Responses of auditory cortex to complex stimuli: functional organization revealed using intrinsic optical signals.

We used optical imaging of intrinsic signals to study the large-scale organization of ferret auditory cortex in response to complex sounds. Cortical responses were collected during continuous stimulation by sequences of sounds with varying frequency, period, or interaural level differences. We used a set of stimuli that differ in spectral structure, but have the same periodicity and therefore evoke the same pitch percept (click trains, sinusoidally amplitude modulated tones, and iterated ripple noise). These stimuli failed to reveal a consistent periodotopic map across the auditory fields imaged. Rather, gradients of period sensitivity differed for the different types of periodic stimuli. Binaural interactions were studied both with single contralateral, ipsilateral, and diotic broadband noise bursts and with sequences of broadband noise bursts with varying level presented contralaterally, ipsilaterally, or in opposite phase to both ears. Contralateral responses were generally largest and ipsilateral responses were smallest when using single noise bursts, but the extent of the activated area was large and comparable in all three aural configurations. Modulating the amplitude in counter phase to the two ears generally produced weaker modulation of the optical signals than the modulation produced by the monaural stimuli. These results suggest that binaural interactions seen in cortex are most likely predominantly due to subcortical processing. Thus our optical imaging data do not support the theory that the primary or nonprimary cortical fields imaged are topographically organized to form consistent maps of systematically varying sensitivity either to stimulus pitch or to simple binaural properties of the acoustic stimuli.

[1]  M. Semple,et al.  Binaural processing of sound pressure level in cat primary auditory cortex: evidence for a representation based on absolute levels rather than interaural level differences. , 1993, Journal of neurophysiology.

[2]  Gal Chechik,et al.  Encoding Stimulus Information by Spike Numbers and Mean Response Time in Primary Auditory Cortex , 2005, Journal of Computational Neuroscience.

[3]  J. Kelly,et al.  Organization of auditory cortex in the albino rat: binaural response properties. , 1988, Journal of neurophysiology.

[4]  Quantifying the distortion products generated by amplitude-modulated noise. , 1999, The Journal of the Acoustical Society of America.

[5]  Ernst Terhardt,et al.  Binaural fusion and the representation of virtual pitch in the human auditory cortex , 1996, Hearing Research.

[6]  J. Pettigrew,et al.  Spontaneous and stimulus-evoked intrinsic optical signals in primary auditory cortex of the cat. , 2001, Journal of neurophysiology.

[7]  J. C. Middlebrooks,et al.  Binaural response-specific bands in primary auditory cortex (AI) of the cat: Topographical organization orthogonal to isofrequency contours , 1980, Brain Research.

[8]  D. P. Phillips,et al.  Intracortical connections and their physiological correlates in the primary auditory cortex (AI) of the cat , 1988, The Journal of comparative neurology.

[9]  Israel Nelken,et al.  Relating cluster and population responses to natural sounds and tonal stimuli in cat primary auditory cortex , 2001, Hearing Research.

[10]  Robert V. Harrison,et al.  Three Distinct Auditory Areas of Cortex (AI, AII, and AAF) Defined by Optical Imaging of Intrinsic Signals , 2000, NeuroImage.

[11]  Holger Schulze,et al.  Superposition of horseshoe‐like periodicity and linear tonotopic maps in auditory cortex of the Mongolian gerbil , 2002, The European journal of neuroscience.

[12]  Ben Godde,et al.  Optical Imaging of Cat Auditory Cortex Cochleotopic Selectivity Evoked by Acute Electrical Stimulation of a Multi‐channel Cochlear Implant , 1997, The European journal of neuroscience.

[13]  J. Kelly,et al.  Binaural organization of primary auditory cortex in the ferret (Mustela putorius). , 1994, Journal of Neurophysiology.

[14]  R E Kettner,et al.  Topography of binaural organization in primary auditory cortex of the cat: effects of changing interaural intensity. , 1986, Journal of neurophysiology.

[15]  Gal Chechik,et al.  Reduction of Information Redundancy in the Ascending Auditory Pathway , 2006, Neuron.

[16]  M. Stryker,et al.  Fine functional organization of auditory cortex revealed by Fourier optical imaging. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Christoph E Schreiner,et al.  Order and disorder in auditory cortical maps , 1995, Current Opinion in Neurobiology.

[18]  D. McAlpine Neural sensitivity to periodicity in the inferior colliculus: evidence for the role of cochlear distortions. , 2004, Journal of neurophysiology.

[19]  P. Heil,et al.  Parallels between timing of onset responses of single neurons in cat and of evoked magnetic fields in human auditory cortex. , 2000, Journal of neurophysiology.

