Circadian clock neurons constantly monitor environmental temperature to set sleep timing

Abstract

Circadian clocks coordinate behaviour, physiology and metabolism with Earth's diurnal cycle. These clocks entrain to both light and temperature cycles, and daily environmental temperature oscillations probably contribute to human sleep patterns. However, the neural mechanisms through which circadian clocks monitor environmental temperature and modulate behaviour remain poorly understood. Here we elucidate how the circadian clock neuron network of Drosophila melanogaster processes changes in environmental temperature. In vivo calcium-imaging techniques demonstrate that the posterior dorsal neurons 1 (DN1s), which are a discrete subset of sleep-promoting clock neurons, constantly monitor modest changes in environmental temperature. We find that these neurons are acutely inhibited by heating and excited by cooling; this is an unexpected result when considering the strong correlation between temperature and light, and the fact that light excites clock neurons. We demonstrate that the DN1s rely on peripheral thermoreceptors located in the chordotonal organs and the aristae. We also show that the DN1s and their thermosensory inputs are required for the normal timing of sleep in the presence of naturalistic temperature cycles. These results identify the DN1s as a major gateway for temperature sensation into the circadian neural network, which continuously integrates temperature changes to coordinate the timing of sleep and activity.

Connectomics analysis reveals first, second, and third order thermosensory and hygrosensory neurons in the adultDrosophilabrain

“…We also identified 8 new classes of lACA-associated neurons, most of which connect, not to Kenyon cells, but rather to each other and/or as yet unidentified neurons in other neuropils. Intriguingly, we discovered circadian clock neurons DN1a and DN1p innervating the lACA, thus potentially mediating temperature-based entrainment [49] or, alternatively, modulating temperature preference, which fluctuates with a daily rhythm in animals from flies to humans [50]. Three of the lACA network's main output neuropils are the LH, SMP, and antlers, all previously associated with olfactory responses [51]; in particular, the SMP features both DAN inputs and MBON outputs [40].…”

Insulin Producing Cells Monitor the Cold and Compensate the Cold-Induced Sleep in Drosophila

“…For instance, the important circadian protein PER and TIM protein are thermosensitive, and are found to mediate the thermoregulation of circadian [10]. Circuit level mechanism is poorly examined but DN1 neuron has been found to monitor the cold and set sleep timing [11]. Previous work in our lab confirmed that insulin producing cells(IPCs) in larva brain can sense cold through synaptic connection with the cold sensing neuron named 11216 [12].…”

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

“…The circadian circuit is anatomically dispersed with most of the important circadian neurons on the lateral or dorsal surface of brain; they are therefore well-positioned to sense the environment, for example light and temperature fluctuations (Yadlapalli et al, 2018;Zhang et al, 2010b) . However, it is still unclear how this sensory information is integrated with circadian timekeeping and then processed to change central brain activity patterns and most importantly to influence the status of wake/sleep and arousal levels.…”