Cellular Mechanisms for Information Coding in Auditory Brainstem Nuclei

The brainstem auditory nuclei carry out a wide variety of transformations of the signals carried by the auditory nerve. Although basic frequency and intensity information is first encoded in the cochlea, brainstem circuitry must perform further neural definitions and refinements of these parameters, as well as integrate the cues necessary for the localization of sounds in space. Each of these aspects is associated not just with certain cell types, morphologies, and synaptic connections, but with cells having characteristic electrical response profiles. Such response properties are an outcome of the complement of ion channels that the cells possess and of the dynamic properties of the synapses through which cells communicate.

[1]  Nace L. Golding,et al.  Physiological identification of the targets of cartwheel cells in the dorsal cochlear nucleus. , 1997, Journal of neurophysiology.

[2]  B. Sakmann,et al.  Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS , 1995, Neuron.

[3]  E. Evans,et al.  Neuropharmacological and Neurophysiological Dissection of Inhibition in the Mammalian Dorsal Cochlear Nucleus , 1993 .

[4]  B. Katz,et al.  Quantal components of the end‐plate potential , 1954, The Journal of physiology.

[5]  Nace L. Golding,et al.  Synaptic inputs to stellate cells in the ventral cochlear nucleus. , 1998, Journal of neurophysiology.

[6]  L. Trussell,et al.  Delayed clearance of transmitter and the role of glutamate transporters at synapses with multiple release sites , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  P. Jonas,et al.  Ionotropic Glutamate Receptors in the CNS , 1999, Handbook of Experimental Pharmacology.

[8]  L. Trussell,et al.  A characterization of excitatory postsynaptic potentials in the avian nucleus magnocellularis. , 1994, Journal of neurophysiology.

[9]  R. Helfert,et al.  GABA and Glycine Inputs Control Discharge Rate within the Excitatory Response Area of Primary-Like and Phase-Locked AVCN Neurons , 1993 .

[10]  D. Caspary,et al.  Inhibitory inputs modulate discharge rate within frequency receptive fields of anteroventral cochlear nucleus neurons. , 1994, Journal of neurophysiology.

[11]  J. Borst,et al.  The Reduced Release Probability of Releasable Vesicles during Recovery from Short-Term Synaptic Depression , 1999, Neuron.

[12]  Leonard K. Kaczmarek,et al.  High-frequency firing helps replenish the readily releasable pool of synaptic vesicles , 1998, Nature.

[13]  H. Brew,et al.  Differential expression of voltage-gated potassium channel genes in auditory nuclei of the mouse brainstem , 2000, Hearing Research.

[14]  D. Ryugo,et al.  Endbulbs of held and spherical bushy cells in cats: Morphological correlates with physiological properties , 1989, The Journal of comparative neurology.

[15]  T. Moser,et al.  Kinetics of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse of the mouse. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[16]  I. Raman,et al.  AMPA receptors with high Ca2+ permeability mediate synaptic transmission in the avian auditory pathway. , 1995, The Journal of physiology.

[17]  Donata Oertel,et al.  Correlation of AMPA Receptor Subunit Composition with Synaptic Input in the Mammalian Cochlear Nuclei , 2001, The Journal of Neuroscience.

[18]  W. S. Rhode,et al.  Structural and functional properties distinguish two types of multipolar cells in the ventral cochlear nucleus , 1989, The Journal of comparative neurology.

[19]  I. Forsythe,et al.  The binaural auditory pathway: excitatory amino acid receptors mediate dual timecourse excitatory postsynaptic currents in the rat medial nucleus of the trapezoid body , 1993, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[20]  L. Trussell,et al.  Long-Term Specification of AMPA Receptor Properties after Synapse Formation , 2000, The Journal of Neuroscience.

[21]  P. Monsivais,et al.  The Superior Olivary Nucleus and Its Influence on Nucleus Laminaris: A Source of Inhibitory Feedback for Coincidence Detection in the Avian Auditory Brainstem , 1999, The Journal of Neuroscience.

