An anatomical and functional topography of human auditory cortical areas

While advances in magnetic resonance imaging (MRI) throughout the last decades have enabled the detailed anatomical and functional inspection of the human brain non-invasively, to date there is no consensus regarding the precise subdivision and topography of the areas forming the human auditory cortex. Here, we propose a topography of the human auditory areas based on insights on the anatomical and functional properties of human auditory areas as revealed by studies of cyto- and myelo-architecture and fMRI investigations at ultra-high magnetic field (7 Tesla). Importantly, we illustrate that—whereas a group-based approach to analyze functional (tonotopic) maps is appropriate to highlight the main tonotopic axis—the examination of tonotopic maps at single subject level is required to detail the topography of primary and non-primary areas that may be more variable across subjects. Furthermore, we show that considering multiple maps indicative of anatomical (i.e., myelination) as well as of functional properties (e.g., broadness of frequency tuning) is helpful in identifying auditory cortical areas in individual human brains. We propose and discuss a topography of areas that is consistent with old and recent anatomical post-mortem characterizations of the human auditory cortex and that may serve as a working model for neuroscience studies of auditory functions.

[1]  J. Rauschecker,et al.  Functional specialization of medial auditory belt cortex in the alert rhesus monkey. , 2009, Journal of neurophysiology.

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

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

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

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

[6]  D. Lewis,et al.  Mapping auditory core, lateral belt, and parabelt cortices in the human superior temporal gyrus , 2005, The Journal of comparative neurology.

[7]  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.

[8]  T. Elbert,et al.  Specific tonotopic organizations of different areas of the human auditory cortex revealed by simultaneous magnetic and electric recordings. , 1995, Electroencephalography and clinical neurophysiology.

[9]  N. Geschwind,et al.  Human Brain: Left-Right Asymmetries in Temporal Speech Region , 1968, Science.

[10]  R. Zatorre,et al.  Spectral and temporal processing in human auditory cortex. , 2001, Cerebral cortex.

[11]  N. Geschwind,et al.  Right-left asymmetrics in the brain. , 1978, Science.

[12]  Jelliffe Vergleichende Lokalisationslehre der Grosshirnrinde , 1910 .

[13]  Teemu Rinne,et al.  Functional Maps of Human Auditory Cortex: Effects of Acoustic Features and Attention , 2009, PloS one.

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

[15]  K. Scheffler,et al.  Tonotopic organization of the human auditory cortex as detected by BOLD-FMRI , 1998, Hearing Research.

[16]  R V Shannon,et al.  Speech Recognition with Primarily Temporal Cues , 1995, Science.

[17]  Bernd Lütkenhöner,et al.  High-Precision Neuromagnetic Study of the Functional Organization of the Human Auditory Cortex , 1998, Audiology and Neurotology.

[18]  Franck Ramus,et al.  Interhemispheric differences in auditory processing revealed by fMRI in awake rhesus monkeys. , 2012, Cerebral cortex.

[19]  Essa Yacoub,et al.  Spatial organization of frequency preference and selectivity in the human inferior colliculus , 2012, Nature Communications.

[20]  Dave R. M. Langers,et al.  Tonotopic mapping of human auditory cortex , 2014, Hearing Research.

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

[22]  J. Minckler,et al.  A note on the gross configurations of the human auditory cortex , 1976, Brain and Language.

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

[24]  Almut Engelien,et al.  A combined functional in vivo measure for primary and secondary auditory cortices , 2000, Hearing Research.

[25]  Alan C. Evans,et al.  Interhemispheric anatomical differences in human primary auditory cortex: probabilistic mapping and volume measurement from magnetic resonance scans. , 1996, Cerebral cortex.

[26]  C. Economo,et al.  Über Windungsrelief, Maße und Rindenarchitektonik der Supratemporalfläche, ihre individuellen und ihre Seitenunterschiede , 1930 .

[27]  D. Poeppel,et al.  Towards a functional neuroanatomy of speech perception , 2000, Trends in Cognitive Sciences.

[28]  J. Kaas The Evolution of Auditory Cortex: The Core Areas , 2011 .

[29]  S. Scott,et al.  Identification of a pathway for intelligible speech in the left temporal lobe. , 2000, Brain : a journal of neurology.

[30]  Paul J. Abbas,et al.  A chronic microelectrode investigation of the tonotopic organization of human auditory cortex , 1996, Brain Research.

[31]  Klaus Scheffler,et al.  fMRI of the auditory system: understanding the neural basis of auditory gestalt. , 2003, Magnetic resonance imaging.

[32]  B Lütkenhöner,et al.  Studies of tonotopy based on wave N100 of the auditory evoked field are problematic , 2003, NeuroImage.

[33]  Teemu Rinne,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[34]  G L Romani,et al.  Tonotopic organization of the human auditory cortex revealed by steady state neuromagnetic measurements. , 1986, Acta oto-laryngologica. Supplementum.

[35]  Julien Cohen-Adad,et al.  T2* mapping and B0 orientation-dependence at 7T reveal cyto- and myeloarchitecture organization of the human cortex , 2012, NeuroImage.

