An Optimization-Based Study of Equivalent Circuit Models for Representing Recordings at the Neuron-Electrode Interface

Vaibhav Thakore, Peter Molnar, James J. Hickman*

*Corresponding author for this work

Research output: Contribution to journalArticleScientificpeer-review

Abstract

Extracellular neuroelectronic interfacing is an emerging field with important applications in the fields of neural prosthetics, biological computation, and biosensors. Traditionally, neuron-electrode interfaces have been modeled as linear point or area contact equivalent circuits but it is now being increasingly realized that such models cannot explain the shapes and magnitudes of the observed extracellular signals. Here, results were compared and contrasted from an unprecedented optimization-based study of the point contact models for an extracellular "on-cell" neuron-patch electrode and a planar neuron-microelectrode interface. Concurrent electrophysiological recordings from a single neuron simultaneously interfaced to three distinct electrodes (intracellular, "on-cell" patch, and planar microelectrode) allowed novel insights into the mechanism of signal transduction at the neuron-electrode interface. After a systematic isolation of the nonlinear neuronal contribution to the extracellular signal, a consistent underestimation of the simulated suprathreshold extracellular signals compared to the experimentally recorded signals was observed. This conclusively demonstrated that the dynamics of the interfacial medium contribute nonlinearly to the process of signal transduction at the neuron-electrode interface. Further, an examination of the optimized model parameters for the experimental extracellular recordings from sub-and suprathreshold stimulations of the neuron-electrode junctions revealed that ionic transport at the "on-cell" neuron-patch electrode is dominated by diffusion whereas at the neuron-microelectrode interface the electric double layer (EDL) effects dominate. Based on this study, the limitations of the equivalent circuit models in their failure to account for the nonlinear EDL and ionic electrodiffusion effects occurring during signal transduction at the neuron-electrode interfaces are discussed.

Original languageEnglish
Pages (from-to)2338-2347
Number of pages10
JournalIEEE Transactions on Biomedical Engineering
Volume59
Issue number8
DOIs
Publication statusPublished - Aug 2012
MoE publication typeA1 Journal article-refereed

Keywords

  • Microelectrode arrays (MEAs)
  • neuroelectronic interface
  • nonlinear ionic electrodiffusion
  • whole-cell biosensors
  • EXTRACELLULAR RECORDINGS
  • SIGNAL TRANSFER
  • TRANSISTOR
  • MICROELECTRODE
  • MEMBRANE
  • CURRENTS
  • STIMULATION
  • IMPEDANCE
  • JUNCTION
  • ARRAYS

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