Modelling firing regularity in the ventral cochlear nucleus: mechanisms, and effects of stimulus level and synaptopathy

The auditory system processes temporal information at multiple scales, and disruptions to this temporal processing may lead to deficits in auditory tasks such as detecting and discriminating sounds in a noisy environment. Here, a modelling approach is used to study the temporal regularity of firing by chopper cells in the ventral cochlear nucleus, in both the normal and impaired auditory system. Chopper cells, which have a strikingly regular firing response, divide into two classes, sustained and transient, based on the time course of this regularity. Several hypotheses have been proposed to explain the behaviour of chopper cells, and the difference between sustained and transient cells in particular. However, there is no conclusive evidence so far. Here, a reduced mathematical model is developed and used to compare and test a wide range of hypotheses with a limited number of parameters. Simulation results show a continuum of cell types and behaviours: chopper-like behaviour arises for a wide range of parameters, suggesting that multiple mechanisms may underlie this behaviour. The model accounts for systematic trends in regularity as a function of stimulus level that have previously only been reported anecdotally. Finally, the model is used to predict the effects of a reduction in the number of auditory nerve fibres (deafferentation due to, for example, cochlear synaptopathy). An interactive version of this paper in which all the model parameters can be changed is available online.

[1]  Xiao-Jing Wang,et al.  Mean-Driven and Fluctuation-Driven Persistent Activity in Recurrent Networks , 2007, Neural Computation.

[2]  Christopher J. Plack,et al.  Toward a Diagnostic Test for Hidden Hearing Loss , 2015, Trends in hearing.

[3]  Nicolas Brunel,et al.  Dynamics of Sparsely Connected Networks of Excitatory and Inhibitory Spiking Neurons , 2000, Journal of Computational Neuroscience.

[4]  Ying-Cheng Lai,et al.  A model of selective processing of auditory-nerve inputs by stellate cells of the antero-ventral cochlear nucleus , 1994, Journal of Computational Neuroscience.

[5]  A. Faisal,et al.  Noise in the nervous system , 2008, Nature Reviews Neuroscience.

[6]  Frédéric Berthommier,et al.  Neuronal correlates of perceptual amplitude-modulation detection , 1995, Hearing Research.

[7]  Bertrand Delgutte,et al.  Decoding Sound Source Location and Separation Using Neural Population Activity Patterns , 2013, The Journal of Neuroscience.

[8]  Ray Meddis,et al.  The representation of periodic sounds in simulated sustained chopper units of the ventral cochlear nucleus. , 2004, The Journal of the Acoustical Society of America.

[9]  Andrew J. Oxenham,et al.  Predicting the Perceptual Consequences of Hidden Hearing Loss , 2016, Trends in hearing.

[10]  Robert D Frisina,et al.  Encoding of amplitude modulation in the gerbil cochlear nucleus: I. A hierarchy of enhancement , 1990, Hearing Research.

[11]  John Rinzel,et al.  TYPE III EXCITABILITY, SLOPE SENSITIVITY AND COINCIDENCE DETECTION. , 2012, Discrete and continuous dynamical systems. Series A.

[12]  Romain Brette,et al.  The Brian Simulator , 2009, Front. Neurosci..

[13]  Christian Füllgrabe,et al.  Neurometric amplitude‐modulation detection threshold in the guinea‐pig ventral cochlear nucleus , 2013, The Journal of physiology.

[14]  Enrique A. Lopez-Poveda,et al.  Perception of stochastically undersampled sound waveforms: a model of auditory deafferentation , 2013, Front. Neurosci..

[15]  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.

[16]  L. Carney,et al.  A phenomenological model of peripheral and central neural responses to amplitude-modulated tones. , 2004, The Journal of the Acoustical Society of America.

[17]  Romain Brette,et al.  Brian: A Simulator for Spiking Neural Networks in Python , 2008, Frontiers Neuroinformatics.

[18]  M. Liberman,et al.  Noise-induced cochlear neuropathy is selective for fibers with low spontaneous rates. , 2013, Journal of neurophysiology.

[19]  Naoya Itatani,et al.  Enhancement of forward suppression begins in the ventral cochlear nucleus , 2016, Brain Research.

[20]  Ray Meddis,et al.  The role of auditory nerve innervation and dendritic filtering in shaping onset responses in the ventral cochlear nucleus , 2009, Brain Research.

[21]  David J. Freedman,et al.  Independent Category and Spatial Encoding in Parietal Cortex , 2013, Neuron.

[22]  Romain Brette,et al.  Equation-oriented specification of neural models for simulations , 2013, Front. Neuroinform..

[23]  M. Sachs,et al.  Classification of unit types in the anteroventral cochlear nucleus: PST histograms and regularity analysis. , 1989, Journal of neurophysiology.

[24]  Romain Brette,et al.  Computing with Neural Synchrony , 2012, PLoS Comput. Biol..

[25]  M. B. Sachs,et al.  Auditory nerve inputs to cochlear nucleus neurons studied with cross-correlation , 2008, Neuroscience.

[26]  Kenneth E. Hancock,et al.  Homeostatic normalization of sensory gain in auditory corticofugal feedback neurons , 2017, bioRxiv.

[27]  Eero P. Simoncelli,et al.  Article Sound Texture Perception via Statistics of the Auditory Periphery: Evidence from Sound Synthesis , 2022 .

[28]  C. Koch,et al.  A brief history of time (constants). , 1996, Cerebral cortex.

[29]  J. Rothman,et al.  Differential expression of three distinct potassium currents in the ventral cochlear nucleus. , 2003, Journal of neurophysiology.