[22]  E. Mugnaini,et al.  The Mammalian Cochlear Nuclei , 1993, NATO ASI series.

[23]  W. S. Rhode,et al.  Physiological response properties of cells labeled intracellularly with horseradish peroxidase in cat ventral cochlear nucleus , 1983, The Journal of comparative neurology.

[24]  J. McGee,et al.  Contributions of ion conductances to the onset responses of octopus cells in the ventral cochlear nucleus: simulation results. , 2000, Journal of neurophysiology.

[25]  I. Raman,et al.  Pathway-specific variants of AMPA receptors and their contribution to neuronal signaling , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  W. Shofner,et al.  Regularity and latency of units in ventral cochlear nucleus: implications for unit classification and generation of response properties. , 1988, Journal of neurophysiology.

[27]  G. Westbrook,et al.  Channel kinetics determine the time course of NMDA receptor-mediated synaptic currents , 1990, Nature.

[28]  B. Grothe,et al.  Bilateral inhibition by glycinergic afferents in the medial superior olive. , 1993, Journal of neurophysiology.

[29]  D. Oertel,et al.  Hyperpolarization-activated, mixed-cation current (I(h)) in octopus cells of the mammalian cochlear nucleus. , 2000, Journal of neurophysiology.

[30]  E. C. Kane,et al.  Octopus cells in the cochlear nucleus of the cat: heterotypic synapses upon homeotypic neurons. , 1973, The International journal of neuroscience.

[31]  M. Hollmann Structure of Ionotropic Glutamate Receptors , 1999 .

[32]  E. Puil,et al.  Membrane properties that shape the auditory code in three nuclei of the central nervous system. , 1998, The Journal of otolaryngology.

[33]  E. Rouiller,et al.  Intracellular marking of physiologically characterized cells in the ventral cochlear nucleus of the cat , 1984, The Journal of comparative neurology.

[34]  J. Boudreau,et al.  Encoding of stimulus frequency and intensity by cat superior olive S-segment cells. , 1967, The Journal of the Acoustical Society of America.

[35]  Peter Dallos,et al.  Neural coding in the chick cochlear nucleus , 1990, Journal of Comparative Physiology A.

[36]  E. Rubel,et al.  Organization and development of brain stem auditory nuclei of the chicken: Tonotopic organization of N. magnocellularis and N. laminaris , 1975, The Journal of comparative neurology.

[37]  H. Monyer,et al.  A molecular determinant for submillisecond desensitization in glutamate receptors. , 1994, Science.

[38]  K K Osen,et al.  Cytoarchitecture of the cochlear nuclei in the cat , 1969 .

[39]  M. Konishi,et al.  A circuit for detection of interaural time differences in the brain stem of the barn owl , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  J. Kauer,et al.  Whole-Cell Patch-Clamp Recording Reveals Subthreshold Sound-Evoked Postsynaptic Currents in the Inferior Colliculus of Awake Bats , 1996, The Journal of Neuroscience.

[41]  L. Trussell,et al.  Inhibitory Transmission Mediated by Asynchronous Transmitter Release , 2000, Neuron.

[42]  W. S. Rhode,et al.  Encoding timing and intensity in the ventral cochlear nucleus of the cat. , 1986, Journal of neurophysiology.

[43]  Hannah Monyer,et al.  Functional and Molecular Differences between Voltage-Gated K+ Channels of Fast-Spiking Interneurons and Pyramidal Neurons of Rat Hippocampus , 1998, The Journal of Neuroscience.

[44]  R. Altschuler,et al.  Diversity and plasticity in amino acid receptor subunits in the rat auditory brain stem , 2000, Hearing Research.

[45]  T. Yin,et al.  Interaural time sensitivity in medial superior olive of cat. , 1990, Journal of neurophysiology.

[46]  L. Kaczmarek,et al.  Localization of a high threshold potassium channel in the rat cochlear nucleus , 1997, The Journal of comparative neurology.

