Spectral and temporal modulation tradeoff in the inferior colliculus.

The cochlea encodes sounds through frequency-selective channels that exhibit low-pass modulation sensitivity. Unlike the cochlea, neurons in the auditory midbrain are tuned for spectral and temporal modulations found in natural sounds, yet the role of this transformation is not known. We report a distinct tradeoff in modulation sensitivity and tuning that is topographically ordered within the central nucleus of the inferior colliculus (CNIC). Spectrotemporal receptive fields (STRFs) were obtained with 16-channel electrodes inserted orthogonal to the isofrequency lamina. Surprisingly, temporal and spectral characteristics exhibited an opposing relationship along the tonotopic axis. For low best frequencies (BFs), units were selective for fast temporal and broad spectral modulations. A systematic progression was observed toward slower temporal and finer spectral modulation sensitivity at high BF. This tradeoff was strongly reflected in the arrangement of excitation and inhibition and, consequently, in the modulation tuning characteristics. Comparisons with auditory nerve fibers show that these trends oppose the pattern imposed by the peripheral filters. These results suggest that spectrotemporal preferences are reordered within the tonotopic axis of the CNIC. This topographic organization has profound implications for the coding of spectrotemporal features in natural sounds and could underlie a number of perceptual phenomena.

[1]  M. Malmierca,et al.  Stimulus-Specific Adaptation in the Inferior Colliculus of the Anesthetized Rat , 2009, The Journal of Neuroscience.

[2]  J. Borst,et al.  Intracellular responses of neurons in the mouse inferior colliculus to sinusoidal amplitude-modulated tones. , 2009, Journal of neurophysiology.

[3]  M. Escabí,et al.  Distinct Roles for Onset and Sustained Activity in the Neuronal Code for Temporal Periodicity and Acoustic Envelope Shape , 2008, The Journal of Neuroscience.

[4]  John C. Middlebrooks,et al.  Intraneural stimulation for auditory prosthesis: Modiolar trunk and intracranial stimulation sites , 2008, Hearing Research.

[5]  M. Malmierca,et al.  The cytoarchitecture of the inferior colliculus revisited: A common organization of the lateral cortex in rat and cat , 2008, Neuroscience.

[6]  N. Lesica,et al.  Dynamic Spectrotemporal Feature Selectivity in the Auditory Midbrain , 2008, The Journal of Neuroscience.

[7]  P. Joris,et al.  Comparison of bandwidths in the inferior colliculus and the auditory nerve. II: Measurement using a temporally manipulated stimulus. , 2007, Journal of neurophysiology.

[8]  M. Semple,et al.  Transformation of Temporal Properties between Auditory Midbrain and Cortex in the Awake Mongolian Gerbil , 2007, The Journal of Neuroscience.

[9]  Na Li,et al.  Spectrotemporal Receptive Fields in the Inferior Colliculus Revealing Selectivity for Spectral Motion in Conspecific Vocalizations , 2007, The Journal of Neuroscience.

[10]  Katherine I. Nagel,et al.  Temporal Processing and Adaptation in the Songbird Auditory Forebrain , 2006, Neuron.

[11]  K. Nataraj,et al.  Roles of inhibition in complex auditory responses in the inferior colliculus: inhibited combination-sensitive neurons. , 2006, Journal of neurophysiology.

[12]  R. Batra,et al.  Sensitivity to interaural time differences in the dorsal nucleus of the lateral lemniscus of the unanesthetized rabbit: comparison with other structures. , 2006, Journal of neurophysiology.

[13]  M. Malmierca,et al.  Laminar inputs from dorsal cochlear nucleus and ventral cochlear nucleus to the central nucleus of the inferior colliculus: Two patterns of convergence , 2005, Neuroscience.

[14]  Lee M. Miller,et al.  The Contribution of Spike Threshold to Acoustic Feature Selectivity, Spike Information Content, and Information Throughput , 2005, The Journal of Neuroscience.

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

[16]  C. Schreiner,et al.  Short-term adaptation of auditory receptive fields to dynamic stimuli. , 2004, Journal of neurophysiology.

[17]  Lee M. Miller,et al.  Naturalistic Auditory Contrast Improves Spectrotemporal Coding in the Cat Inferior Colliculus , 2003, The Journal of Neuroscience.

