Bidirectional modulation of evoked synaptic transmission by pulsed infrared light

Abstract

Infrared (IR) neuromodulation (INM) has been demonstrated as a novel modulation modality of neuronal excitability. However, the effects of pulsed IR light on synaptic transmission have not been investigated systematically. In this report, the IR light (2 μm) is used to directly modulate evoked synaptic transmission at the crayfish opener neuromuscular junction. The extracellularly recorded terminal action potentials (tAPs) and evoked excitatory postsynaptic currents (EPSCs) modulated by localized IR light illumination (500 ms, 3–13 mW) aimed at the synapses are analyzed. The impact of a single IR light pulse on the presynaptic Ca2+ influx is monitored with Ca2+ indicators. The EPSC amplitude is enhanced, and its rising phase is accelerated under relatively low IR light power levels and localized temperature rises. Increasing the IR light power reversibly suppresses and eventually blocks the EPSCs. Meanwhile, the synaptic delay, tAP amplitude, and presynaptic Ca2+ influx decrease monotonously with higher IR light power. It is demonstrated for the first time that IR light illumination has bidirectional effects on evoked synaptic transmission. These results highlight the efficacy and flexibility of using pulsed IR light to directly control synaptic transmission and advance our understanding of INM of neural networks.

Infrared neuromodulation—a review

“…However, it was suggested that Na + channels do not play as significant a role for an IR light block of the CAP propagation. A more recent study [117] also identified an IR light-induced K + channel-mediated potential component in the crayfish motor axons capable of disrupting any rhythmic axonal AP firing. Its amplitude and polarity were dependent on the membrane potential.…”

“…IR light irradiation aimed onto the presynaptic neuronal soma or axon has been shown to enhance the spontaneous inhibitory postsynaptic currents via altering the GABAergic neurotransmission in rat cortical neuron cultures [54]. Moreover, the direct contribution from synapses under pulsed IR light [117] in the case of illuminating neuronal networks should also be incorporated (see section 6.1 below). [29,35,39] and even potentially higher, without inducing histological damage in neurons [44,[118][119][120] or astrocytes [121].…”

“…In order to isolate the IR light effect on synaptic function, ideally pulsed IR light should be restricted to the synapses, and the direct responses should be monitored and studied. Our recent study [117] discovered that pulsed IR light (λ = 1.994 µm, D = 50 µm, τ = 500 ms, P = 3-13 mW) specifically targeting the crayfish motor synapses can modulate AP-evoked synaptic transmission in both the directions of stimulation and inhibition: lower temperature rises tend to enhance synaptic transmission and higher temperature rises can suppress and even reversibly block evoked synaptic transmission. We concluded that this bidirectional modulation of evoked synaptic transmission was due to the different temperature sensitivities of the various synaptic events.…”

“…We concluded that this bidirectional modulation of evoked synaptic transmission was due to the different temperature sensitivities of the various synaptic events. Moreover, when compared to axons, synapses seem to have a higher sensitivity to IR light-induced temperature transients [103,117]. This suggests that the selection of the illuminated targets even at the subcellular levels can play a critical role in determining the outcomes of INM and that synapses could form a major player in INM of neuronal networks and brain in vivo.…”

Two-photon imaging of excitatory and inhibitory neural response to infrared neural stimulation

“…To date, our understanding of neuronal response is still rudimentary. The underlying mechanism of action is unknown [16][17][18][19][20][21][22][23] and the effect on responses of different neuronal subtypes as well as different physiological states in vivo at a cellular level is still lacking. In particular, even though INS has been shown to induce BOLD activation at distant cortical sites in fMRI studies, little is known about the cellular circuits contributions to this functional connectivity result.…”