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Human cochlear nerve model

Human cochlear nerve model

Frank Rattay (ORCID: 0000-0002-2819-8827)
  • Grant DOI 10.55776/P21848
  • Funding program Principal Investigator Projects
  • Status ended
  • Start August 19, 2009
  • End November 18, 2013
  • Funding amount € 241,290
  • Project website

Disciplines

Biology (20%); Computer Sciences (30%); Clinical Medicine (30%); Medical Engineering (20%)

Keywords

    Human Cochlea, Morphometry, Neuron Cluster, Computer Simulation, Spiral Ganglion, Cochlear Implant

Abstract Final report

The main purpose of the project is to gather new detailed anatomic and morphometric information about the afferent part of the human cochlear nerve (spiral ganglion) and to use this data in a new computational model for analyzing input output relations for both the acoustically and the electrically stimulated ear. Moreover, the pathways of the spiral ganglion cells will be investigated. The results are of considerable interest to the cochlear implant research in order to overcome shortcomings like speech understanding in a noisy environment. The neural elements responsible for signal transport from the cochlea to the brain show essential anatomic differences between man and mammalian species, leading to several non tested and unproved hypotheses concerning functional consequences. Currently the signaling strategies for cochlea prostheses are mainly based on single fiber recordings in cat. Due to missing fundamental investigations on the neural elements of the human cochlea neurons, even the latest signal processing strategies for cochlear implant users are de facto designed for cats instead of humans. Most striking for the uniqueness of the human spiral ganglion cells is the soma region, typically with (i) poor insulation by myelin and (ii) clusters containing several cell bodies. A goal of the project is to expand to a large extent our knowledge about the relevant ultra-structure. Using existing equipment and material (temporal bones from several individuals and a selection of inner ears from primates) allows to quantify human peculiarities. A comparison with primates should give a clue about the development of the unique morphological features in humans. As an alternative to single fiber recordings which are not available for humans, we will develop a general biophysical model for cochlear neurons including cluster properties in order to understand the functional consequences of neuron variability seen in mammals and humans by analyzing the influence of relevant geometric and electric parameters. With this model we will analyze how the three main auditory nerve coding principles (i-iii) in man are related with the specific human anatomy and morphometry and, additionally, we will include a discussion about consequences for cochlear implants. In more detail, the model analysis is concerned with (i) tonotopic organization: a shift in frequency mapping concerning distal fiber endings originating in the organ of Corti (almost 2 cochlear turns) and soma regions in Rosenthal canal (1 turns), (ii) temporal fine structure of the neural code: a) for short interspike intervals in the distal axon there is a possible loss of signals when passing the soma region and b) in case of electrical stimulation: a confusing bimodal distribution of delay times as a consequence of more than one spike initiation regions along a single cochlear neuron (iii) spontaneous spiking is a supporting mechanism for acoustic signals just above the hearing threshold resulting in a mix of spikes with and without temporal information about the acoustic input; clusters of several somas may act as filter elements as a first step in neural code processing.

The main purpose of the project was to gather new detailed anatomic and morphometric information about the afferent part of the human cochlear nerve (spiral ganglion) and to use this data in a new computational model for analyzing input output relations for both the acoustically and the electrically stimulated ear. Moreover, the pathways of the spiral ganglion cells were investigated. The results are of considerable interest to the cochlear implant research in order to overcome shortcomings like speech understanding in a noisy environment. The neural elements responsible for signal transport from the cochlea to the brain show essential anatomic differences between man and mammalian species, leading to several non-tested and unproved hypotheses concerning functional consequences. Currently the signaling strategies for cochlea prostheses are mainly based on single fiber recordings in cat. Due to missing fundamental investigations on the neural elements of the human cochlea neurons, even the latest signal processing strategies for cochlear implant users are de facto designed for cats instead of humans. Most striking for the uniqueness of the human spiral ganglion cells is the soma region, typically with poor insulation by myelin and clusters containing several cell bodies. Our analysis showed that in human (i) the cell somas are smaller than reported earlier, (ii) the central axon diameter is always nearly just 2 times the peripheral ones and (iii) there are more neural clusters than expected. These three observations are contrary to findings in cats. Furthermore, neural pathway tracing showed spiraled shapes for the apical neurons implying loss of the tonotopically related excitation for low frequency components when cochlear implants substitute the natural neural firing pattern. This effect is explained by a short distance of a target neuron of the auditory nerve to several electrode contacts when the implant is active in the upper cochlear turn.Furthermore, we analyzed the action potential (spike) conductance along the auditory nerve, that is, from the inner hair cell (auditory receptor cell) to the next processing region called cochlear nucleus in the brainstem. Evaluation of our biophysical excitation model demonstrated that the synaptic currents from the inner hair cells are about 15 times stronger than needed. Wasting this synaptic energy boosts spike initiation, which guarantees the rapid transmission of temporal fine structure of auditory signals. Auditory brainstem response measurements are used as clinical tool in order to test the auditory pathway in patients. In spite of its importance it is not clear which neural elements are the generators of the peaks in the recorded signal. Our computer modeling study give evidence that peak I of the human auditory brainstem response results from the somatic regions of type I cells in the auditory nerve.