[18]  N. C. Singh,et al.  Modulation spectra of natural sounds and ethological theories of auditory processing. , 2003, The Journal of the Acoustical Society of America.

[19]  Günter Ehret,et al.  Spatial map of frequency tuning‐curve shapes in the mouse inferior colliculus , 2003, Neuroreport.

[20]  John C Middlebrooks,et al.  Vertical-plane sound localization probed with ripple-spectrum noise. , 2003, The Journal of the Acoustical Society of America.

[21]  C. Schreiner,et al.  Gabor analysis of auditory midbrain receptive fields: spectro-temporal and binaural composition. , 2003, Journal of neurophysiology.

[22]  Daniel J Tollin,et al.  Spectral cues explain illusory elevation effects with stereo sounds in cats. , 2003, Journal of neurophysiology.

[23]  J. Kelly,et al.  Glutamatergic and GABAergic regulation of neural responses in inferior colliculus to amplitude-modulated sounds. , 2003, Journal of neurophysiology.

[24]  G. Langner,et al.  Temporal and spatial coding of periodicity information in the inferior colliculus of awake chinchilla (Chinchilla laniger) , 2002, Hearing Research.

[25]  C. Schreiner,et al.  Nonlinear Spectrotemporal Sound Analysis by Neurons in the Auditory Midbrain , 2002, The Journal of Neuroscience.

[26]  J. C. Middlebrooks,et al.  Listener weighting of cues for lateral angle: the duplex theory of sound localization revisited. , 2002, The Journal of the Acoustical Society of America.

[27]  Michael S. Lewicki,et al.  Efficient coding of natural sounds , 2002, Nature Neuroscience.

[28]  Manuel S. Malmierca,et al.  Iontophoresis In Vivo Demonstrates a Key Role for GABAA and Glycinergic Inhibition in Shaping Frequency Response Areas in the Inferior Colliculus of Guinea Pig , 2001, The Journal of Neuroscience.

[29]  D. Oliver Ascending efferent projections of the superior olivary complex , 2000, Microscopy research and technique.

[30]  C H Keller,et al.  Representation of temporal features of complex sounds by the discharge patterns of neurons in the owl's inferior colliculus. , 2000, Journal of neurophysiology.

[31]  E D Young,et al.  Linear and nonlinear pathways of spectral information transmission in the cochlear nucleus. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[32]  J. H. Casseday,et al.  Neural measurement of sound duration: control by excitatory-inhibitory interactions in the inferior colliculus. , 2000, Journal of neurophysiology.

[33]  Matthew C. Guyton,et al.  Spectro-temporal modulation transfer functions and speech intelligibility. , 1999, The Journal of the Acoustical Society of America.

[34]  R. Batra,et al.  Discharge patterns of neurons in the ventral nucleus of the lateral lemniscus of the unanesthetized rabbit. , 1999, Journal of neurophysiology.

[35]  K. A. Davis,et al.  Single-unit responses in the inferior colliculus of decerebrate cats. I. Classification based on frequency response maps. , 1999, Journal of neurophysiology.

[36]  H. Steven Colburn,et al.  Role of spectral detail in sound-source localization , 1998, Nature.

[37]  Hagai Attias,et al.  Coding of Naturalistic Stimuli by Auditory Midbrain Neurons , 1997, NIPS.

[38]  S Kuwada,et al.  Intracellular Recordings in Response to Monaural and Binaural Stimulation of Neurons in the Inferior Colliculus of the Cat , 1997, The Journal of Neuroscience.

[39]  Gerald Langner,et al.  Laminar fine structure of frequency organization in auditory midbrain , 1997, Nature.

[40]  Hagai Attias,et al.  Temporal Low-Order Statistics of Natural Sounds , 1996, NIPS.

[41]  P. Joris Envelope coding in the lateral superior olive. II. Characteristic delays and comparison with responses in the medial superior olive. , 1996, Journal of neurophysiology.

[42]  T. Irino,et al.  Temporal asymmetry in the auditory system. , 1996, The Journal of the Acoustical Society of America.

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

[44]  W. S. Rhode Interspike intervals as a correlate of periodicity pitch in cat cochlear nucleus. , 1995, The Journal of the Acoustical Society of America.

[45]  T. Blackstad,et al.  The central nucleus of the inferior colliculus in rat: A Golgi and computer reconstruction study of neuronal and laminar structure , 1993, The Journal of comparative neurology.