[36]  L. Chalupa,et al.  Organization of Visual Areas in Macaque and Human Cerebral Cortex , 2002 .

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

[38]  K. Amunts,et al.  Receptor mapping: architecture of the human cerebral cortex , 2009, Current opinion in neurology.

[39]  Stephanie Clarke,et al.  Architecture, Connectivity, and Transmitter Receptors of Human Auditory Cortex , 2012 .

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

[41]  J. Kaas,et al.  Subdivisions of auditory cortex and ipsilateral cortical connections of the parabelt auditory cortex in macaque monkeys , 1998, The Journal of comparative neurology.

[42]  Rainer Goebel,et al.  Development from childhood to adulthood increases morphological and functional inter-individual variability in the right superior temporal cortex , 2013, NeuroImage.

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

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

[45]  D. Yves von Cramon,et al.  Is It Tonotopy after All? , 2002, NeuroImage.

[46]  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.

[47]  P. Marquis,et al.  Intracerebral Evoked Potentials in Pitch Perception Reveal a Functional Asymmetry of the Human Auditory Cortex , 2001, Annals of the New York Academy of Sciences.

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

[49]  Christoph E. Schreiner,et al.  Auditory Cortex Mapmaking: Principles, Projections, and Plasticity , 2007, Neuron.

[50]  Timothy D. Griffiths,et al.  Orthogonal representation of sound dimensions in the primate midbrain , 2011, Nature Neuroscience.

[51]  M. Sereno,et al.  Mapping of Contralateral Space in Retinotopic Coordinates by a Parietal Cortical Area in Humans , 2001, Science.

[52]  Rafael Malach,et al.  Large-Scale Mirror-Symmetry Organization of Human Occipito-Temporal Object Areas , 2003, Neuron.

[53]  Bruce Fischl,et al.  Mapping an intrinsic MR property of gray matter in auditory cortex of living humans: A possible marker for primary cortex and hemispheric differences , 2006, NeuroImage.

[54]  R. Reale,et al.  Tonotopic organization in auditory cortex of the cat , 1980, The Journal of comparative neurology.

[55]  N. Logothetis,et al.  Functional Imaging Reveals Numerous Fields in the Monkey Auditory Cortex , 2006, PLoS biology.

[56]  J. Kaas,et al.  Tonotopic organization, architectonic fields, and connections of auditory cortex in macaque monkeys , 1993, The Journal of comparative neurology.

[57]  Colin Humphries,et al.  Tonotopic organization of human auditory cortex , 2010, NeuroImage.

[58]  J. Rauschecker,et al.  Processing of complex sounds in the macaque nonprimary auditory cortex. , 1995, Science.

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

[60]  Timothy D Griffiths,et al.  Mapping Pitch Representation in Neural Ensembles with fMRI , 2012, The Journal of Neuroscience.

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

[62]  D. Bendor,et al.  The neuronal representation of pitch in primate auditory cortex , 2005, Nature.

[63]  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.

[64]  Shihab A. Shamma,et al.  Dichotomy of functional organization in the mouse auditory cortex , 2010, Nature Neuroscience.

[65]  Amir Amedi,et al.  Extensive Cochleotopic Mapping of Human Auditory Cortical Fields Obtained with Phase-Encoding fMRI , 2011, PloS one.

[66]  Larry E. Roberts,et al.  Frequency organization of the 40-Hz auditory steady-state response in normal hearing and in tinnitus , 2006, NeuroImage.

[67]  R. Zatorre,et al.  Pitch perception of complex tones and human temporal-lobe function. , 1988, The Journal of the Acoustical Society of America.

[68]  E. G. Jones,et al.  Tonotopic organization of auditory cortical fields delineated by parvalbumin immunoreactivity in macaque monkeys , 1997, The Journal of comparative neurology.

[69]  C. Kayser,et al.  Tonotopic organization in human auditory cortex revealed by dedicated fMRI sequence , 2009 .

[70]  N. Logothetis,et al.  A voice region in the monkey brain , 2008, Nature Neuroscience.

[71]  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.

[72]  J W Belliveau,et al.  Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. , 1995, Science.

[73]  Dave R M Langers,et al.  Assessment of tonotopically organised subdivisions in human auditory cortex using volumetric and surface‐based cortical alignments , 2013, Human brain mapping.

[74]  A. Schleicher,et al.  Architectonics of the human cerebral cortex and transmitter receptor fingerprints: reconciling functional neuroanatomy and neurochemistry , 2002, European Neuropsychopharmacology.

[75]  Lisa A. de la Mothe,et al.  A comparison of neuron response properties in areas A1 and CM of the marmoset monkey auditory cortex: tones and broadband noise. , 2005, Journal of neurophysiology.

[76]  S. F. Witelson,et al.  Left hemisphere specialization for language in the newborn. Neuroanatomical evidence of asymmetry. , 1973, Brain : a journal of neurology.

[77]  Pim van Dijk,et al.  Spectrotemporal features of the auditory cortex: the activation in response to dynamic ripples , 2003, NeuroImage.

