How neurons move during action potentials

Author:

Ling TongORCID,Boyle Kevin C.,Zuckerman Valentina,Flores Thomas,Ramakrishnan Charu,Deisseroth Karl,Palanker Daniel

Abstract

AbstractNeurons undergo nanometer-scale deformations during action potentials, and the underlying mechanism has been actively debated for decades. Previous observations were limited to a single spot or the cell boundary, while movement across the entire neuron during the action potential remained unclear.We report full-field imaging of cellular deformations accompanying the action potential in mammalian neuron somas (−1.8nm~1.3nm) and neurites (−0.7nm~0.9nm), using fast quantitative phase imaging with a temporal resolution of 0.1ms and an optical pathlength sensitivity of <4pm per pixel. Spike-triggered average, synchronized to electrical recording, demonstrates that the time course of the optical phase changes matches the dynamics of the electrical signal, with the optical signal revealing the intracellular potential rather than its time derivative detected via extracellular electrodes. Using 3D cellular morphology extracted via confocal microscopy, we demonstrate that the voltage-dependent changes in the membrane tension induced by ionic repulsion can explain the magnitude, time course and spatial features of the phase imaging. Our full-field observations of the spike-induced deformations in mammalian neurons opens the door to non-invasive label-free imaging of neural signaling.

Publisher

Cold Spring Harbor Laboratory

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