[30]  Baranidharan Raman,et al.  Temporally Diverse Firing Patterns in Olfactory Receptor Neurons Underlie Spatiotemporal Neural Codes for Odors , 2010, The Journal of Neuroscience.

[31]  M. Nolan,et al.  Tuning of Synaptic Integration in the Medial Entorhinal Cortex to the Organization of Grid Cell Firing Fields , 2008, Neuron.

[32]  R Meddis,et al.  Regularity of cochlear nucleus stellate cells: a computational modeling study. , 1993, The Journal of the Acoustical Society of America.

[33]  Eve Marder,et al.  Computational models in the age of large datasets , 2015, Current Opinion in Neurobiology.

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

[35]  M. Liberman,et al.  Adding Insult to Injury: Cochlear Nerve Degeneration after “Temporary” Noise-Induced Hearing Loss , 2009, The Journal of Neuroscience.

[36]  Leonard Maler,et al.  Neural heterogeneity and efficient population codes for communication signals. , 2010, Journal of neurophysiology.

[37]  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.

[38]  Aravinthan D. T. Samuel,et al.  An olfactory neuron responds stochastically to temperature and modulates Caenorhabditis elegans thermotactic behavior , 2008, Proceedings of the National Academy of Sciences.

[39]  Robert A. Levine,et al.  Brainstem Auditory Evoked Potentials Suggest a Role for the Ventral Cochlear Nucleus in Tinnitus , 2012, Journal of the Association for Research in Otolaryngology.

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

[41]  Enrique A. Lopez-Poveda,et al.  Why do I hear but not understand? Stochastic undersampling as a model of degraded neural encoding of speech , 2014, Front. Neurosci..

[42]  N. Urban,et al.  Intrinsic biophysical diversity decorrelates neuronal firing while increasing information content , 2010, Nature Neuroscience.

[43]  Laurel H. Carney,et al.  Speech Coding in the Brain: Representation of Vowel Formants by Midbrain Neurons Tuned to Sound Fluctuations1,2,3 , 2015, eNeuro.

[44]  Nicolas Brunel,et al.  Dynamics of the Firing Probability of Noisy Integrate-and-Fire Neurons , 2002, Neural Computation.

[45]  Cori Bargmann,et al.  Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans , 1991, Neuron.

[46]  M. Liberman,et al.  Toward a Differential Diagnosis of Hidden Hearing Loss in Humans , 2016, PloS one.

[47]  R. Shannon,et al.  Speech recognition in noise as a function of the number of spectral channels: comparison of acoustic hearing and cochlear implants. , 2001, The Journal of the Acoustical Society of America.

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

[49]  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.

[50]  W. Newsome,et al.  The Variable Discharge of Cortical Neurons: Implications for Connectivity, Computation, and Information Coding , 1998, The Journal of Neuroscience.

[51]  J. Rothman,et al.  Kinetic analyses of three distinct potassium conductances in ventral cochlear nucleus neurons. , 2003, Journal of neurophysiology.

[52]  Gérard Faucon,et al.  Evaluation of two computational models of amplitude modulation coding in the inferior colliculus , 2006, Hearing Research.

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

[54]  G. Turrigiano Homeostatic synaptic plasticity: local and global mechanisms for stabilizing neuronal function. , 2012, Cold Spring Harbor perspectives in biology.

[55]  D. Caspary,et al.  Elevated Fusiform Cell Activity in the Dorsal Cochlear Nucleus of Chinchillas with Psychophysical Evidence of Tinnitus , 2002, The Journal of Neuroscience.

[56]  I. Winter,et al.  Responses of single units in the anteroventral cochlear nucleus of the guinea pig , 1990, Hearing Research.

[57]  Damon A. Clark,et al.  The AFD Sensory Neurons Encode Multiple Functions Underlying Thermotactic Behavior in Caenorhabditis elegans , 2006, The Journal of Neuroscience.

[58]  Luke Campagnola,et al.  A Map of Functional Synaptic Connectivity in the Mouse Anteroventral Cochlear Nucleus , 2014, The Journal of Neuroscience.

[59]  Romain Brette,et al.  Decoding neural responses to temporal cues for sound localization , 2013, eLife.

[60]  R Meddis,et al.  A computer model of a cochlear-nucleus stellate cell: responses to amplitude-modulated and pure-tone stimuli. , 1992, The Journal of the Acoustical Society of America.

[61]  J. Rothman,et al.  The roles potassium currents play in regulating the electrical activity of ventral cochlear nucleus neurons. , 2003, Journal of neurophysiology.

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

[63]  Anna R. Chambers,et al.  Central Gain Restores Auditory Processing following Near-Complete Cochlear Denervation , 2016, Neuron.

[64]  H. Francis,et al.  Effects of deafferentation on the electrophysiology of ventral cochlear nucleus neurons , 2000, Hearing Research.

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

[66]  M B Sachs,et al.  Transformation of temporal discharge patterns in a ventral cochlear nucleus stellate cell model: implications for physiological mechanisms. , 1995, Journal of neurophysiology.

[67]  A. Palmer,et al.  The Effect of Correlated Neuronal Firing and Neuronal Heterogeneity on Population Coding Accuracy in Guinea Pig Inferior Colliculus , 2013, PloS one.

[68]  D. McAlpine,et al.  Tinnitus with a Normal Audiogram: Physiological Evidence for Hidden Hearing Loss and Computational Model , 2011, The Journal of Neuroscience.

[69]  Ray Meddis,et al.  Physiological Correlates of Comodulation Masking Release in the Mammalian Ventral Cochlear Nucleus , 2001, The Journal of Neuroscience.

[70]  Bernhard Englitz,et al.  Multidimensional Characterization and Differentiation of Neurons in the Anteroventral Cochlear Nucleus , 2012, PloS one.