TY - JOUR
T1 - Hub-organized parallel circuits of central circadian pacemaker neurons for visual photoentrainment in Drosophila
AU - Li, Meng Tong
AU - Cao, Li Hui
AU - Xiao, Na
AU - Tang, Min
AU - Deng, Bowen
AU - Yang, Tian
AU - Yoshii, Taishi
AU - Luo, Dong Gen
N1 - Funding Information:
The eye removal experiments (Supplementary Fig. 3) suggested that the central pacemaker neurons received visual inputs from H–B eyelets or compound eyes, or both. Next, we investigated whether the H–B eyelets provided visual inputs to central circadian pacemaker neurons (Fig. 6a). There are four photoreceptors in each H–B eyelet47. However, the nature of their light responses is unknown. We performed patch-clamp recordings on the eyelet photoreceptors and found that a brief flash of light triggered an inward current that depolarized the eyelet photoreceptor (Fig. 6b). Like the retinal photoreceptors in compound eyes, H–B eyelet photoreceptors did not fire action potentials. Interestingly, H–B eyelet was reported to be able to use a PLC-independent light signaling to photoentrain the flies49. To examine the pho-totransduction mechanisms in H–B eyelet photoreceptors, we next performed patch-clamp recordings on the eyelet photoreceptors of norpA mutant flies and found a complete loss of light-induced electrical responses (Supplementary Fig. 7a). In addition, we found that H–B eyelet photoreceptors lost their light-induced electrical responses in Rhodopsin 6 (Rh6) mutant flies (Supplementary Fig. 7a). These data demonstrated that H–B eyelet photoreceptors detect light with Rh6 through the PLC-mediated phototransduction. This conclusion was further supported by our finding that light-induced electrical responses were restored to the H–B eyelet photoreceptors after rescuing norpA by Rh6-Gal4 in norpA mutant flies (Supplementary Fig. 7b). The light responses of central circadian pacemaker neurons in Rh6[1] flies, which lacked Rh6, were dramatically reduced (Fig. 6c), revealing visual inputs from H–B eyelets. This conclusion was supported by a partial restoration of light responses of circadian
Publisher Copyright:
© 2018, The Author(s).
PY - 2018/12/1
Y1 - 2018/12/1
N2 - Circadian rhythms are orchestrated by a master clock that emerges from a network of circadian pacemaker neurons. The master clock is synchronized to external light/dark cycles through photoentrainment, but the circuit mechanisms underlying visual photoentrainment remain largely unknown. Here, we report that Drosophila has eye-mediated photoentrainment via a parallel pacemaker neuron organization. Patch-clamp recordings of central circadian pacemaker neurons reveal that light excites most of them independently of one another. We also show that light-responding pacemaker neurons send their dendrites to a neuropil called accessary medulla (aMe), where they make monosynaptic connections with Hofbauer–Buchner eyelet photoreceptors and interneurons that transmit compound-eye signals. Laser ablation of aMe and eye removal both abolish light responses of circadian pacemaker neurons, revealing aMe as a hub to channel eye inputs to central circadian clock. Taken together, we demonstrate that the central clock receives eye inputs via hub-organized parallel circuits in Drosophila.
AB - Circadian rhythms are orchestrated by a master clock that emerges from a network of circadian pacemaker neurons. The master clock is synchronized to external light/dark cycles through photoentrainment, but the circuit mechanisms underlying visual photoentrainment remain largely unknown. Here, we report that Drosophila has eye-mediated photoentrainment via a parallel pacemaker neuron organization. Patch-clamp recordings of central circadian pacemaker neurons reveal that light excites most of them independently of one another. We also show that light-responding pacemaker neurons send their dendrites to a neuropil called accessary medulla (aMe), where they make monosynaptic connections with Hofbauer–Buchner eyelet photoreceptors and interneurons that transmit compound-eye signals. Laser ablation of aMe and eye removal both abolish light responses of circadian pacemaker neurons, revealing aMe as a hub to channel eye inputs to central circadian clock. Taken together, we demonstrate that the central clock receives eye inputs via hub-organized parallel circuits in Drosophila.
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U2 - 10.1038/s41467-018-06506-5
DO - 10.1038/s41467-018-06506-5
M3 - Article
C2 - 30315165
AN - SCOPUS:85054893956
SN - 2041-1723
VL - 9
JO - Nature Communications
JF - Nature Communications
IS - 1
M1 - 4247
ER -