Differentially Timed Extracellular Signals Synchronize Pacemaker Neuron Clocks

Collins, Ben; Kaplan, Harris S.; Cavey, Matthieu; Lelito, Katherine R.; Bahle, Andrew; Zhu, Z.; Macara, Ann Marie; Roman, Gregg; Shafer, Orie T.; Blau, Justin

doi:10.1371/journal.pbio.1001959

Cited by 48 publications

(55 citation statements)

References 67 publications

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“…Inputs from other clock neurons help synchronize individual s-LNv molecular clocks and regulate their neuronal activity (Collins et al, 2012; Collins et al, 2014). Since EM studies of s-LNv axonal projections had revealed they have input synapses (Yasuyama and Meinertzhagen, 2010), we tested if s-LNv plasticity is also associated with altered accumulation of post-synaptic components.…”

Section: Resultsmentioning

confidence: 99%

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Circadian Rhythms in Rho1 Activity Regulate Neuronal Plasticity and Network Hierarchy

Petsakou

Sapsis

Blau

2015

Cell

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144

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Summary Neuronal plasticity helps animals learn from their environment. However, it is challenging to link specific changes in defined neurons to altered behavior. Here we focus on circadian rhythms in the structure of the principal s-LNv clock neurons in Drosophila. By quantifying neuronal architecture, we observed that s-LNv structural plasticity changes the amount of axonal material in addition to cycles of fasciculation and defasciculation. We found that this is controlled by rhythmic Rho1 activity that retracts s-LNv axonal termini by increasing myosin phosphorylation and simultaneously changes the balance of pre-synaptic and dendritic markers. This plasticity is required to change clock network hierarchy and allow seasonal adaptation. Rhythms in Rho1 activity are controlled by clock-regulated transcription of Puratrophin-1-like (Pura), a Rho1 GEF. Since spinocerebellar ataxia is associated with mutations in human Puratrophin-1, our data support the idea that defective actin-related plasticity underlies this ataxia.

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Section: Resultsmentioning

confidence: 99%

“…Immunocytochemistry was carried out as in (Collins et al, 2012; Collins et al, 2014). Antibodies are described in the supplementary information.…”

Section: Methodsmentioning

confidence: 99%

Circadian Rhythms in Rho1 Activity Regulate Neuronal Plasticity and Network Hierarchy

Petsakou

Sapsis

Blau

2015

Cell

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144

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“…Our work builds on a broad consensus that Drosophila PDF signaling proceeds early in the photophase (Park et al , 2000; Cusumano et al , 2009; Zhang et al , 2009; Im et al , 2011; Collins et al, 2014; Choi et al , 2014). The specific thought is that ligand availability (via PDF release) is greatest in the morning.…”

Section: Discussionmentioning

confidence: 99%

“…The neurons interact extensively via conventional neurotransmission and via neuropeptidergic signals to organize temporal information across the network and to mediate entrainment to environmental signals (Collins et al , 2014; Chung et al , 2009; Guo et al , 2014, Hermann-Luibl et al , 2014; Kunst et al , 2014; Parisky et al , 2008; Renn et al , 1999; Shafer et al, 2008). …”

Section: Introductionmentioning

confidence: 99%

Functional PDF Signaling in the Drosophila Circadian Neural Circuit Is Gated by Ral A-Dependent Modulation

Klose

Duvall

et al. 2016

Neuron

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The neuropeptide PDF promotes the normal sequencing of circadian behavioral rhythms in Drosophila, but its signaling mechanisms are not well understood. We report daily rhythmicity in responsiveness to PDF in critical pacemakers called small LNvs. There is a daily change in potency, as great as 10-fold higher, around dawn. The rhythm persists in constant darkness, does not require endogenous ligand (PDF) signaling, or rhythmic receptor gene transcription. Furthermore, rhythmic responsiveness reflects the properties of the pacemaker cell type, not the receptor. Dopamine responsiveness also cycles, in phase with that of PDF, in the same pacemakers, but does not cycle in large LNv. The activity of RalA GTPase in s-LNv regulates PDF responsiveness and behavioral locomotor rhythms. Additional, cell autonomous PDF signaling reversed the circadian behavioral effects of lowered RalA activity. Thus RalA activity confers high PDF responsiveness, providing a daily gate around the dawn hours to promote functional PDF signaling.

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“…Notably, in DD, the s-LNvs operate at the pinnacle of a hierarchy as they enforce a majority of other oscillators to realign their clock program in accordance with the sLNv pace (Stoleru et al 2005). In contrast, messages from the non-PDF clocks have considerably subdued influence on the running of the master pacemaker in DD (Stoleru et al 2005;Picot et al 2007;Collins et al 2014). Recently, however, the existence of a centralized monopolar circuit organization in DD has been seriously challenged.…”

Section: Layout Of the Network In Constant Conditionsmentioning

confidence: 99%

Control of Sleep-Wake Cycles in Drosophila

Chatterjee

Rouyer

2016

Research and Perspectives in Endocrine Interactions

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Inter-oscillator communication modulates and sustains the circadian locomotor rhythms in flies and rodent animal models. In Drosophila, the multioscillator network that controls sleep-wake cycles includes about 150 clock neurons. A subset of lateral neurons (LNs) expressing the Pigment-dispersing factor (PDF) appears to act as a master clock in constant darkness (DD). In light-dark (LD) cycles, flies show a bimodal distribution of their activity, and the PDF-expressing LNs play a major role in the control of the morning bout of activity. In contrast, a subset of PDF-negative LNs can generate evening activity in the absence of other functional oscillators. How these oscillators interact in a fully functional network to shape the sleep-wake cycle remains debated. The PDF neurons strongly influence the PDF-negative ones in DD and, to a lesser extent, in LD. The extent of hierarchy depends on environmental conditions and the way the dominance of PDF neurons is exerted on the different types of PDF-negative neurons is unclear. The recent discovery of light-and temperature-dependent oscillators in the dorsal neurons (DNs) sheds new light on the circuits that control the Drosophila diurnal behavior and its adaptation to environmental changes.

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Differentially Timed Extracellular Signals Synchronize Pacemaker Neuron Clocks

Abstract: Circadian pacemaker neurons in Drosophila are regulated by two synchronizing signals that are released at opposite times of day, generating a rhythm in intracellular cyclic AMP.

Cited by 48 publications

References 67 publications

Circadian Rhythms in Rho1 Activity Regulate Neuronal Plasticity and Network Hierarchy

Circadian Rhythms in Rho1 Activity Regulate Neuronal Plasticity and Network Hierarchy

Functional PDF Signaling in the Drosophila Circadian Neural Circuit Is Gated by Ral A-Dependent Modulation

Control of Sleep-Wake Cycles in Drosophila

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