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

" 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." {Credits 1}

" The subthreshold waves in the present study can propagate with wavelengths consistent with those observed in the rodent hippocampus [10] or the surface of the human hippocampus [11]. The spatial wavelength of these oscillating waves is in the millimeter range and the rodent hippocampus is several millimeters long. Therefore, a subthreshold wave propagating with a frequency in the theta range and wavelength of about 14 mm (Figure 3A), will encompass the entire rodent hippocampus. Furthermore, these subthreshold waves can propagate non-synaptic ally across the hippocampal slice at various frequency bands with similar speeds (Figure 2D). A propagation speed independent of frequency ensures minimum distortion during propagation and therefore, implies that there exists in the hippocampus a mechanism that allows analog propagation of neural activity along the hippocampus that is both distortion-free within a narrow frequency range and independent of synaptic transmission." {Credits 1}

" In summary, the present study shows that optogenetic stimulation can trigger propagating subthreshold waves in the hippocampus tissue. These subthreshold waves can propagate across a transection, suggesting that electric field coupling is responsible for the propagation. Furthermore, the subthreshold waves can interfere with each other. These results suggest that the neural tissue is wired to allow propagation of waves producing interference patterns with or without synaptic transmission. Although the function of the subthreshold waves in the neural network is unknown, the results described above open the possibility that signal processing of very low amplitude signals could produce interfering patterns below the threshold of neural firing, leading to new level of analog neural computation across neural networks not previously described." {Credits 1}

{Credits 1} 🎪 Chiang, C.-C.; Durand, D.M. Subthreshold Oscillating Waves in Neural Tissue Propagate by Volume Conduction and Generate Interference. Brain Sci. 2023, 13, 74. https://doi.org/10.3390/brainsci13010074. © 2022 The Authors. This article is licensed under a Creative Commons Attribution International 4.0 License..