Research institution(s)
  • Medizinische Universität Innsbruck - 54%
  • Technische Universität Wien - 46%
Project participants
  • Anneliese Schrott-Fischer, Medizinische Universität Innsbruck , associated research partner
International project participants
  • Tania Hanekom, University of Pretoria - South Africa
  • Helge Rask-Andersen, Uppsala University Hospital - Sweden

Research Output

  • 644 Citations
  • 20 Publications
Publications
  • 2020
    Title Finite element analysis and three-dimensional reconstruction of tonotopically aligned human auditory fiber pathways: A computational environment for modeling electrical stimulation by a cochlear implant based on micro-CT
    DOI 10.1016/j.heares.2020.108001
    Type Journal Article
    Author Potrusil T
    Journal Hearing Research
    Pages 108001
  • 2017
    Title Molecular composition and distribution of gap junctions in the sensory epithelium of the human cochlea—a super-resolution structured illumination microscopy (SR-SIM) study
    DOI 10.1080/03009734.2017.1322645
    Type Journal Article
    Author Liu W
    Journal Upsala Journal of Medical Sciences
    Pages 1-11
    Link Publication
  • 2017
    Title Role of BDNF and neurotrophic receptors in human inner ear development
    DOI 10.1007/s00441-017-2686-9
    Type Journal Article
    Author Johnson Chacko L
    Journal Cell and Tissue Research
    Pages 347-363
    Link Publication
  • 2016
    Title Neurosensory Differentiation and Innervation Patterning in the Human Fetal Vestibular End Organs between the Gestational Weeks 8–12
    DOI 10.3389/fnana.2016.00111
    Type Journal Article
    Author Chacko L
    Journal Frontiers in Neuroanatomy
    Pages 111
    Link Publication
  • 2015
    Title Nanoparticle mediated drug delivery of rolipram to tyrosine kinase B positive cells in the inner ear with targeting peptides and agonistic antibodies
    DOI 10.3389/fnagi.2015.00071
    Type Journal Article
    Author Glueckert R
    Journal Frontiers in Aging Neuroscience
    Pages 71
    Link Publication
  • 2014
    Title Development of the innervation of the human inner ear
    DOI 10.1002/dneu.22242
    Type Journal Article
    Author Pechriggl E
    Journal Developmental Neurobiology
    Pages 683-702
    Link Publication
  • 2011
    Title Neurotrophic Receptors as Potential Therapy Targets in Postnatal Development, in Adult, and in Hearing Loss-Affected Inner Ear
    DOI 10.1097/mao.0b013e31821f7cc1
    Type Journal Article
    Author Bitsche M
    Journal Otology & Neurotology
    Pages 761-773
  • 2011
    Title Current-Distance Relations for Microelectrode Stimulation of Pyramidal Cells
    DOI 10.1111/j.1525-1594.2011.01224.x
    Type Journal Article
    Author Wenger C
    Journal Artificial Organs
    Pages 263-266
  • 2011
    Title Lateral superior olive function in congenital deafness
    DOI 10.1016/j.heares.2011.01.012
    Type Journal Article
    Author Couchman K
    Journal Hearing Research
    Pages 163-175
    Link Publication
  • 2013
    Title Nanomedicine strategies for drug delivery to the ear
    DOI 10.2217/nnm.13.104
    Type Journal Article
    Author Pritz C
    Journal Nanomedicine (London, England)
    Pages 1155-1172
  • 2010
    Title Enhancement of vowel encoding for cochlear implants by adding a high frequency signal: a modelling study.
    Type Conference Proceeding Abstract
    Author Paredes L
    Conference Proceedings 10th Vienna international workshop on functional electrical stimulation
  • 2010
    Title Which elements of the mammalian central nervous system are excited by low current stimulation with microelectrodes?
    DOI 10.1016/j.neuroscience.2010.07.032
    Type Journal Article
    Author Rattay F
    Journal Neuroscience
    Pages 399-407
    Link Publication
  • 2014
    Title Peak I of the human auditory brainstem response results from the somatic regions of type I spiral ganglion cells: Evidence from computer modeling
    DOI 10.1016/j.heares.2014.07.001
    Type Journal Article
    Author Rattay F
    Journal Hearing Research
    Pages 67-79
    Link Publication
  • 2013
    Title Research in Electrical Stimulation Fundamentals
    DOI 10.1111/aor.12258
    Type Journal Article
    Author Rattay F
    Journal Artificial Organs
    Pages 1023-1026
    Link Publication
  • 2013
    Title Impact of Morphometry, Myelinization and Synaptic Current Strength on Spike Conduction in Human and Cat Spiral Ganglion Neurons
    DOI 10.1371/journal.pone.0079256
    Type Journal Article
    Author Rattay F
    Journal PLoS ONE
    Link Publication
  • 2012
    Title Morphometric classification and spatial organization of spiral ganglion neurons in the human cochlea: Consequences for single fiber response to electrical stimulation
    DOI 10.1016/j.neuroscience.2012.03.033
    Type Journal Article
    Author Potrusil T
    Journal Neuroscience
    Pages 120-135
    Link Publication
  • 2012
    Title Sheep as a Large Animal Model for Middle and Inner Ear Implantable Hearing Devices
    DOI 10.1097/mao.0b013e318248ee3a
    Type Journal Article
    Author Schnabl J
    Journal Otology & Neurotology
    Pages 481-489
  • 2012
    Title Strength–duration relationship for intra- versus extracellular stimulation with microelectrodes
    DOI 10.1016/j.neuroscience.2012.04.004
    Type Journal Article
    Author Rattay F
    Journal Neuroscience
    Pages 1-13
    Link Publication
  • 2012
    Title Human Cochlea: Anatomical Characteristics and their Relevance for Cochlear Implantation
    DOI 10.1002/ar.22599
    Type Journal Article
    Author Rask-Andersen H
    Journal The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology
    Pages 1791-1811
  • 2011
    Title Improving Hearing Performance Using Natural Auditory Coding Strategies
    DOI 10.1007/978-3-642-11934-7_12
    Type Book Chapter
    Author Rattay F
    Publisher Springer Nature
    Pages 249-261

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