PDF Cells Are a GABA-Responsive Wake-Promoting Component of the Drosophila Sleep Circuit

Parisky, Katherine M.; Agosto, José; Pulver, Stefan R.; Shang, Yuhua; Kuklin, Elena A.; Hodge, James J L; Kang, Kyung-In; Liu, Xu; Garrity, Paul; Rosbash, Michael; Griffith, Leslie C.

doi:10.1016/j.neuron.2008.12.017

Cited by 13 publications

(13 citation statements)

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“…Previous studies had suggested that this cell group is less important for circadian rhythms (Yang and Sehgal, 2001;Grima et al, 2004). However, recently, several groups demonstrated that the l-LN v cells are responsible for arousal/sleep (Sheeba et al, 2008a;Parisky et al, 2008;Shang et al, 2008). In addition, the l-LN v responds to light with increased spontaneous action potential firing (Sheeba et al, 2008b), and the ablation of the l-LN v cells reduces the diurnal photoresponse at dawn .…”

Section: Discussionmentioning

confidence: 99%

Synergic Entrainment of Drosophila’s Circadian Clock by Light and Temperature

et al. 2009

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Daily light and temperature cycles are considered the most important zeitgebers for circadian clocks in many organisms. The influence of each single zeitgeber on the clock has been well studied, but little is known about any synergistic effects of both zeitgebers on the clock. In nature, light and temperature show characteristic daily oscillations with the temperature rising during the light phase and reaching its maximum in the late afternoon. Here, we studied behavioral and molecular rhythms in Drosophila melanogaster under simulated natural low light-dark (LD) and temperature (T) cycles that typically occur during the September equinox. Wild-type flies were either subjected to simulated LD or T cycles alone or to a combination of both. Behavioral rhythms and molecular rhythms in the different clock neurons were assessed under the 3 different conditions. Although behavioral rhythms entrained to all conditions, the rhythms were most robust under the combination of LD and T cycles. The clock neurons responded differently to LD and T cycles. Some were not entrained by T cycles alone; others were only slightly entrained by LD cycles alone. The amplitude of the molecular cycling was not different between LD alone and T cycles alone; but LD alone could set the pacemaker neurons to similar phases, whereas T cycles alone could not. The combination of the 2 zeitgebers entrained all clock neurons not only with similar phase but also enhanced the amplitude of Timeless cycling in the majority of cells. Our results show that the 2 zeitgebers synergistically entrain behavioral and molecular rhythms of Drosophila melanogaster.

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Section: Discussionmentioning

confidence: 99%

Synergic Entrainment of Drosophila’s Circadian Clock by Light and Temperature

et al. 2009

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“…Thus, it is very likely that in the cockroach, the light-dependent change in the length of the PDF-ir processes reflects respective light-dependent changes in the volume of PDF-ir neuropils. It is not completely resolved how light affects the PDF-ir l-LNvs to control PDF release at dawn in the fruit fly to elicit arousal (Parisky et al, 2008;Park and Griffith, 2006). Even less is known about the preand postsynaptic cells of the PDF-ir neurons in the cockroach.…”

Section: Plasticity Of the Optic Lobesmentioning

confidence: 99%

Light Affects the Branching Pattern of Peptidergic Circadian Pacemaker Neurons in the Brain of the CockroachLeucophaea maderae