[47]  E. Young,et al.  The electrotonic structure of regular-spiking neurons in the ventral cochlear nucleus may determine their response properties. , 1994, Journal of neurophysiology.

[48]  M. Nadler,et al.  Presynaptic glycine receptors enhance transmitter release at a mammalian central synapse , 2022 .

[49]  I. Forsythe,et al.  Characterisation of inhibitory and excitatory postsynaptic currents of the rat medial superior olive , 2000, The Journal of physiology.

[50]  D. Oertel,et al.  Context-dependent synaptic action of glycinergic and GABAergic inputs in the dorsal cochlear nucleus , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[51]  R. Petralia,et al.  Ionotropic and metabotropic glutamate receptors show unique postsynaptic, presynaptic, and glial localizations in the dorsal cochlear nucleus , 1996, The Journal of comparative neurology.

[52]  G D Pollak,et al.  Multiple components of ipsilaterally evoked inhibition in the inferior colliculus. , 1999, Journal of neurophysiology.

[53]  W G Regehr,et al.  Calcium Dependence and Recovery Kinetics of Presynaptic Depression at the Climbing Fiber to Purkinje Cell Synapse , 1998, The Journal of Neuroscience.

[54]  D. Taylor,et al.  Cobalt-permeable non-NMDA receptors in developing chick brainstem auditory nuclei. , 1995, Neuroreport.

[55]  A. Erisir,et al.  Function of specific K(+) channels in sustained high-frequency firing of fast-spiking neocortical interneurons. , 1999, Journal of neurophysiology.

[56]  J. Kelly,et al.  Synaptic pharmacology of the superior olivary complex studied in mouse brain slice , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[57]  H. von Gersdorff,et al.  Fine-Tuning an Auditory Synapse for Speed and Fidelity: Developmental Changes in Presynaptic Waveform, EPSC Kinetics, and Synaptic Plasticity , 2000, The Journal of Neuroscience.

[58]  Russell R. Pfeiffer,et al.  Classification of response patterns of spike discharges for units in the cochlear nucleus: Tone-burst stimulation , 2004, Experimental Brain Research.

[59]  D. Oertel Synaptic responses and electrical properties of cells in brain slices of the mouse anteroventral cochlear nucleus , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[60]  W. S. Rhode,et al.  Characterization of HRP‐labeled globular bushy cells in the cat anteroventral cochlear nucleus , 1987, The Journal of comparative neurology.

[61]  A. Rodríguez-Moreno,et al.  Kainate Receptors Presynaptically Downregulate GABAergic Inhibition in the Rat Hippocampus , 1997, Neuron.

[62]  R. Wickesberg,et al.  Tuberculoventral neurons project to the multipolar cell area but not to the octopus cell area of the posteroventral cochlear nucleus , 1991, The Journal of comparative neurology.

[63]  M. Sachs,et al.  Regularity analysis in a compartmental model of chopper units in the anteroventral cochlear nucleus. , 1991, Journal of neurophysiology.

[64]  Paul B. Manis,et al.  Transient Potassium Currents Regulate the Discharge Patterns of Dorsal Cochlear Nucleus Pyramidal Cells , 1999, The Journal of Neuroscience.

[65]  J. Rothman,et al.  Convergence of auditory nerve fibers onto bushy cells in the ventral cochlear nucleus: implications of a computational model. , 1993, Journal of neurophysiology.

[66]  C E Carr,et al.  Processing of temporal information in the brain. , 1993, Annual review of neuroscience.

[67]  A. C. Meyer,et al.  Released Fraction and Total Size of a Pool of Immediately Available Transmitter Quanta at a Calyx Synapse , 1999, Neuron.

[68]  T. Otis,et al.  Direct Measurement of AMPA Receptor Desensitization Induced by Glutamatergic Synaptic Transmission , 1996, The Journal of Neuroscience.

[69]  W. S. Rhode,et al.  Physiological response properties of cells labeled intracellularly with horseradish peroxidase in cat dorsal cochlear nucleus , 1983, The Journal of comparative neurology.

