Tonotopic organization of the human auditory cortex probed with frequency-modulated tones

Using neuromagnetic source imaging, we investigated tonotopic representation and direction sensitivity in the auditory cortex of humans (N = 15). For this purpose, source analysis was undertaken at every single sampling point during the presentation of a frequency-modulated tone (FM) sweeping slowly downward or upward across periods of 3 s duration. Stimuli were selected to target response properties of the central part of the primary auditory cortical field, which has been shown to exhibit sensitivity to distinct FM-sound features as compared to the ventral and dorsal part. Linear mixed-effects model statistics confirm tonotopic gradients in medial-lateral and anterior-posterior directions. The high resolution provided by this method revealed that the relationship between frequency and spatial location of the responding neural tissue is nonlinear. The idea that neurons specifically sensitive to the employed sound characteristics (slow, downward modulation) were activated is supported by the fact that the upward sweep of identical duration produced a different pattern of functional organisation.

[1]  H. Goldstein.  Multilevel Statistical Models , 2006 .

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

[3]  D. Bates,et al.  Mixed-Effects Models in S and S-PLUS , 2001 .

[4]  I. Taniguchi,et al.  Optical recording of responses to frequency‐modulated sounds in the auditory cortex , 1998, Neuroreport.

[5]  Günter Ehret,et al.  The Central Auditory System , 1996 .

[6]  M. Gluck,et al.  Spectrotemporal sensitivities in rat auditory cortical neurons , 2001, Hearing Research.

[7]  M Hoke,et al.  Tonotopic organization of the auditory cortex: pitch versus frequency representation. , 1989, Science.

[8]  L. Pessoa,et al.  Filling-in: From perceptual completion to cortical reorganization. , 2003 .

[9]  M Hoke,et al.  The auditory evoked sustained field: origin and frequency dependence. , 1994, Electroencephalography and clinical neurophysiology.

[10]  Matthias M. Müller,et al.  Expansion of the Tonotopic Area in the Auditory Cortex of the Blind , 2002, The Journal of Neuroscience.

[11]  I. Nelken,et al.  Responses to linear and logarithmic frequency‐modulated sweeps in ferret primary auditory cortex , 2000, The European journal of neuroscience.

[12]  Ross Ihaka,et al.  Gentleman R: R: A language for data analysis and graphics , 1996 .

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

[14]  C. Schreiner,et al.  Modular organization of frequency integration in primary auditory cortex. , 2000, Annual review of neuroscience.

[15]  D. Irvine,et al.  Functional specialization in auditory cortex: responses to frequency-modulated stimuli in the cat's posterior auditory field. , 1998, Journal of neurophysiology.

[16]  D. Irvine,et al.  Sensitivity of neurons in cat primary auditory cortex to tones and frequency-modulated stimuli. I: Effects of variation of stimulus parameters , 1992, Hearing Research.

[17]  P. Chauvel,et al.  Neuromagnetic source localization of auditory evoked fields and intracerebral evoked potentials: a comparison of data in the same patients , 2001, Clinical Neurophysiology.

[18]  Jacob Cohen.  Statistical Power Analysis for the Behavioral Sciences , 1969, The SAGE Encyclopedia of Research Design.

[19]  M. Cynader,et al.  Sensitivity of cat primary auditory cortex (Al) neurons to the direction and rate of frequency modulation , 1985, Brain Research.

[20]  J. Kaas,et al.  Auditory processing in primate cerebral cortex , 1999, Current Opinion in Neurobiology.

[21]  I. Nelken,et al.  In search of the best stimulus: An optimization procedure for finding efficient stimuli in the cat auditory cortex , 1994, Hearing Research.

[22]  D. Irvine,et al.  Sensitivity of neurons in cat primary auditory cortex to tones and frequency-modulated stimuli. II: Organization of response properties along the ‘isofrequency’ dimension , 1992, Hearing Research.

[23]  Peter Herscovitch,et al.  Tonotopic organization in human auditory cortex revealed by positron emission tomography , 1985, Hearing Research.

[24]  L. Kaufman,et al.  Tonotopic organization of the human auditory cortex. , 1982, Science.

[25]  R. Burkard,et al.  The functional anatomy of the normal human auditory system: responses to 0.5 and 4.0 kHz tones at varied intensities. , 1999, Cerebral cortex.

[26]  C. Pantev,et al.  Tonotopic organization of the sources of human auditory steady-state responses , 1996, Hearing Research.

[27]  J P Rauschecker,et al.  Processing of frequency-modulated sounds in the cat's anterior auditory field. , 1994, Journal of neurophysiology.

[28]  C. Elberling,et al.  Auditory magnetic fields: source location and 'tonotopical organization' in the right hemisphere of the human brain. , 1982, Scandinavian audiology.

[29]  H. Scheich,et al.  Optical imaging of neural activity in multiple auditory cortical fields of guinea pigs , 2001, Neuroreport.

[30]  Stephen T. Neely,et al.  Signals, Sound, and Sensation , 1997 .

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

[32]  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.

[33]  M. Bozkurt,et al.  Functional anatomy. , 1980, Equine veterinary journal.

[34]  Li I. Zhang,et al.  Topography and synaptic shaping of direction selectivity in primary auditory cortex , 2003, Nature.

[35]  J. Eggermont.  Between sound and perception: reviewing the search for a neural code , 2001, Hearing Research.

[36]  C Pantev,et al.  A high-precision magnetoencephalographic study of human auditory steady-state responses to amplitude-modulated tones. , 2000, The Journal of the Acoustical Society of America.

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

[38]  R. Ilmoniemi,et al.  Magnetoencephalography-theory, instrumentation, and applications to noninvasive studies of the working human brain , 1993 .

[39]  S. Shamma,et al.  Organization of response areas in ferret primary auditory cortex. , 1993, Journal of neurophysiology.

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

[41]  L. Kaufman,et al.  Characterization of the human auditory cortex by the neuromagnetic method , 2004, Experimental Brain Research.

[42]  Gerald Langner,et al.  Processing of frequency-modulated stimuli in the chick auditory cortex analogue: evidence for topographic representations and possible mechanisms of rate and directional sensitivity , 1992, Journal of Comparative Physiology A.

[43]  M. Merzenich,et al.  Optimizing sound features for cortical neurons. , 1998, Science.

[44]  G. Ehret.  The auditory cortex , 1997, Journal of Comparative Physiology A.

[45]  William E. O'Neill,et al.  Temporal processing across frequency channels by FM selective auditory neurons can account for FM rate selectivity , 1998, Hearing Research.

[46]  J P Rauschecker,et al.  Processing of frequency-modulated sounds in the cat's posterior auditory field. , 1994, Journal of neurophysiology.

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

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

[49]  W Vennart,et al.  Magnetism in Medicine: A Handbook , 1999 .