Biomechanical micromotion at the neural interface modulates intracellular membrane potentials in vivo

Jonathan Duncan, Arati Sridharan, Swathy Sampath Kumar, Diane Iradukunda, Jit Muthuswamy

Research output: Contribution to journalArticlepeer-review

1 Scopus citations

Abstract

Objective. Respiration and vascular pulsation cause relative micromotion of brain tissue against stationary implants resulting in repetitive displacements of 2-4 µm (due to vascular pulsation) and 10-30 µm (due to breathing) in rats. However, the direct functional impact of such tissue micromotion on the cells at the neural interface remains unknown. This study aims to test the hypothesis that micromotion in brain tissue causes changes in membrane potentials (MPs) through the activation of mechanosensitive ion channels. Approach. Intracellular MPs were recorded from Aplysia ganglion cells (n = 8) and cortical cells (n = 15) in vivo in n = 7 adult rats. Cyclic stresses between 0.2 and 4 kPa repeated at 1 Hz were tested in Aplysia ganglion cells. For the in vivo experiments, 30 μM of gadolinium chloride (Gd3+), a non-selective blocker of mechanosensitive ion channels, was used to assess the role of such ion channels. Main results. In Aplysia ganglion cells, there were no MP changes for <1.5 kPa, and action potentials were observed at >3.1 kPa. Drug studies utilizing 5-HT showed an 80% reduction in firing frequency from controls. In in vivo experiments, periodic pulsations (1-10 mV) were observed in the MPs of cells that corresponded to breathing and heart-rate. In response to the addition of 30 µM Gd3+, we observed a significant reduction (0.5-3 mV) in the periodic pulsations in MP in all cortical cells across four different rats, suggesting the role of mechanosensitive ion channels in mediating MP fluctuations due to tissue micromotion at the neural interface. Significance. Under chronic conditions, the tissue at the interface stiffens due to scar tissue formation, which is expected to increase the likelihood of recruiting stretch-receptors due to tissue micromotion. It is speculated that such chronic sub-threshold pulsations in MPs might trigger the immune response at the neural interface.

Original languageEnglish (US)
Article number045010
JournalJournal of neural engineering
Volume18
Issue number4
DOIs
StatePublished - Aug 2021

Keywords

  • brain tissue
  • implant
  • neural prostheses
  • neural recordings

ASJC Scopus subject areas

  • Biomedical Engineering
  • Cellular and Molecular Neuroscience

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