The role of PDF neurons in setting the preferred temperature before dawn in Drosophila

Abstract

Animals have sophisticated homeostatic controls. While mammalian body temperature fluctuates throughout the day, small ectotherms, such as Drosophila achieve a body temperature rhythm (BTR) through their preference of environmental temperature. Here, we demonstrate that pigment dispersing factor (PDF) neurons play an important role in setting preferred temperature before dawn. We show that small lateral ventral neurons (sLNvs), a subset of PDF neurons, activate the dorsal neurons 2 (DN2s), the main circadian clock cells that regulate temperature preference rhythm (TPR). The number of temporal contacts between sLNvs and DN2s peak before dawn. Our data suggest that the thermosensory anterior cells (ACs) likely contact sLNvs via serotonin signaling. Together, the ACs-sLNs-DN2s neural circuit regulates the proper setting of temperature preference before dawn. Given that sLNvs are important for sleep and that BTR and sleep have a close temporal relationship, our data highlight a possible neuronal interaction between body temperature and sleep regulation.DOI: http://dx.doi.org/10.7554/eLife.23206.001

Thermosensory perception regulates speed of movement in response to temperature changes inDrosophila melanogaster

“…However, the studies on daily entrainment have not systematically concluded that either dTrpA1 or AC neurons are fundamental for temperature entrainment (Das et al, 2015;Lee and Montell, 2013;Roessingh et al, 2015). So far, dTrpA1 expression has been observed only in subsets of clock neurons (Das et al, 2016;Lee and Montell, 2013;Yoshii et al, 2015), and AC neurons have been related to temperature preference but not to temperature entrainment (Tang et al, 2017). This suggests that the central system of Drosophila thermal behavior has a high level of complexity beyond AC neurons that allows an efficient and detailed detection of thermal stimuli and their integration with other internal states to coordinate the most efficient behavioral response.…”

Neuroanatomical details of the lateral neurons of Drosophila melanogaster support their functional role in the circadian system

“…Even before this study, it has been well established that the clock neurons form a vastly overlapping network (Helfrich‐Förster, ; Helfrich‐Förster et al, ), which integrates multisensory inputs (e.g., light and temperature cues) from the environment (Helfrich‐Förster et al, ; Yoshii, Sakamoto, & Tomioka, ; Yoshii et al, ; Busza, Murad, & Emery, ; Yoshii et al, ; Veleri, Rieger, Helfrich‐Förster, & Stanewsky, ; Picot, Klarsfeld, Chélot, Malpel, & Rouyer, ; Sehadova et al, ; Yoshii, Vanin, Costa, & Helfrich‐Förster, ; Kaneko et al, ; Buhl et al, ; Harper, Dayan, Albert, & Stanewsky, ; Tang et al, ). Although Drosophila 's clock has been shown to have an implication on the fly's metabolism (Xu, Zheng, & Sehgal, ; Xu, DiAngelo, Hughes, Hogenesch, & Sehgal, ), sleep (Hendricks et al, ; Shaw, Cirelli, Greenspan, & Tononi, ; Hendricks et al, ), the control of locomotor rhythms (Konopka & Benzer, ; Handler & Konopka, ; Helfrich & Engelmann, ), the gating of eclosion and metamorphosis (Pittendrigh & Skopik, ; Konopka & Benzer, ; Hamblen‐Coyle, Wheeler, Rutila, Rosbash, & Hall, ; Sehgal, Price, Man, & Young, ; Myers, Yu, & Sehgal, ), as well as on learning and memory (Lyons & Roman, ; Fropf et al, ; Chouhan, Wolf, Helfrich‐Förster, & Heisenberg, ), the coverage of specific connections to downstream neurons of the circadian network still lags behind.…”

“…Particularly the analysis of putative in‐ and output sites, showing the presynaptic nature of the E‐cells' projections in that region, furthermore suggests the PI as a target of multiple clock neurons. Since the s‐LN v s (Fernández, Berni, & Ceriani, ; Sivachenko, Li, Abruzzi, & Rosbash, ; Gorostiza, Depetris‐Chauvin, Frenkel, Pírez, & Ceriani, ; Petsakou, Sapsis, & Blau, ) and the DN 2 (Tang et al, ) are reported to undergo activity‐dependent circadian remodeling, it is likely, that also other clock neurons experience neuronal circadian plasticity. We controlled this effect in our study by collecting and fixing all samples at a particular time‐point (ZT23).…”

Molecular and circuit mechanisms mediating circadian clock output in the Drosophila brain

“…The DN2s also have temperature‐entrainable molecular clocks and regulate rhythms of temperature preference, namely the tendency of flies to seek different temperatures at different times of day (Kaneko et al., ; Yoshii et al., ). A circuit for temperature preference at dawn has been mapped from the thermosensory anterior cells to s‐LNvs to DN2s (Tang et al., ). The molecular clocks in LPNs are also strongly synchronized to temperature cycles (Miyasako, Umezaki, & Tomioka, ).…”

“…Presumably, the increased terminal complexity indicates more synaptic connections. Indeed, using the GRASP (GFP reconstitution across synaptic partners) assay, which labels synaptic contacts between two populations of neurons, the number of contacts between s‐LNv and their partners were found to be higher during the day than in the evening (Gorostiza, Depetris‐Chauvin, Frenkel, Pírez, & Ceriani, ; Tang et al., ). As such, the structural plasticity of s‐LNv projections is a circadian output rhythm, regulated by the molecular clock and maintained in constant darkness (Fernández et al., ).…”