Circadian- and Light-Dependent Regulation of Resting Membrane Potential and Spontaneous Action Potential Firing of <i>Drosophila</i> Circadian Pacemaker Neurons

Sheeba, Vasu; Gu, Huaiyu; Sharma, Vijay Kumar; O’Dowd, Diane K.; Holmes, Todd C.

doi:10.1152/jn.00930.2007

Cited by 182 publications

(238 citation statements)

References 63 publications

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“…One recent study that recorded electrophysiologically from l-LNvs showed that neuronal firing is light-stimulated (17). This report also showed that light-mediated firing during the light phase was substantially (2/3) reduced in a mutant cry background, consistent with direct photoreception by l-LNvs in our behavioral studies.…”

Section: Discussionsupporting

confidence: 89%

“…Although we do not detect direct projections from l-LNvs to these regions (data not shown), secreted PDF may still be able to reach EB PDFR. Because l-LNvs increase firing rate in response to light (17), PDF secretion from these cells may be light-regulated. This is consistent with the fact that both PDF null and PDF-receptor hypomorphic mutants showed increased daytime sleep (36).…”

Section: Discussionmentioning

confidence: 99%

“…The 10 l-LNvs (5 on each side of the brain) are among the first circadian neurons identified in Drosophila (14), and there are some indications that they may function as coincident detectors for light (9,12,(15)(16)(17). However, they have never been assigned a circadian or behavioral function, because there are no tools available to selectively address their function.…”

mentioning

confidence: 99%

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Light-arousal and circadian photoreception circuits intersect at the large PDF cells of the Drosophila brain

Shang

Griffith

Rosbash

2008

Proc. Natl. Acad. Sci. U.S.A.

272

277

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The neural circuits that regulate sleep and arousal as well as their integration with circadian circuits remain unclear, especially in Drosophila. This issue intersects with that of photoreception, because light is both an arousal signal in diurnal animals and an entraining signal for the circadian clock. To identify neurons and circuits relevant to light-mediated arousal as well as circadian phase-shifting, we developed genetic techniques that link behavior to single cell-type resolution within the Drosophila central brain. We focused on the unknown function of the 10 PDFcontaining large ventral lateral neurons (l-LNvs) of the Drosophila circadian brain network and show here that these cells function in light-dependent arousal. They also are important for phase shifting in the late-night (dawn), indicating that the circadian photoresponse is a network property and therefore non-cell-autonomous. The data further indicate that the circuits underlying light-induced arousal and circadian photoentrainment intersect at the l-LNvs and then segregate.L ight promotes arousal in diurnal species. Drosophila arousalsleep circuits remain largely uncharacterized. Exceptions are the mushroom body with a role in sleep-arousal (1, 2) as well as neurons of the pars intercerebralis (PI) and the ellipsoid body (EB) of the central complex (CC) with roles in locomotion (3, 4). Importantly, there is no indication of how the poorly understood fly sleep-movement circuits are coordinated or communicate with the well-studied brain circadian network, or whether these Ϸ150 circadian neurons impact directly on sleep or arousal.

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Section: Discussionsupporting

confidence: 89%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Light-arousal and circadian photoreception circuits intersect at the large PDF cells of the Drosophila brain

Shang

Griffith

Rosbash

2008

Proc. Natl. Acad. Sci. U.S.A.

272

277

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“…lLNv neurons were identified using eGFP tag and recorded in whole cell current clamp or voltage clamp modes based on their better accessibility relative to sLNv neurons. Although immunocytochemical studies suggest that oscillations in PER, TIM or PDP-1 protein levels do not persist in lLNv in prolonged DD in contrast to the sLNv, our studies suggest that in fact membrane electrical properties continue to show circadian oscillation in DD in these neurons (Sheeba et al, 2008). Furthermore, mRNA levels of tim has been shown to exhibit robust oscillation in lLNv for up to 8 d in DD (Peng et al, 2003;Stoleru et al, 2005).…”

Section: Electrophysiological Properties Of Lnv Neurons Are Altered Bcontrasting

confidence: 63%

Pigment Dispersing Factor-Dependent and -Independent Circadian Locomotor Behavioral Rhythms

