Peak I of the human auditory brainstem response results from the somatic regions of type I spiral ganglion cells: Evidence from computer modeling

Early neural responses to acoustic signals can be electrically recorded as a series of waves, termed the auditory brainstem response (ABR). The latencies of the ABR waves are important for clinical and neurophysiological evaluations. Using a biophysical model of transmembrane currents along spiral ganglion cells, we show that in human (i) the non-myelinated somatic regions of type I cells, which innervate inner hair cells, predominantly contribute to peak I, (ii) the supra-strong postsynaptic stimulating current (400 pA) and transmembrane currents of the myelinated peripheral axons of type I cells are an order smaller; such postsynaptic currents correspond to the short latencies of a small recordable ABR peak I’, (iii) the ABR signal involvement of the central axon of bipolar type I cells is more effective than their peripheral counterpart as the doubled diameter causes larger transmembrane currents and a larger spike dipole-length, (iv) non-myelinated fibers of type II cells which innervate the outer hair cells generate essentially larger transmembrane currents but their ABR contribution is small because of the small ratio type II/type I cells, low firing rates and a short dipole length of spikes propagating slowly in non-myelinated fibers. Using a finite element model of a simplified head, peaks In and II (where In is the negative peak after peak I) are found to be stationary potentials when volleys of spikes cross the external electrical conductivity barrier at the bone&dura/CSF and at the CSF/brainstem interface whereas peaks I’ and I may be generated by strong local transmembrane currents as postsynaptic events at the distal ending and the soma region of type I cells, respectively. All simulated human inter-peak times (I–I′, II–I, In–I) are close to published data.

[1]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1990 .

[2]  D L Jewett,et al.  Auditory-evoked far fields averaged from the scalp of humans. , 1971, Brain : a journal of neurology.

[3]  A. Møller,et al.  Contributions from the auditory nerve to the brain-stem auditory evoked potentials (BAEPs): results of intracranial recording in man. , 1988, Electroencephalography and clinical neurophysiology.

[4]  Rainer Hartmann,et al.  Discharge patterns of cat primary auditory fibers with electrical stimulation of the cochlea , 1984, Hearing Research.

[5]  Yousheng Shu,et al.  Distinct contributions of Nav1.6 and Nav1.2 in action potential initiation and backpropagation , 2009, Nature Neuroscience.

[6]  F. Rattay,et al.  The basic mechanism for the electrical stimulation of the nervous system , 1999, Neuroscience.

[7]  Yaşargil Mg The internal acoustic meatus. , 2002 .

[8]  Frank Rattay,et al.  A model of the electrically excited human cochlear neuron. II. Influence of the three-dimensional cochlear structure on neural excitability , 2001, Hearing Research.

[9]  T. Nakanishi Action potentials recorded by fluid electrodes. , 1982, Electroencephalography and clinical neurophysiology.

[10]  J. Nadol,et al.  Patterns of neural degeneration in the human cochlea and auditory nerve: implications for cochlear implantation. , 1997, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[11]  I. A. Boyd,et al.  Scaling factor relating conduction velocity and diameter for myelinated afferent nerve fibres in the cat hind limb. , 1979, The Journal of physiology.

[12]  R. Kimura,et al.  Ultrastructural study of the human spiral ganglion. , 1980, Acta oto-laryngologica.

[13]  F. Rattay,et al.  Modeling axon membranes for functional electrical stimulation , 1993, IEEE Transactions on Biomedical Engineering.

[14]  N. Kiang,et al.  Generators of the brainstem auditory evoked potential in cat. I. An experimental approach to their identification , 1996, Hearing Research.

[15]  P. Fuchs,et al.  Synaptic Transfer from Outer Hair Cells to Type II Afferent Fibers in the Rat Cochlea , 2012, The Journal of Neuroscience.

[16]  D L Jewett,et al.  Volume-conducted potentials in response to auditory stimuli as detected by averaging in the cat. , 1970, Electroencephalography and clinical neurophysiology.

[17]  Peter G. LoPresti,et al.  Handbook of Neuroprosthetic Methods , 2002 .

[18]  Frank Rattay,et al.  Electrical Nerve Stimulation: "Theory, Experiments And Applications" , 2001 .

[19]  A. Nuttall,et al.  Characterization of an EPSP-like potential recorded remotely from the round window. , 1989, The Journal of the Acoustical Society of America.

[20]  F Rattay,et al.  Epidural electrical stimulation of posterior structures of the human lumbosacral cord: 2. quantitative analysis by computer modeling , 2000, Spinal Cord.

[21]  M. Yașargil The internal acoustic meatus. , 2002, Journal of neurosurgery.

[22]  J. Guinan,et al.  The Auditory Nerve Overlapped Waveform (ANOW) Originates in the Cochlear Apex , 2014, Journal of the Association for Research in Otolaryngology.

[23]  Paul J. Abbas,et al.  Intracochlear and extracochlear ECAPs suggest antidromic action potentials , 2004, Hearing Research.

[24]  Steve Davolt Universal Infant Hearing Screening Gains Momentum in States , 1999 .

[25]  F. Rattay,et al.  A study of the application of the Hodgkin-Huxley and the Frankenhaeuser-Huxley model for electrostimulation of the acoustic nerve , 1986, Neuroscience.

