Field interactions in the peripheral auditory neural system with reference to cochlear implants

Abstract

This study investigates the effect of field interactions on neural excitation profiles within the electrically stimulated auditory system on two levels: interneural by studying the ephaptic excitatory effect of neurons on one another and extraneural by studying the effect of inhomogeneities in the neural volume on excitation profiles. The investigation contributes to the tool base available for computational neuromodelling. Ephaptic stimulation of a neuron refers to excitation of a neuron by the extracellular environment induced by other neurons. It is usually assumed that neurons communicate only through anatomical specializations such as gap junctions or synapses, but since a large extracellular potential from active neurons, arising during the propagation of action potentials, can trigger an action potential in another subthreshold neuron, ephaptic stimulation could be significant and should therefore be taken into account when dealing with neuron interaction. The objective of the study was to quantify the influence of ephaptic excitation on nerve stimulation utilizing models with increasing anatomical, morphological and morphometrical detail and determine whether it is a necessary factor in neuromodelling. An initial, simple model of ephaptic excitation suggested a possible significant effect on electric hearing. The results show that the contribution of ephaptic excitation is most significant close to threshold and continues to be significant up to at least 6-7dB above threshold. Cochlear implant subjects normally have a small dynamic range (average of 7 dB), indicating that the ephaptic effect might be important in models of the implanted cochlea. The model was extended to include more details including neural membrane noise, the three-dimensional geometry and conductive properties of the cochlear volume and variation in stimulating pulse shape. It was shown that the ephaptic effect is still significant in the presence of these amendments and is affected by all of the mentioned parameters. It was also shown that ephaptic excitation significantly contributes to cross-turn stimulation which in turn has implications for pitch perception in cochlear implant subjects. Ephaptic excitation of ectopic neural populations was proposed as a possible mechanism that could produce pitch confusions suggesting that interpretation of psychoacoustic and neural response data from literature may be aided when the ephaptic effect is taken into account. The effect of heterogeneity, caused by the structure of the neural tissue, on potential distributions within the neural population was investigated by means of finite element modelling. It was demonstrated that the presence of fibres in the medium has a significant effect on the extracellular potential distribution at small distances from the point sources in that it decreased the potential. This in turn affects the excitation profile within the neural population. The results of this study show that the significance of the ephaptic effect at stimulus intensities close to threshold can be demonstrated by a very simple deterministic model. However, further quantification of the effect shows that factors such as anatomical, morphological and morphometrical details, membrane noise and stimulus waveform should be included when modelling the responsiveness of auditory nerve fibres close to threshold.