Sheeba

Sharma²,

Gu³

et al. 2008

J. Neurosci.

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Circadian pacemaker circuits consist of ensembles of neurons, each expressing molecular oscillations, but how circuit-wide coordination of multiple oscillators regulates rhythmic physiological and behavioral outputs remains an open question. To investigate the relationship between the pattern of oscillator phase throughout the circadian pacemaker circuit and locomotor activity rhythms in Drosophila, we perturbed the electrical activity and pigment dispersing factor (PDF) levels of the lateral ventral neurons (LNv) and assayed their combinatorial effect on molecular oscillations in different parts of the circuit and on locomotor activity behavior. Altered electrical activity of PDF-expressing LNv causes initial behavioral arrhythmicity followed by gradual long-term emergence of two concurrent short-and long-period circadian behavioral activity bouts in ϳ60% of flies. Initial desynchrony of circuit-wide molecular oscillations is followed by the emergence of a novel pattern of period (PER) synchrony whereby two subgroups of dorsal neurons (DN1 and DN2) exhibit PER oscillation peaks coinciding with two activity bouts, whereas other neuronal subgroups exhibit a single PER peak coinciding with one of the two activity bouts. The emergence of this novel pattern of circuit-wide oscillator synchrony is not accompanied by concurrent change in the electrical activity of the LNv. In PDF-null flies, altered electrical activity of LNv drives a short-period circadian activity bout only, indicating that PDF-independent factors underlie the short-period circadian activity component and that the long-period circadian component is PDF-dependent. Thus, polyrhythmic behavioral patterns in electrically manipulated flies are regulated by circuit-wide coordination of molecular oscillations and electrical activity of LNv via PDF-dependent and -independent factors.

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“…phototransduction | potassium channel | redox | cryptochrome C RYPTOCHROME (CRY) is a photoreceptor that mediates rapid membrane depolarization and increased spontaneous action potential firing rate in response to blue light in arousal and circadian neurons in Drosophila melanogaster (1,2). CRY regulates circadian entrainment by targeting circadian clock proteins to proteasomal degradation in response to light (3)(4)(5)(6).…”

mentioning

confidence: 99%

CRYPTOCHROME-mediated phototransduction by modulation of the potassium ion channel β-subunit redox sensor

Fogle

Baik

Houl

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

120

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Blue light activation of the photoreceptor CRYPTOCHROME (CRY) evokes rapid depolarization and increased action potential firing in a subset of circadian and arousal neurons in Drosophila melanogaster. Here we show that acute arousal behavioral responses to blue light significantly differ in mutants lacking CRY, as well as mutants with disrupted opsin-based phototransduction. Lightactivated CRY couples to membrane depolarization via a well conserved redox sensor of the voltage-gated potassium (K + ) channel β-subunit (Kvβ) Hyperkinetic (Hk). The neuronal light response is almost completely absent in hk −/− mutants, but is functionally rescued by genetically targeted neuronal expression of WT Hk, but not by Hk point mutations that disable Hk redox sensor function. Multiple K + channel α-subunits that coassemble with Hk, including Shaker, Ether-a-go-go, and Ether-a-go-go-related gene, are ion conducting channels for CRY/Hk-coupled light response. Light activation of CRY is transduced to membrane depolarization, increased firing rate, and acute behavioral responses by the Kvβ subunit redox sensor.phototransduction | potassium channel | redox | cryptochrome

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Circadian- and Light-Dependent Regulation of Resting Membrane Potential and Spontaneous Action Potential Firing of Drosophila Circadian Pacemaker Neurons

Cited by 182 publications

References 63 publications

Light-arousal and circadian photoreception circuits intersect at the large PDF cells of the Drosophila brain

Light-arousal and circadian photoreception circuits intersect at the large PDF cells of the Drosophila brain

Pigment Dispersing Factor-Dependent and -Independent Circadian Locomotor Behavioral Rhythms

CRYPTOCHROME-mediated phototransduction by modulation of the potassium ion channel β-subunit redox sensor

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