in Human Auditory Cortex with Minimally Salient Acoustic Stimulation , 2011, Cerebral cortex.

[6]  M. Sutter Spectral processing in the auditory cortex. , 2005, International review of neurobiology.

[7]  C. Schroeder,et al.  Layer Specific Sharpening of Frequency Tuning by Selective Attention in Primary Auditory Cortex , 2014, The Journal of Neuroscience.

[8]  P. Rakic Confusing cortical columns , 2008, Proceedings of the National Academy of Sciences.

[9]  C E Schreiner,et al.  Neural processing of amplitude-modulated sounds. , 2004, Physiological reviews.

[10]  Frédéric E. Theunissen,et al.  The Modulation Transfer Function for Speech Intelligibility , 2009, PLoS Comput. Biol..

[11]  D. P. Phillips,et al.  Some features of binaural input to single neurons in physiologically defined area AI of cat cerebral cortex. , 1983, Journal of neurophysiology.

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

[13]  S. Shamma,et al.  Spectro-temporal modulation transfer functions and speech intelligibility. , 1999, The Journal of the Acoustical Society of America.

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

[15]  D. V. van Essen,et al.  Mapping Human Cortical Areas In Vivo Based on Myelin Content as Revealed by T1- and T2-Weighted MRI , 2011, The Journal of Neuroscience.

[16]  R. Nieuwenhuys The myeloarchitectonic studies on the human cerebral cortex of the Vogt–Vogt school, and their significance for the interpretation of functional neuroimaging data , 2013, Brain Structure and Function.

[17]  Essa Yacoub,et al.  Encoding of Natural Sounds at Multiple Spectral and Temporal Resolutions in the Human Auditory Cortex , 2014, PLoS Comput. Biol..

[18]  J. Kaas,et al.  Architectonic identification of the core region in auditory cortex of macaques, chimpanzees, and humans , 2001, The Journal of comparative neurology.

[19]  Essa Yacoub,et al.  High resolution data analysis strategies for mesoscale human functional MRI at 7 and 9.4 T , 2018, NeuroImage.

[20]  R. Tootell,et al.  Columnar Segregation of Magnocellular and Parvocellular Streams in Human Extrastriate Cortex , 2017, The Journal of Neuroscience.

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

[22]  Ikuo Taniguchi,et al.  The columnar and layer-specific response properties of neurons in the primary auditory cortex of Mongolian gerbils , 1997, Hearing Research.

[23]  R. Goebel,et al.  Cortical Depth Dependent Functional Responses in Humans at 7T: Improved Specificity with 3D GRASE , 2013, PloS one.

[24]  I. Aharon,et al.  Three‐dimensional mapping of cortical thickness using Laplace's Equation , 2000, Human brain mapping.

[25]  M. Schönwiesner,et al.  Spectro-temporal modulation transfer function of single voxels in the human auditory cortex measured with high-resolution fMRI , 2009, Proceedings of the National Academy of Sciences.

[26]  C. Schreiner,et al.  Functional topography of cat primary auditory cortex: responses to frequency-modulated sweeps , 2004, Experimental Brain Research.

[27]  Gregory Hickok,et al.  Orthogonal acoustic dimensions define auditory field maps in human cortex , 2012, Proceedings of the National Academy of Sciences.

[28]  F. Dick,et al.  In Vivo Functional and Myeloarchitectonic Mapping of Human Primary Auditory Areas , 2012, The Journal of Neuroscience.

[29]  S. Clarke,et al.  Cytochrome Oxidase, Acetylcholinesterase, and NADPH-Diaphorase Staining in Human Supratemporal and Insular Cortex: Evidence for Multiple Auditory Areas , 1997, NeuroImage.

[30]  Jonathan Winawer,et al.  GLMdenoise: a fast, automated technique for denoising task-based fMRI data , 2013, Front. Neurosci..

[31]  C E Schreiner,et al.  Modular organization of intrinsic connections associated with spectral tuning in cat auditory cortex , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Richard S. J. Frackowiak,et al.  Human Primary Auditory Cortex Follows the Shape of Heschl's Gyrus , 2011, The Journal of Neuroscience.

[33]  Elia Formisano,et al.  Processing of Natural Sounds in Human Auditory Cortex: Tonotopy, Spectral Tuning, and Relation to Voice Sensitivity , 2012, The Journal of Neuroscience.

[34]  C. Schreiner,et al.  Columnar transformations in auditory cortex? A comparison to visual and somatosensory cortices. , 2003, Cerebral Cortex.

