Neuronal synchronization in Drosophila

Abstract

Rhythms are intrinsic to biological processes across temporal and spatial scales. In the brain, the synchronized oscillatory activity of neurons creates collective rhythms that are essential for complex functions. While this is a recognized phenomenon in the mammalian brain, information about insect neuronal synchrony and its underlying mechanisms is scarce. In the fly brain, neuronal oscillations were reported in individual lateral ventral neurons (LNvs), which play a key role in circadian and sleep behaviors. However, it is still unclear whether and how these participate in a collective rhythm. In this work, we perform thorough whole-cell patch clamp recordings of LNvs, and demonstrate consistent membrane potential oscillations. We show that oscillations degrade over time, and disappear upon exposure to an acetylcholine receptor blocker. Together with a flat phase response curve, these results suggest that oscillations are exogenously produced. Prompted by these results, we propose a generic forced oscillator theory that can account for the experimental phase response. The theory further predicts that neurons with similar properties should oscillate in synchrony with zero lags, while neurons with different properties may show coherent oscillations with non-zero lags. We confirm this prediction through simultaneous patch clamp recordings of neuronal pairs, revealing that large LNvs are consistently advanced relative to small LNvs. Additionally, we find that other neurons in the accessory medulla also exhibit coherent membrane potential oscillations, with diverse lags. Our findings suggest the intriguing possibility that brain waves may arise from collective neuronal activity within this region of the fly brain.