Optocapacitive Generation of Action Potentials by Microsecond Laser Pulses of Nanojoule Energy

Abstract

Millisecond pulses of laser light delivered to gold nanoparticles residing in close proximity to the surface membrane of neurons can induce membrane depolarization and initiate an action potential. An optocapacitance mechanism proposed as the basis of this effect posits that the membrane-interfaced particle photothermally induces a cell-depolarizing capacitive current, and predicts that delivering a given laser pulse energy within a shorter period should increase the pulse's action-potential-generating effectiveness by increasing the magnitude of this capacitive current. Experiments on dorsal root ganglion cells show that, for each of a group of interfaced gold nanoparticles and microscale carbon particles, reducing pulse duration from milliseconds to microseconds markedly decreases the minimal pulse energy required for AP generation, providing strong support for the optocapacitance mechanism hypothesis.

Thermal Optofluidics: Principles and Applications

“…Recently, the manipulation of cellular activity, such as light‐mediated neuromodulation techniques, has become more popular in physiological and clinical applications, because its high spatial and temporal resolution deliver real benefits to neuroscience research . For example, as shown in Figure c, the reversible inhibition of neural spiking activity in a localized area was achieved via plasmonic gold nanorod‐mediated photothermal stimulation under NIR illumination .…”

“…[39,41,59] Because of its unique properties of remote con trol and ultrafast ondemand nanoscale thermal production, it has also been widely employed in biosensing and manipulation of cellular functions, such as ultrafast plasmonic PCR, [60][61][62] intracellular gene delivery and release, [63] as well as singlecell neural activity control. [64][65][66][67][68] The above three optofluidic applications are greatly influ enced by optical and thermodynamic interactions. By carefully tailoring these interactions, one can achieve their desired opto fluidic functions.…”

Nongenetic Optical Methods for Measuring and Modulating Neuronal Response

“…To quantitatively understand how photothermal stimulation can give rise to membrane depolarization, we refer to Carvalho-de-Souza et al 61 , where they represented the cell membrane as an equivalent circuit following the HH model (Figure 2b), such that C m is the membrane capacitance. Modeling the cell membrane in this way gives rise to the governing relation: $$C_m(t)=C_0+C_0\gamma E\frac{F\left(t\right)}{\Delta t}$$ Where γ is the efficiency of thermal transfer between a particle and the membrane (~1% in the case of gold nanorods), C 0 is the initial capacitance, E is radiative pulse of energy, and F(t) is the equation for change in particle temperature as a function of time, t. While Carvalho-de-Souza et al 61 go on to model F(t) more precisely for a gold nanorod, this equation can be used to form some intuitive insights into photothermal stimulation.…”

“…Modeling the cell membrane in this way gives rise to the governing relation: $$C_m(t)=C_0+C_0\gamma E\frac{F\left(t\right)}{\Delta t}$$ Where γ is the efficiency of thermal transfer between a particle and the membrane (~1% in the case of gold nanorods), C 0 is the initial capacitance, E is radiative pulse of energy, and F(t) is the equation for change in particle temperature as a function of time, t. While Carvalho-de-Souza et al 61 go on to model F(t) more precisely for a gold nanorod, this equation can be used to form some intuitive insights into photothermal stimulation. Namely, that larger laser powers, E, lead to higher capacitance changes (Figure 2c), and that materials which generate, F(t), and transfer heat, γ, most efficiently serve as the best devices to change membrane capacitance.…”

“…F and F 0 are the output and input frequencies receptively. Modified and reproduced with permission from J. Carvalho-de-Souza et al 61 (b-d) and Y. Jiang et al 61 . (e-f) .…”