[20]  B Lütkenhöner,et al.  Neuromagnetic evidence for a pitch processing center in Heschl's gyrus. , 2003, Cerebral cortex.

[21]  Israel Nelken,et al.  Large-scale organization of ferret auditory cortex revealed using continuous acquisition of intrinsic optical signals. , 2004, Journal of neurophysiology.

[22]  P. Heil,et al.  Frequency and periodicity are represented in orthogonal maps in the human auditory cortex: evidence from magnetoencephalography , 1997, Journal of Comparative Physiology A.

[23]  Robert V. Harrison,et al.  Optical Imaging of Intrinsic Signals in Chinchilla Auditory Cortex , 1998, Audiology and Neurotology.

[24]  Christoph E Schreiner Functional organization of the auditory cortex: Maps and mechanisms , 1992, Current Biology.

[25]  A Hess,et al.  Optical and FDG mapping of frequency-specific activity in auditory cortex. , 1996, Neuroreport.

[26]  Xiaoqin Wang,et al.  Neural representations of temporally asymmetric stimuli in the auditory cortex of awake primates. , 2001, Journal of neurophysiology.

[27]  N. Harel,et al.  Blood capillary distribution correlates with hemodynamic-based functional imaging in cerebral cortex. , 2002, Cerebral cortex.

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

[29]  T. Imig,et al.  Binaural columns in the primary field (A1) of cat auditory cortex , 1977, Brain Research.

[30]  L. Demany,et al.  The Upper Limit of "Musical" Pitch , 1990 .

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

[32]  D. Ts'o,et al.  Cortical functional architecture and local coupling between neuronal activity and the microcirculation revealed by in vivo high-resolution optical imaging of intrinsic signals. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[33]  J. Bakin,et al.  Suprathreshold auditory cortex activation visualized by intrinsic signal optical imaging. , 1996, Cerebral cortex.

[34]  Michael P. Stryker,et al.  New Paradigm for Optical Imaging Temporally Encoded Maps of Intrinsic Signal , 2003, Neuron.

[35]  David R Moore,et al.  Optical imaging of intrinsic signals in ferret auditory cortex: responses to narrowband sound stimuli. , 2002, Journal of neurophysiology.

[36]  G. Recanzone,et al.  Functional organization of spectral receptive fields in the primary auditory cortex of the owl monkey , 1999, The Journal of comparative neurology.

[37]  Alan R Palmer,et al.  Organisation of binaural interactions in the primary and dorsocaudal fields of the guinea pig auditory cortex , 2000, Hearing Research.

[38]  Xiaoqin Wang,et al.  Sustained firing in auditory cortex evoked by preferred stimuli , 2005, Nature.

[39]  M N Semple,et al.  Focal selectivity for binaural sound pressure level in cat primary auditory cortex: two-way intensity network tuning. , 1993, Journal of neurophysiology.

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

[41]  J. B. Kelly,et al.  Primary auditory cortex in the ferret (Mustela putorius): neural response properties and topographic organization , 1988, Brain Research.

[42]  R. Patterson,et al.  The lower limit of melodic pitch. , 2001, The Journal of the Acoustical Society of America.

[43]  I. Nelken,et al.  Representation of Tone in Fluctuating Maskers in the Ascending Auditory System , 2005, The Journal of Neuroscience.

[44]  P. Heil Representation of Sound Onsets in the Auditory System , 2001, Audiology and Neurotology.

[45]  Dennis L Barbour,et al.  Temporal coherence sensitivity in auditory cortex. , 2002, Journal of neurophysiology.

[46]  I. Nelken,et al.  Processing of low-probability sounds by cortical neurons , 2003, Nature Neuroscience.

[47]  I. Nelken,et al.  Functional organization of ferret auditory cortex. , 2005, Cerebral cortex.

[48]  I. Nelken,et al.  Responses of Neurons in Cat Primary Auditory Cortex to Bird Chirps: Effects of Temporal and Spectral Context , 2002, The Journal of Neuroscience.

[49]  W A Yost,et al.  A time domain description for the pitch strength of iterated rippled noise. , 1996, The Journal of the Acoustical Society of America.

[50]  Robert A. A. Campbell,et al.  Binaural-level functions in ferret auditory cortex: evidence for a continuous distribution of response properties. , 2006, Journal of neurophysiology.

[51]  R. Patterson,et al.  The lower limit of pitch as determined by rate discrimination. , 2000, The Journal of the Acoustical Society of America.

[52]  Huib Versnel,et al.  Development of contralateral and ipsilateral frequency representations in ferret primary auditory cortex , 2006, The European journal of neuroscience.