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

Abstract

Significance: Systematic studies of the physiological outputs induced by infrared (IR)-mediated inhibition of motor nerves can provide guidance for therapeutic applications and offer critical insights into IR light modulation of complex neural networks. Aim: We explore the IR-mediated inhibition of action potentials (APs) that either propagate along single axons or are initiated locally and their downstream synaptic transmission responses. Approach: APs were evoked locally by two-electrode current clamp or at a distance for propagating APs. The neuromuscular transmission was recorded with intracellular electrodes in muscle cells or macro-patch pipettes on terminal bouton clusters. Results: IR light pulses completely and reversibly terminate the locally initiated APs firing at low frequencies, which leads to blocking of the synaptic transmission. However, IR light pulses only suppress but do not block the amplitude and duration of propagating APs nor locally initiated APs firing at high frequencies. Such suppressed APs do not influence the postsynaptic responses at a distance. While the suppression of AP amplitude and duration is similar for propagating and locally evoked APs, only the former exhibits a 7% to 21% increase in the maximum time derivative of the AP rising phase. Conclusions: The suppressed APs of motor axons can resume their waveforms after passing the localized IR light illumination site, leaving the muscular and synaptic responses unchanged. IR-mediated modulation on propagating and locally evoked APs should be considered as two separate models for axonal and somatic modulations.

Bidirectional modulation of evoked synaptic transmission by pulsed infrared light

“…The parameters measured from the first five tAPs fluctuated randomly around zero and started a downward trend when the IR light pulse was turned on between the 5th and 6th stimuli. The maximum reduction of the tAP amplitude was around 15%, which was comparable to the reduction in propagating axonal AP amplitude recorded intracellularly 39 . The maximum reduction of the tAP peak timing was ~ 80 μs.…”

“…In a previous study with the same preparation, we found that, although a single localized IR light pulse can successfully suppress propagating axonal APs by reducing their amplitudes and duration, this suppression may have little effects on the downstream synaptic transmission due to the recovery of the AP waveforms once the suppressed APs propagated beyond the illuminated regions 39 . Here, we show that when the same IR light pulse was aimed directly at synapses, the synaptic transmission could be reversibly enhanced, suppressed, and blocked.…”

“…IR light effects on terminal APs. Our previous study showed that IR light pulse can suppress the amplitude and duration of propagating APs recorded in the main trunk of the motor axon 39 . Though in the current study the axonal APs recorded around the main branching point remained completely unchanged (Supplementary Fig.…”

“…For example, when IR light pulses were applied to the presynaptic neuronal soma or axon of cultured rat neurons, the spontaneous inhibitory postsynaptic currents were altered in their amplitude, frequency, and decay time constant 38 . Our previous study with the crayfish neuromuscular preparation demonstrated the feasibility of changing postsynaptic potentials by modulating presynaptic axonal action potentials (APs) 39 . In the vestibular system, it has also been demonstrated that IR light pulses changed afferent nerve firing via IR light modulation of presynaptic hair cells 25 , 37 .…”

Two-photon GCaMP6f imaging of infrared neural stimulation evoked calcium signals in mouse cortical neurons in vivo

“…This is usually achieved through viral transfections, which—despite their good controllability and the advantage of offering cell type specificity through the use of a promoter—, strongly limits applicability in humans. This is not the case for infrared neural stimulation (INS), an alternative to optogenetics, which has gained more and more interest in the last decade 4 – 8 , as it has the same advantages as optogenetics, yet without requiring any genetic manipulation. Indeed, in this case, the infrared radiation (typically around 1470 nm, 1860 nm or 2120 nm) 9 interacts directly with the biological tissue without the need of any exogenous agents, thus offering numerous advantages for translation to clinical applications.…”