Subthreshold Oscillating Waves in Neural Tissue Propagate by Volume Conduction and Generate Interference

Abstract

Subthreshold neural oscillations have been observed in several brain regions and can influence the timing of neural spikes. However, the spatial extent and function of these spontaneous oscillations remain unclear. To study the mechanisms underlying these oscillations, we use optogenetic stimulation to generate oscillating waves in the longitudinal hippocampal slice expressing optopatch proteins. We found that optogenetic stimulation can generate two types of neural activity: suprathreshold neural spikes and subthreshold oscillating waves. Both waves could propagate bidirectionally at similar speeds and go through a transection of the tissue. The propagating speed is independent of the oscillating frequency but increases with increasing amplitudes of the waves. The endogenous electric fields generated by oscillating waves are about 0.6 mV/mm along the dendrites and about 0.3 mV/mm along the cell layer. We also observed that these oscillating waves could interfere with each other. Optical stimulation applied simultaneously at each slice end generated a larger wave in the middle of the tissue (constructive interference) or destructive interference with laser signals in opposite phase. However, the suprathreshold neural spikes were annihilated when they collided. Finally, the waves were not affected by the NMDA blocker (APV) and still propagated in the presence of tetrodotoxin (TTX) but at a significantly lower amplitude. The role of these subthreshold waves in neural function is unknown, but the results show that at low amplitude, the subthreshold propagating waves lack a refractory period allowing a novel analog form of preprocessing of neural activity by interference independent of synaptic transmission.