Transient bold activity locked to perceptual reversals of auditory streaming in human auditory cortex and inferior colliculus.

Our auditory system separates and tracks temporally interleaved sound sources by organizing them into distinct auditory streams. This streaming phenomenon is partly determined by physical stimulus properties but additionally depends on the internal state of the listener. As a consequence, streaming perception is often bistable and reversals between one- and two-stream percepts may occur spontaneously or be induced by a change of the stimulus. Here, we used functional MRI to investigate perceptual reversals in streaming based on interaural time differences (ITD) that produce a lateralized stimulus perception. Listeners were continuously presented with two interleaved streams, which slowly moved apart and together again. This paradigm produced longer intervals between reversals than stationary bistable stimuli but preserved temporal independence between perceptual reversals and physical stimulus transitions. Results showed prominent transient activity synchronized with the perceptual reversals in and around the auditory cortex. Sustained activity in the auditory cortex was observed during intervals where the ΔITD could potentially produce streaming, similar to previous studies. A localizer-based analysis additionally revealed transient activity time locked to perceptual reversals in the inferior colliculus. These data suggest that neural activity associated with streaming reversals is not limited to the thalamo-cortical system but involves early binaural processing in the auditory midbrain, already.

[1]  Anders M. Dale,et al.  Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex , 2001, IEEE Transactions on Medical Imaging.

[2]  J. Hupé,et al.  Temporal Dynamics of Auditory and Visual Bistability Reveal Common Principles of Perceptual Organization , 2006, Current Biology.

[3]  R W Cox,et al.  Real‐time 3D image registration for functional MRI , 1999, Magnetic resonance in medicine.

[4]  B. Delgutte,et al.  A Physiologically Based Model of Interaural Time Difference Discrimination , 2004, The Journal of Neuroscience.

[5]  A. Gutschalk,et al.  Functional dissociation of transient and sustained fMRI BOLD components in human auditory cortex revealed with a streaming paradigm based on interaural time differences , 2010, The European journal of neuroscience.

[6]  Dennis P Phillips,et al.  The relation between auditory temporal interval processing and sequential stream segregation examined with stimulus laterality differences , 2005, Perception & psychophysics.

[7]  Douglas Johnson,et al.  Stream Segregation and Peripheral Channeling , 1991 .

[8]  Torsten Marquardt,et al.  Representation of interaural time delay in the human auditory midbrain , 2006, Nature Neuroscience.

[9]  Alexander Gutschalk,et al.  Activity associated with stream segregation in human auditory cortex is similar for spatial and pitch cues. , 2010, Cerebral cortex.

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

[11]  Irina S. Sigalovsky,et al.  Short-term sound temporal envelope characteristics determine multisecond time patterns of activity in human auditory cortex as shown by fMRI. , 2005, Journal of neurophysiology.

[12]  N. Suga,et al.  Experience-dependent corticofugal adjustment of midbrain frequency map in bat auditory system. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[13]  R.B. Lake,et al.  Programs for digital signal processing , 1981, Proceedings of the IEEE.

[14]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[15]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

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

[17]  Mitchell Steinschneider,et al.  Neural correlates of auditory stream segregation in primary auditory cortex of the awake monkey , 2001, Hearing Research.

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

[19]  Makio Kashino,et al.  Involvement of the Thalamocortical Loop in the Spontaneous Switching of Percepts in Auditory Streaming , 2009, The Journal of Neuroscience.

[20]  Sabine Kastner,et al.  Neural correlates of binocular rivalry in the human lateral geniculate nucleus , 2005, Nature Neuroscience.

[21]  Andrew J Oxenham,et al.  Human Cortical Activity during Streaming without Spectral Cues Suggests a General Neural Substrate for Auditory Stream Segregation , 2007, The Journal of Neuroscience.

[22]  Robert Tibshirani,et al.  An Introduction to the Bootstrap , 1994 .

[23]  A. Dale,et al.  Selective averaging of rapidly presented individual trials using fMRI , 1997, Human brain mapping.

[24]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[25]  Nobuo Suga,et al.  Multiparametric corticofugal modulation and plasticity in the auditory system , 2003, Nature Reviews Neuroscience.

[26]  Victoria M Bajo,et al.  The descending corticocollicular pathway mediates learning-induced auditory plasticity , 2010, Nature Neuroscience.

[27]  I. Winter,et al.  Descending projections from auditory brainstem nuclei to the cochlea and cochlear nucleus of the guinea pig , 1989, The Journal of comparative neurology.

[28]  Mikko Sams,et al.  Auditory selective attention modulates activation of human inferior colliculus. , 2008, Journal of neurophysiology.

[29]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[30]  Alan R Palmer,et al.  Reassessing mechanisms of low-frequency sound localisation , 2004, Current Opinion in Neurobiology.

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

[32]  G. A. Miller,et al.  The Trill Threshold , 1950 .

[33]  Andrew J Oxenham,et al.  Cortical FMRI activation to sequences of tones alternating in frequency: relationship to perceived rate and streaming. , 2007, Journal of neurophysiology.

[34]  D. Pressnitzer,et al.  Perceptual Organization of Sound Begins in the Auditory Periphery , 2008, Current Biology.

[35]  R. Deichmann,et al.  Eye-specific effects of binocular rivalry in the human lateral geniculate nucleus , 2005, Nature.

[36]  L. V. Noorden Temporal coherence in the perception of tone sequences , 1975 .

[37]  M. Harms,et al.  Sound repetition rate in the human auditory pathway: representations in the waveshape and amplitude of fMRI activation. , 2002, Journal of neurophysiology.

[38]  A. M. Dale,et al.  A hybrid approach to the skull stripping problem in MRI , 2004, NeuroImage.

[39]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[40]  Stuart Anstis,et al.  Adaptation to auditory streaming of frequency-modulated tones. , 1985 .

[41]  Richard S. J. Frackowiak,et al.  Representation of the temporal envelope of sounds in the human brain. , 2000, Journal of neurophysiology.