[46]  L. Robles,et al.  Two-tone suppression in the basilar membrane of the cochlea: mechanical basis of auditory-nerve rate suppression. , 1992, Journal of neurophysiology.

[47]  E D Young,et al.  Organization of dorsal cochlear nucleus type IV unit response maps and their relationship to activation by bandlimited noise. , 1991, Journal of neurophysiology.

[48]  A. Rees,et al.  Neuronal responses to amplitude-modulated and pure-tone stimuli in the guinea pig inferior colliculus, and their modification by broadband noise. , 1989, The Journal of the Acoustical Society of America.

[49]  R. Batra,et al.  Temporal coding of envelopes and their interaural delays in the inferior colliculus of the unanesthetized rabbit. , 1989, Journal of neurophysiology.

[50]  C. Schreiner,et al.  Periodicity coding in the inferior colliculus of the cat. II. Topographical organization. , 1988, Journal of neurophysiology.

[51]  C. Schreiner,et al.  Periodicity coding in the inferior colliculus of the cat. I. Neuronal mechanisms. , 1988, Journal of neurophysiology.

[52]  M. Merzenich,et al.  Covariation of latency and temporal resolution in the inferior colliculus of the cat , 1987, Hearing Research.

[53]  C V Pavlovic,et al.  Derivation of primary parameters and procedures for use in speech intelligibility predictions. , 1987, The Journal of the Acoustical Society of America.

[54]  A. Palmer,et al.  Phase-locking in the cochlear nerve of the guinea-pig and its relation to the receptor potential of inner hair-cells , 1986, Hearing Research.

[55]  T Houtgast,et al.  Spectral sharpness and vowel dissimilarity. , 1985, The Journal of the Acoustical Society of America.

[56]  Adrian Rees,et al.  Responses of neurons in the inferior colliculus of the rat to AM and FM tones , 1983, Hearing Research.

[57]  M. S. Keshner 1/f noise , 1982, Proceedings of the IEEE.

[58]  M N Semple,et al.  Representation of sound frequency and laterality by units in central nucleus of cat inferior colliculus. , 1979, Journal of neurophysiology.

[59]  J. Adams Ascending projections to the inferior colliculus , 1979, The Journal of comparative neurology.

[60]  R. Voss,et al.  ‘1/fnoise’ in music and speech , 1975, Nature.

[61]  M M Merzenich,et al.  Representation of the cochlea within the inferior colliculus of the cat. , 1974, Brain research.

[62]  J. L. Goldstein An optimum processor theory for the central formation of the pitch of complex tones. , 1973, The Journal of the Acoustical Society of America.

[63]  J. C. Steinberg,et al.  Factors Governing the Intelligibility of Speech Sounds , 1945 .

[64]  S. Ewert,et al.  Transformation of Temporal Properties between Auditory Midbrain and Cortex in the Injections, Tones of Different Durations, and Sinusoidal Amplitude-modulated Tones Comparison of Responses of Neurons in the Mouse Inferior Colliculus to Current Cortex Conductive Hearing Loss Disrupts Synaptic and Spi , 2008 .

[65]  P. Joris,et al.  Comparison of bandwidths in the inferior colliculus and the auditory nerve. I. Measurement using a spectrally manipulated stimulus. , 2007, Journal of neurophysiology.

[66]  Khaled H. Hamed,et al.  Time-frequency analysis , 2003 .

[67]  Lee M. Miller,et al.  Spectrotemporal receptive fields in the lemniscal auditory thalamus and cortex. , 2002, Journal of neurophysiology.

[68]  E D Young,et al.  Comparative analysis of spectro-temporal receptive fields, reverse correlation functions, and frequency tuning curves of auditory-nerve fibers. , 1994, The Journal of the Acoustical Society of America.

[69]  T. Yin,et al.  Responses to amplitude-modulated tones in the auditory nerve of the cat. , 1992, The Journal of the Acoustical Society of America.

[70]  R. Plomp The Role of Modulation in Hearing , 1983 .

[71]  N. Kiang,et al.  Acoustic trauma in cats. Cochlear pathology and auditory-nerve activity. , 1978, Acta oto-laryngologica. Supplementum.

[72]  Dennis Gabor,et al.  Theory of communication , 1946 .