Infrared Light Excites Cells via Transient Changes in Membrane Electrical Capacitance

Abstract

Control of excitable cells using optical technologies such as optogenetics has enabled important advances in neuroscience and the development of clinical applications. Most existing methods of optical control require the use of genetic or chemical sensitizers that enable light to alter the ionic conductance of cell membranes. By contrast, infrared (IR) light of wavelengths > 1.5μm has been shown in vivo to excite neural and muscle tissue without any pre-treatment. Unfortunately, the mechanism of IR stimulation is unknown. Here, we describe how IR light excites cells by transiently altering their membrane electrical capacitance. Our data from voltage clamped Xenopus laevis oocytes, mammalian cells and artificial lipid bilayers shows that IR energy absorbed by water produces a rapid local increase in temperature at the cell membrane, transiently increasing its electrical capacitance, and generating depolarizing currents. Correspondingly, under current clamp conditions, IR pulses produce rapid changes in membrane potential. This unexpected mechanism is fully reversible and requires only the most basic properties of cell membranes. Changes in capacitance were verified by direct measurement in mammalian cells and artificial bilayers, and are consistent with a classical theoretical description of cell membranes as coupled double-layer capacitors. In shedding light on the mechanism of IR stimulation, our findings point to this technology's unique generality as a means to control excitable cells, and raise questions about other thermal phenomena that may meaningfully affect membrane electrostatics. Supported by the NIH: GM030376 and DC011481-01A1.