[35]  J. Rauschecker,et al.  Processing of band-passed noise in the lateral auditory belt cortex of the rhesus monkey. , 2004, Journal of neurophysiology.

[36]  Essa Yacoub,et al.  Robust detection of ocular dominance columns in humans using Hahn Spin Echo BOLD functional MRI at 7 Tesla , 2007, NeuroImage.

[37]  M. Escabí,et al.  Spectral and temporal modulation tradeoff in the inferior colliculus. , 2010, Journal of Neurophysiology.

[38]  Steen Moeller,et al.  T 1 weighted brain images at 7 Tesla unbiased for Proton Density, T 2 ⁎ contrast and RF coil receive B 1 sensitivity with simultaneous vessel visualization , 2009, NeuroImage.

[39]  R. Goebel,et al.  High-Resolution Mapping of Myeloarchitecture In Vivo: Localization of Auditory Areas in the Human Brain. , 2015, Cerebral cortex.

[40]  Essa Yacoub,et al.  Sensitivity and specificity considerations for fMRI encoding, decoding, and mapping of auditory cortex at ultra-high field , 2018, NeuroImage.

[41]  R. Goebel,et al.  Processing of Natural Sounds: Characterization of Multipeak Spectral Tuning in Human Auditory Cortex , 2013, The Journal of Neuroscience.

[42]  A. Galaburda,et al.  Cytoarchitectonic organization of the human auditory cortex , 1980, The Journal of comparative neurology.

[43]  A. E. Hoerl,et al.  Ridge Regression: Applications to Nonorthogonal Problems , 1970 .

[44]  Christoph E Schreiner,et al.  Functional architecture of auditory cortex , 2002, Current Opinion in Neurobiology.

[45]  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.

[46]  M. Abeles,et al.  Functional architecture in cat primary auditory cortex: columnar organization and organization according to depth. , 1970, Journal of neurophysiology.

[47]  Essa Yacoub,et al.  Processing of frequency and location in human subcortical auditory structures , 2015, Scientific Reports.

[48]  V. Mountcastle The columnar organization of the neocortex. , 1997, Brain : a journal of neurology.

[49]  Daniel L Adams,et al.  The cortical column: a structure without a function , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[50]  Keiji Tanaka,et al.  Human Ocular Dominance Columns as Revealed by High-Field Functional Magnetic Resonance Imaging , 2001, Neuron.

[51]  C. Atencio,et al.  Hierarchical computation in the canonical auditory cortical circuit , 2009, Proceedings of the National Academy of Sciences.

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

[53]  Arthur E. Hoerl,et al.  Ridge Regression: Biased Estimation for Nonorthogonal Problems , 2000, Technometrics.

[54]  D. Feinberg,et al.  GRASE (Gradient‐and Spin‐Echo) imaging: A novel fast MRI technique , 1991, Magnetic resonance in medicine.

[55]  Powen Ru,et al.  Multiresolution spectrotemporal analysis of complex sounds. , 2005, The Journal of the Acoustical Society of America.

[56]  E. G. Jones,et al.  Microcolumns in the cerebral cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[57]  Kathleen A. Hansen,et al.  Modeling low‐frequency fluctuation and hemodynamic response timecourse in event‐related fMRI , 2008, Human brain mapping.

[58]  C. Atencio,et al.  Laminar diversity of dynamic sound processing in cat primary auditory cortex. , 2010, Journal of neurophysiology.

[59]  R. Goebel,et al.  Frequency preference and attention effects across cortical depths in the human primary auditory cortex , 2015, Proceedings of the National Academy of Sciences.

[60]  Klaus Scheffler,et al.  Spatial representations of temporal and spectral sound cues in human auditory cortex , 2013, Cortex.

[61]  D P Phillips,et al.  Responses of single neurons in physiologically defined primary auditory cortex (AI) of the cat: frequency tuning and responses to intensity. , 1981, Journal of neurophysiology.

[62]  J. Fritz,et al.  Rapid task-related plasticity of spectrotemporal receptive fields in primary auditory cortex , 2003, Nature Neuroscience.

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

[64]  M. Merzenich,et al.  Responses of neurons in auditory cortex of the macaque monkey to monaural and binaural stimulation. , 1973, Journal of neurophysiology.

[65]  Pierre-Louis Bazin,et al.  Anatomically motivated modeling of cortical laminae , 2014, NeuroImage.

[66]  T. Imig,et al.  Functional organization of sound direction and sound pressure level in primary auditory cortex of the cat. , 1994, Journal of neurophysiology.