Abstract
The circadian clock of the nocturnal Madeira cockroach is located in the accessory medulla, a small nonretinotopic neuropil in the brain’s visual system. The clock comprises about 240 neurons that control rhythms in physiology and behavior such as sleep-wake cycles. The clock neurons contain an abundant number of partly colocalized neuropeptides, among them pigment-dispersing factor (PDF), the insects’ most important circadian coupling signal that controls sleep-wake rhythms. We performed long-term loose-patch clamp recordings under 12:12-hr light-dark cycles in the cockroach clock in vivo. A wide range of timescales, from milliseconds to seconds, were found in spike and field potential patterns. We developed a framework of wavelet transform–based methods to detect these multiscale electrical events. We analyzed frequencies and patterns of events with interesting dynamic features, such as mixed-mode oscillations reminiscent of sharp-wave ripples. Oscillations in the beta/gamma frequency range (20–40 Hz) were observed to rise at dawn, when PDF is released, peaking just before the onset of locomotor activity of the nocturnal cockroach. We expect that in vivo electrophysiological recordings combined with neuropeptide/antagonist applications and behavioral analysis will determine whether specific patterns of electrical activity recorded in the network of the cockroach circadian clock are causally related to neuropeptide-dependent control of behavior.
Highlights
Rhythms in animals are generated by complex interplays of molecular and cellular feedback loops and by network synchronizations producing temporally structured outputs
For the first time, we gained information about recurring events, oscillations, and network dynamics from a circadian clock receiving sensory information from the compound eyes, as well as phase information from both bilaterally symmetric clocks in the cockroach. Based upon these in vivo recordings, we developed a framework for the analysis of the activity of the circadian clock network over different timescales
To search for Zeitgeber time (ZT)-dependent changes of activity in a circadian clock that are indicative of neuropeptide actions, we performed 24- to 48-hr-long in vivo loose-patch clamp (∼ 1 Gigaohm seal) recordings of the accessory medulla (AME), the circadian clock of the Madeira cockroach (n = 18)
Summary
Rhythms in animals are generated by complex interplays of molecular and cellular feedback loops (biological clocks) and by network synchronizations producing temporally structured outputs. Best studied are the pigment-dispersing factor (PDF)-expressing clock neurons that control circadian sleep-wake rhythms in the cockroach, and in other insects such as the fruit fly Drosophila melanogaster (Figure 1A; reviews: Hermann-Luibl & Helfrich-Foerster, 2015; Stengl & Arendt, 2016). To resemblance of PDF’s and VIP’s circadian functions, the cellular and molecular organization of the cockroach and the mammalian clock resemble each other (Vansteensel, Michel, & Meijer, 2008). Both clocks are abundant with neuropeptides that do not require direct synaptic connectivity (Patton & Hastings, 2018). Circadian clocks with their numerous colocalized neuropeptides are well suited for the study of neuropeptide actions/functions in general
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