Oscillatory brain activity in spontaneous and induced sleep stages in flies

Abstract

Sleep is a dynamic process comprising multiple stages, each associated with distinct electrophysiological properties and potentially serving different functions. While these phenomena are well described in vertebrates, it is unclear if invertebrates have distinct sleep stages. We perform local field potential (LFP) recordings on flies spontaneously sleeping, and compare their brain activity to flies induced to sleep using either genetic activation of sleep-promoting circuitry or the GABAA agonist Gaboxadol. We find a transitional sleep stage associated with a 7–10 Hz oscillation in the central brain during spontaneous sleep. Oscillatory activity is also evident when we acutely activate sleep-promoting neurons in the dorsal fan-shaped body (dFB) of Drosophila. In contrast, sleep following Gaboxadol exposure is characterized by low-amplitude LFPs, during which dFB-induced effects are suppressed. Sleep in flies thus appears to involve at least two distinct stages: increased oscillatory activity, particularly during sleep induction, followed by desynchronized or decreased brain activity.

Isoflurane Impairs Low-Frequency Feedback but Leaves High-Frequency Feedforward Connectivity Intact in the Fly Brain

“…Such an increase has not been reported for insects (van Swinderen, 2006; Kirszenblat and van Swinderen, 2015), and we did not observe this here (the results did not change with longer time window (18 s) and/or using a unipolar reference scheme [data not shown]). Interestingly, a recent study reported that sleep induction in flies is accompanied by an increase in 7–10 Hz LFPs power (Yap et al, 2017). However, this was not observed for pharmacologically induced sleep, so any relevance to general anesthesia remains unknown.…”

“…Previous work has shown that the fly heartbeat can manifest as low-frequency (2–4 Hz) oscillatory activity in central channels (Paulk et al, 2013b; Yap et al, 2017). Heartbeats are unlikely to affect the results presented here because we use bipolar rereferencing which eliminates common input to neighboring channels, as may be expected from a muscle artifact (Cohen and Tsuchiya, 2017).…”

Network-specific synchronization of electrical slow-wave oscillations regulates sleep in Drosophila

“…However, in invertebrates it is unknown whether neural oscillations can gate specific behaviors, and whether an electrophysiological sleep correlate, such as slowwave oscillations, exists or is involved in sleep regulation. Local field potential (LFP) measurements in the Drosophila brain indicate that the frequency of large scale compound neuronal activity is reduced during sleep [8][9][10] opening up the possibility that, comparable to vertebrates, slow oscillatory activity could be involved in mediating sleep. Yet, such oscillations so far have not been identified and it remains unknown, which and how neural networks would generate slow-wave oscillations that could be crucial for sleep regulation.…”

A circadian output circuit controls sleep-wake arousal threshold in Drosophila

“…Although there is nothing known about the neuronal mechanism underlying these oscillations nor their purpose (if any), recent work in flies reported increased 7-10 Hz oscillations within the central brain during spontaneous sleep. Although this is much more rapid than mammalian delta waves (Yap et al, 2017), it is tempting to connect these oscillations as well as those we have observed to mammalian sleep. Moreover, it will be interesting to test whether APDN firing can produce similar oscillations or local field potential changes in other sleep-relevant central brain regions like dFSB.…”

“…Sleep in diverse systems is characterized by a set of common features. They include reduced locomotor activity, increased arousal threshold and altered neuronal oscillation patterns in higher brain centers (Yap et al, 2017). Although there is no single mechanism that can account for all these features, we present here a novel anatomical circuit in the fly brain that influences all of them.…”