[78]  W. Singer,et al.  The constructive nature of vision: direct evidence from functional magnetic resonance imaging studies of apparent motion and motion imagery , 1998, The European journal of neuroscience.

[79]  P. Chauvel,et al.  Specialization of left auditory cortex for speech perception in man depends on temporal coding. , 1999, Cerebral cortex.

[80]  R Hari,et al.  Neuromagnetic responses to frequency modulation of a continuous tone. , 1986, Acta oto-laryngologica. Supplementum.

[82]  Jean-Francois Mangin,et al.  Sulcal pattern and morphology of the superior temporal sulcus , 2004, NeuroImage.

[83]  M. Scherg,et al.  Frequency-Specific Sources of the Auditory N19-P30-P50 Response Detected by a Multiple Source Analysis of Evoked Magnetic Fields and Potentials , 1989 .

[84]  Adrian T. Lee,et al.  fMRI of human visual cortex , 1994, Nature.

[85]  Christoph Kayser,et al.  Monkey drumming reveals common networks for perceiving vocal and nonvocal communication sounds , 2009, Proceedings of the National Academy of Sciences.

[86]  Deborah A. Hall,et al.  How challenges in auditory fMRI led to general advancements for the field , 2012, NeuroImage.

[87]  G. Celesia Organization of auditory cortical areas in man. , 1976, Brain : a journal of neurology.

[88]  I. Nelken,et al.  Functional organization and population dynamics in the mouse primary auditory cortex , 2010, Nature Neuroscience.

[89]  Yihong Yang,et al.  Physiological Mapping of Human Auditory Cortices with a Silent Event-Related fMRI Technique , 2002, NeuroImage.

[90]  Daniel S. O'Leary,et al.  An MRI-Based Parcellation Method for the Temporal Lobe , 2000, NeuroImage.

[91]  D. Poeppel,et al.  Latency of auditory evoked M100 as a function of tone frequency , 1996, Neuroreport.

[92]  K. Amunts,et al.  Multimodal architectonic mapping of human superior temporal gyrus , 2005, Anatomy and Embryology.

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

[94]  R. Zatorre,et al.  Voice-selective areas in human auditory cortex , 2000, Nature.

[95]  G. Mangun,et al.  Tonotopy in human auditory cortex examined with functional magnetic resonance imaging , 1997, Human brain mapping.

[96]  J. Clemente,et al.  Diet Drives Convergence in Gut Microbiome Functions Across Mammalian Phylogeny and Within Humans , 2011, Science.

[97]  R. Malach,et al.  The topography of high-order human object areas , 2002, Trends in Cognitive Sciences.

[98]  F. Dick,et al.  Mapping the Human Cortical Surface by Combining Quantitative T1 with Retinotopy† , 2012, Cerebral cortex.

[99]  M. Merzenich,et al.  Representation of the cochlear partition of the superior temporal plane of the macaque monkey. , 1973, Brain research.

[100]  Timothy D. Griffiths,et al.  A unified framework for the organization of the primate auditory cortex , 2013, Front. Syst. Neurosci..

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

[102]  K. Lehnertz,et al.  Tonotopic organization of the human auditory cortex revealed by transient auditory evoked magnetic fields. , 1988, Electroencephalography and clinical neurophysiology.

[103]  A. Dale,et al.  Tonotopic organization in human auditory cortex revealed by progressions of frequency sensitivity. , 2004, Journal of neurophysiology.

[104]  J M Badier,et al.  Evoked potentials recorded from the auditory cortex in man: evaluation and topography of the middle latency components. , 1994, Electroencephalography and clinical neurophysiology.

[105]  Paula Breen,et al.  WHO IS TO SAY , 1967 .

[106]  B. Godde,et al.  A Map of Periodicity Orthogonal to Frequency Representation in the Cat Auditory Cortex , 2009, Frontiers in integrative neuroscience.

[107]  F. Aboitiz,et al.  Bifurcation patterns in the human sylvian fissure: hemispheric and sex differences. , 1996, Cerebral cortex.

[108]  Lutz Jäncke,et al.  Total surface of temporoparietal intrasylvian cortex: Diverging left-right asymmetries , 1990, Brain and Language.

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

[110]  A. Palmer,et al.  Histochemical identification of cortical areas in the auditory region of the human brain , 2002, Experimental Brain Research.

[111]  M M Merzenich,et al.  Cochleotopic organization of primary auditory cortex in the cat. , 1973, Brain research.

[112]  R. Zatorre,et al.  Structure and function of auditory cortex: music and speech , 2002, Trends in Cognitive Sciences.

[113]  Jean-Francois Mangin,et al.  A robust cerebral asymmetry in the infant brain: The rightward superior temporal sulcus , 2011, NeuroImage.

[114]  Dave R. M. Langers,et al.  Representation of lateralization and tonotopy in primary versus secondary human auditory cortex , 2007, NeuroImage.

[115]  Mitchell Steinschneider,et al.  Spectral organization of the human lateral superior temporal gyrus revealed by intracranial recordings. , 2014, Cerebral cortex.

[116]  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.