[70]  A. Reyes,et al.  Membrane properties underlying the firing of neurons in the avian cochlear nucleus , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[71]  C D Geisler,et al.  A two-stage nonlinear cochlear model possesses automatic gain control. , 1986, The Journal of the Acoustical Society of America.

[72]  Nace L. Golding,et al.  Recordings from slices indicate that octopus cells of the cochlear nucleus detect coincident firing of auditory nerve fibers with temporal precision , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[73]  R. L. Marie,et al.  Glycine immunoreactive projections from the dorsal to the anteroventral cochlear nucleus , 1991, Hearing Research.

[74]  A Greig,et al.  Contrasting molecular composition and channel properties of AMPA receptors on chick auditory and brainstem motor neurons , 2000, The Journal of physiology.

[75]  S. Wu,et al.  Glutamate receptors underlying excitatory synaptic transmission in the rat's lateral superior olive studied in vitro , 1998, Hearing Research.

[76]  J. Kelly,et al.  Binaural interaction in the lateral superior olive: time difference sensitivity studied in mouse brain slice. , 1992, Journal of neurophysiology.

[77]  D. Faber,et al.  Properties and Plasticity of Paired-Pulse Depression at a Central Synapse , 2000, The Journal of Neuroscience.

[78]  E. Mroz,et al.  Purification of a low-molecular-weight excitatory substance from the inner ears of goldfish , 1990, Hearing Research.

[79]  B. Walmsley,et al.  Receptors underlying excitatory synaptic transmission in slices of the rat anteroventral cochlear nucleus. , 1995, Journal of neurophysiology.

[80]  L. Trussell,et al.  Time Course and Permeation of Synaptic AMPA Receptors in Cochlear Nuclear Neurons Correlate with Input , 1999, The Journal of Neuroscience.

[81]  L. Trussell,et al.  Characterization of outward currents in neurons of the avian nucleus magnocellularis. , 1998, Journal of neurophysiology.

[82]  J. Guinan,et al.  Signal processing in brainstem auditory neurons which receive giant endings (calyces of Held) in the medial nucleus of the trapezoid body of the cat , 1990, Hearing Research.

[83]  M. Mayer,et al.  Structure-activity relationships for amino acid transmitter candidates acting at N-methyl-D-aspartate and quisqualate receptors , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[84]  R. Petralia,et al.  Endbulb Synapses in the Anteroventral Cochlear Nucleus Express a Specific Subset of AMPA-Type Glutamate Receptor Subunits , 1998, The Journal of Neuroscience.

[85]  B. Sakmann,et al.  Flip and flop: a cell-specific functional switch in glutamate-operated channels of the CNS. , 1990, Science.

[86]  V. Kotak,et al.  A Developmental Shift from GABAergic to Glycinergic Transmission in the Central Auditory System , 1998, The Journal of Neuroscience.

[87]  E. Ostapoff,et al.  Uptake and retrograde transport of [3H]GABA from the cochlear nucleus to the superior olive in the guinea pig. , 1990, Journal of chemical neuroanatomy.

[88]  P. Manis,et al.  Outward currents in isolated ventral cochlear nucleus neurons , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[89]  E. Friauf,et al.  Development and influence of inhibition in the lateral superior olivary nucleus , 2000, Hearing Research.

[90]  D. Oertel,et al.  Inhibitory circuitry in the ventral cochlear nucleus is probably mediated by glycine , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[91]  R. Wenthold,et al.  Glutamate Receptors Are Selectively Targeted to Postsynaptic Sites in Neurons , 1997, Neuron.

[92]  Philip H Smith,et al.  Projections of physiologically characterized spherical bushy cell axons from the cochlear nucleus of the cat: Evidence for delay lines to the medial superior olive , 1993, The Journal of comparative neurology.

[93]  B. Sakmann,et al.  Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches , 1981, Pflügers Archiv.

[94]  L. Kaczmarek,et al.  Expression of the mRNAs for the Kv3.1 potassium channel gene in the adult and developing rat brain. , 1992, Journal of neurophysiology.

