Infrared inhibition and waveform modulation of action potentials in the crayfish motor axon

Abstract

The infrared (IR) inhibition of axonal activities in the crayfish neuromuscular preparation is studied using 2 µm IR light pulses with varying durations. The intracellular neuronal activities are monitored with two-electrode current clamp, while the IR-induced temperature changes are measured by the open patch technique simultaneously. It is demonstrated that the IR pulses can reversibly shape or block locally initiated action potentials. Suppression of the AP amplitude and duration and decrease in axonal excitability by IR pulses are quantitatively analyzed. While the AP amplitude and duration decrease similarly during IR illumination, it is discovered that the recovery of the AP duration after the IR pulses is slower than that of the AP amplitude. An IR-induced decrease in the input resistance (8.8%) is detected and discussed together with the temperature dependent changes in channel kinetics as contributing factors for the inhibition reported here.

Infrared inhibition impacts on locally initiated and propagating action potentials and the downstream synaptic transmission

“…4(a) and 4(c) insets]. This separation minimized the transfer and diffusion of the IR-induced localized heat of the axon to the muscle being recorded 19 (Fig. S1).…”

“… 1 – 3 IR-mediated modulation of excitable tissues has been demonstrated in a wide range of promising clinical applications, such as cochlear prostheses, 4 , 5 brain stimulation and mapping, 6 – 9 cardiac pacing, 10 and neural monitoring during surgery. 11 , 12 The main biological processes induced by pulsed IR light are attributed to the spatiotemporal thermal transients generated by water and tissue absorption, 13 which in turn can alter the membrane capacitance, 14 – 17 membrane resistance, 18 , 19 ion channel activities, 19 – 25 and intracellular calcium dynamics. 6 , 26 – 30 The temperature-sensitive transient receptor potential channels have received particular attention due to their intrinsic temperature sentisitivity.…”

“…The inhibition of excitable tissues, 19 – 21 , 32 – 36 including both neural and cardiac preparations, by IR light pulses has been studied extensively and is commonly referred to as IR nerve inhibition (INI). The consensus is that the INI results from temperature-dependent changes of passive membrane properties as well as sodium and potassium ion channel kinetics.…”

“…The consensus is that the INI results from temperature-dependent changes of passive membrane properties as well as sodium and potassium ion channel kinetics. 19 – 24 Due to the precise localization of IR light application and the size of experimental animals, most studies using IR light to inhibit peripheral nerves target a relatively small portion of the nerve. 19 – 21 , 24 Moreover, IR light application to peripheral nerves involves intercepting propagating APs that are depolarized by a strong charging current and typically take off from a resting membrane potential.…”

Spike-frequency dependent inhibition and excitation of neural activity by high-frequency ultrasound

“…As a general principle, thermal neuromodulation effects in response to optical stimulation would be expected to be very similar to thermal neuromodulation effects caused by ultrasound, and studies of optical neuromodulation could therefore provide useful guidance in interpreting our results. However, optically based thermal neuromodulation experiments are highly heterogeneous in terms of the neuromodulation effect, the temperature rise required to produce the effect, and the mechanistic interpretation of the results (Wells et al, 2007;Richter et al, 2011;Shapiro et al, 2012;Duke et al, 2013;Walsh et al, 2016;Lothet et al, 2017;Paris et al, 2017;Owen et al, 2019;Zhu et al, 2019), so their usefulness is limited in this respect. Both inhibition and potentiation of firing have been reported, and the increase in temperature has varied considerably, ranging from less than 1 C to 10's of degrees C. The temperature rise in our simulations is on the low end of this range.…”