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The Journal of Neuroscience, June 18, 2008, 28(25):6493-6501; doi:10.1523/JNEUROSCI.1503-08.2008

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Cellular/Molecular
Circadian Control of Membrane Excitability in Drosophila melanogaster Lateral Ventral Clock Neurons

Guan Cao and Michael N. Nitabach

Department of Cellular and Molecular Physiology, School of Medicine, Yale University, New Haven, Connecticut 06520

Correspondence should be addressed to Dr. Michael N. Nitabach, Department of Cellular and Molecular Physiology, School of Medicine, Yale University, New Haven, CT 06520. Email: michael.nitabach{at}yale.edu

Drosophila circadian rhythms are controlled by a neural circuit containing 150 clock neurons. Although much is known about mechanisms of autonomous cellular oscillation, the connection between cellular oscillation and functional outputs that control physiological and behavioral rhythms is poorly understood. To address this issue, we performed whole-cell patch-clamp recordings on lateral ventral clock neurons (LN_vs), including large (lLN_vs) and small LN_vs (sLN_vs), in situ in adult fly whole-brain explants. We found two distinct sizes of action potentials (APs) in >50% of lLN_vs that fire APs spontaneously, and determined that large APs originate in the ipsilateral optic lobe and small APs in the contralateral. lLN_v resting membrane potential (RMP), spontaneous AP firing rate, and membrane resistance are cyclically regulated as a function of time of day in 12 h light/dark conditions (LD). lLN_v RMP becomes more hyperpolarized as time progresses from dawn to dusk with a concomitant decrease in spontaneous AP firing rate and membrane resistance. From dusk to dawn, lLN_v RMP becomes more depolarized, with spontaneous AP firing rate and membrane resistance remaining stable. In contrast, circadian defective per⁰ null mutant lLN_v membrane excitability is nearly constant in LD. Over 24 h in constant darkness (DD), wild-type lLN_v membrane excitability is not cyclically regulated, although RMP gradually becomes slightly more depolarized. sLN_v RMP is most depolarized around lights-on, with substantial variability centered around lights-off in LD. Our results indicate that LN_v membrane excitability encodes time of day via a circadian clock-dependent mechanism, and likely plays a critical role in regulating Drosophila circadian behavior.

Key words: circadian rhythms; Drosophila; membrane excitabiliy; time of day; clock neuron; cellular oscillation

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Received Oct. 18, 2007; revised May 9, 2008; accepted May 12, 2008.

Correspondence should be addressed to Dr. Michael N. Nitabach, Department of Cellular and Molecular Physiology, School of Medicine, Yale University, New Haven, CT 06520. Email: michael.nitabach{at}yale.edu

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