[95]  Mario A. Ruggero,et al.  Physiology and Coding of Sound in the Auditory Nerve , 1992 .

[96]  S. Jhaveri,et al.  Neuronal architecture in nucleus magnocellularis of the chicken auditory system with observations on nucleus laminaris: A light and electron microscope study , 1982, Neuroscience.

[97]  J. A. Hirsch,et al.  Intrinsic properties of neurones in the dorsal cochlear nucleus of mice, in vitro. , 1988, The Journal of physiology.

[98]  L. Trussell Control of time course of glutamatergic synaptic currents. , 1998, Progress in brain research.

[99]  L. Kaczmarek,et al.  Contribution of the Kv3.1 potassium channel to high‐frequency firing in mouse auditory neurones , 1998, The Journal of physiology.

[100]  N. Kiang,et al.  Single unit activity in the posteroventral cochlear nucleus of the cat , 1975, The Journal of comparative neurology.

[101]  K. Funabiki,et al.  The role of GABAergic inputs for coincidence detection in the neurones of nucleus laminaris of the chick , 1998, The Journal of physiology.

[102]  PB Manis,et al.  Membrane properties and discharge characteristics of guinea pig dorsal cochlear nucleus neurons studied in vitro , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[103]  A. Reyes,et al.  A depolarizing inhibitory response to GABA in brainstem auditory neurons of the chick , 1995, Brain Research.

[104]  I. Forsythe,et al.  Presynaptic Calcium Current Modulation by a Metabotropic Glutamate Receptor , 1996, Science.

[105]  R. Wickesberg,et al.  Delayed, frequency-specific inhibition in the cochlear nuclei of mice: a mechanism for monaural echo suppression , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[106]  J. Rinzel,et al.  The role of dendrites in auditory coincidence detection , 1998, Nature.

[107]  M. Liberman Central projections of auditory‐nerve fibers of differing spontaneous rate. I. Anteroventral cochlear nucleus , 1991, The Journal of comparative neurology.

[108]  R. Dingledine,et al.  Identification of a site in glutamate receptor subunits that controls calcium permeability , 1991, Science.

[109]  T. Yin,et al.  Anatomy and physiology of principal cells of the medial nucleus of the trapezoid body (MNTB) of the cat. , 1998, Journal of neurophysiology.

[110]  W. Regehr,et al.  Short-term synaptic plasticity. , 2002, Annual review of physiology.

[111]  L. Trussell,et al.  Presynaptic glycine receptors enhance transmitter release at a mammalian central synapse , 2001, Nature.

[112]  T. Parks,et al.  The AMPA receptors of auditory neurons , 2000, Hearing Research.

[113]  P. H. Smith,et al.  Intracellular recordings from neurobiotin-labeled cells in brain slices of the rat medial nucleus of the trapezoid body , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[114]  L H Carney,et al.  Enhancement of neural synchronization in the anteroventral cochlear nucleus. I. Responses to tones at the characteristic frequency. , 1994, Journal of neurophysiology.

[115]  Steven Greenberg,et al.  Physiology of the Cochlear Nuclei , 1992 .

[116]  B. Walmsley,et al.  GABA mediates presynaptic inhibition at glycinergic synapses in a rat auditory brainstem nucleus , 2000, The Journal of physiology.

[117]  Donata Oertel,et al.  Maturation of synapses and electrical properties of cells in the cochlear nuclei , 1987, Hearing Research.

[118]  L. Trussell,et al.  Desensitization of AMPA receptors upon multiquantal neurotransmitter release , 1993, Neuron.

[119]  Daniel Johnston,et al.  Dendritic attenuation of synaptic potentials and currents: the role of passive membrane properties , 1994, Trends in Neurosciences.

[120]  R. Fay,et al.  The Mammalian auditory pathway : neurophysiology , 1992 .

[121]  L. Trussell,et al.  Voltage clamp analysis of excitatory synaptic transmission in the avian nucleus magnocellularis. , 1994, The Journal of physiology.