[26]  A. Starr,et al.  Brain Stem Potentials Evoked by Electrical Stimulation of the Cochlea in Human Subjects , 1979, The Annals of otology, rhinology, and laryngology.

[27]  Josef Ladenbauer,et al.  Can the human lumbar posterior columns be stimulated by transcutaneous spinal cord stimulation? A modeling study. , 2011, Artificial organs.

[28]  Gustavo Viani Arruda,et al.  Brainstem evoked response audiometry in normal hearing subjects , 2009, Brazilian journal of otorhinolaryngology.

[29]  F. Rattay,et al.  Which elements of the mammalian central nervous system are excited by low current stimulation with microelectrodes? , 2010, Neuroscience.

[30]  R. Patuzzi,et al.  Evidence that the compound action potential (CAP) from the auditory nerve is a stationary potential generated across dura mater , 2010, Hearing Research.

[31]  Andrew K. Wise,et al.  Impact of Morphometry, Myelinization and Synaptic Current Strength on Spike Conduction in Human and Cat Spiral Ganglion Neurons , 2013, PloS one.

[32]  J. Fraher Axons and glial interfaces: ultrastructural studies * , 2002, Journal of anatomy.

[33]  Jaime A. Undurraga,et al.  The Polarity Sensitivity of the Electrically Stimulated Human Auditory Nerve Measured at the Level of the Brainstem , 2013, Journal of the Association for Research in Otolaryngology.

[34]  H. Davis,et al.  Exploration of Cochlear Potentials in Guinea Pig with a Microelectrode , 1954 .

[35]  J. R. Hughes,et al.  A Review of Generators of the Brainstem Auditory Evoked Potential: Contribution of an Experimental Study , 1985, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[36]  J. Nadol,et al.  Comparative anatomy of the cochlea and auditory nerve in mammals , 1988, Hearing Research.

[37]  Eunyoung Yi,et al.  Dendritic Hcn Channels Shape Excitatory Postsynaptic Potentials at the Inner Hair Cell Afferent Synapse in the Mammalian Cochlea Electrophysiological Recordings , 2022 .

[38]  J. Wouters,et al.  Higher Sensitivity of Human Auditory Nerve Fibers to Positive Electrical Currents , 2008, Journal of the Association for Research in Otolaryngology.

[39]  C. Destrieux,et al.  The internal acoustic meatus and its meningeal layers: a microanatomical study. , 2002, Journal of neurosurgery.

[40]  E. Truy,et al.  Effects of auditory pathway anatomy and deafness characteristics? (1): On electrically evoked auditory brainstem responses , 2007, Hearing Research.

[41]  B. Rakerd,et al.  The I' potential of the brain-stem auditory-evoked potential. , 1992, Scandinavian audiology.

[42]  Gustavo Viani Arruda,et al.  Estudo das latências das ondas dos potenciais auditivos de tronco encefálico em indivíduos normo-ouvintes , 2009 .

[43]  A. Møller On the origin of the compound action potentials (N1, N2) of the cochlea of the rat , 1983, Experimental Neurology.

[44]  H. Pratt,et al.  The origin of the human auditory brain-stem response wave II. , 1995, Electroencephalography and clinical neurophysiology.

[45]  Eunyoung Yi,et al.  Two Modes of Release Shape the Postsynaptic Response at the Inner Hair Cell Ribbon Synapse , 2010, The Journal of Neuroscience.

[46]  A. Dale,et al.  Conductivity tensor mapping of the human brain using diffusion tensor MRI , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[47]  Tiaan Krynauw Malherbe,et al.  Can subject-specific single-fibre electrically evoked auditory brainstem response data be predicted from a model? , 2013, Medical engineering & physics.

[48]  R. Hall,et al.  Estimation of surviving spiral ganglion cells in the deaf rat using the electrically evoked auditory brainstem response , 1990, Hearing Research.

[49]  F. Rattay,et al.  Morphometric classification and spatial organization of spiral ganglion neurons in the human cochlea: Consequences for single fiber response to electrical stimulation , 2012, Neuroscience.

[50]  H. Löwenheim,et al.  The I' potential of the human auditory brainstem response to paired click stimuli , 2001, Scandinavian audiology.

[51]  Frank Rattay,et al.  A model of the electrically excited human cochlear neuron I. Contribution of neural substructures to the generation and propagation of spikes , 2001, Hearing Research.

[52]  Auditory evoked potentials recorded directly from the human VIIIth nerve and brain stem: origins of their fast and slow components. , 1982, Electroencephalography and clinical neurophysiology. Supplement.

[53]  D. Stegeman,et al.  Far-field evoked potential components induced by a propagating generator: computational evidence. , 1987, Electroencephalography and clinical neurophysiology.

[54]  H. Spoendlin Neuroanatomical basis of cochlear coding mechanisms. , 1975, Audiology : official organ of the International Society of Audiology.

[55]  P. Abbas,et al.  Electrically evoked auditory brainstem response: Growth of response with current level , 1991, Hearing Research.

[56]  J. Mason,et al.  Universal infant hearing screening by automated auditory brainstem response measurement. , 1998, Pediatrics.

[57]  Yang Yang,et al.  Where Is the Spike Generator of the Cochlear Nerve? Voltage-Gated Sodium Channels in the Mouse Cochlea , 2005, The Journal of Neuroscience.