Wei

Stengl

2011

J Biol Rhythms

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Pigment-dispersing factor-immunoreactive neurons anterior to the accessory medulla (aPDFMes) in the optic lobes of insects are circadian pacemaker neurons in cockroaches and fruit flies. The authors examined whether any of the aPDFMes of the cockroach Leucophaea maderae are sensitive to changes in period and photoperiod of light/dark (LD) cycles as a prerequisite to adapt to changes in external rhythms. Cockroaches were raised in LD cycles of 11:11, 13:13, 12:12, 6:18, or 18:6 h, and the brains of the adults were examined with immunocytochemistry employing antisera against PDF and orcokinin. Indeed, in 11:11 LD cycles, only the number of medium-sized aPDFMes specifically decreased, while it increased in 13:13. In addition, 18:6 LD cycles increased the number of large- and medium-sized aPDFMes, as well as the posterior pPDFMes, while 6:18 LD cycles only decreased the number of medium-sized aPDFMes. Furthermore, PDF-immunoreactive fibers in the anterior optic commissure and orcokinin-immunoreactive fibers in both the anterior and posterior optic commissures were affected by different lengths of light cycles. Thus, apparently different groups of the PDFMes, most of all the medium-sized aPDFMes, which colocalize orcokinin, respond to changes in period and photoperiod and could possibly allow for the adjustment to different photoperiods.

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“…Here, we show that the response of the l-LNv clock neurons to GABA is also regulated by KCC and NKCC (Figure 3) 1 , suggesting that GABA polarity within these neurons changes during the day. The observation that the l-LNv receive GABAergic input 1,9–11 further support this idea. Because both KCC and NKCC are expressed in subsets of other clock neuronal groups (LNd, DN1, DN3) (Figure S1) it is likely that GABA polarity changes throughout the clock network in a daily fashion.…”

Section: Discussionmentioning

confidence: 57%

“…To determine if the behavioral effects of altered [Cl − ] i as a result of CCC modulation are reflected by physiological changes in the response to GABA, we performed patch-clamp recordings on the GABA responsive l-LNv neurons 1,9–11 to determine the GABA reversal potential (E GABA ). The l-LNv express the ionotropic chloride channel receptor GABA A 9 , and first, we confirmed KCC and NKCC expression in these neurons using suitable intragenic Gal4 insertions to drive a fluorescent cytoplasmic marker (Figure S1) 29 .…”

Section: Resultsmentioning

confidence: 99%

The opposing Chloride Cotransporters KCC and NKCC control locomotor activity in constant light and during long days

Eick¹,

Ogueta²,

Buhl

et al. 2021

Preprint

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Cation Chloride Cotransporters (CCCs) regulate intracellular chloride ion concentration ([Cl-]i) within neurons, which can reverse the direction of the neuronal response to the neurotransmitter GABA. Na+ K+ Cl- (NKCC) and K+ Cl- (KCC) cotransporters transport Cl- into or out of the cell, respectively. When NKCC activity dominates, the resulting high [Cl-]i can lead to an excitatory and depolarizing response of the neuron upon GABAA receptor opening, while KCC dominance has the opposite effect. This inhibitory-to-excitatory GABA switch has been linked to seasonal adaption of circadian clock function to changing day length, and its dysregulation is associated with neurodevelopmental disorders such as epilepsy. Constant light normally disrupts circadian clock function and leads to arrhythmic behavior. Here, we demonstrate a function for KCC in regulating Drosophila locomotor activity and GABA responses in circadian clock neurons because alteration of KCC expression in circadian clock neurons elicits rhythmic behavior in constant light. We observed the same effects after downregulation of the Wnk and Fray kinases, which modulate CCC activity in a [Cl-]i-dependent manner. Patch-clamp recordings from clock neurons show that downregulation of KCC results in a more positive GABA reversal potential, while KCC overexpression has the opposite effect. Finally, KCC downregulation represses morning behavioral activity during long photoperiods, while downregulation of NKCC promotes morning activity. In summary, our results support a model in which the regulation of [Cl-]i by a KCC/NKCC/Wnk/Fray feedback loop determines the response of clock neurons to GABA, which is important for adjusting behavioral activity to constant light and long-day conditions.

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PDF Cells Are a GABA-Responsive Wake-Promoting Component of the Drosophila Sleep Circuit

Abstract: On page 800 of our paper, the intracellular solution used for measurements of LTP is erroneously described as containing KMeS0 3 . In reality, a cesium-based (CsMeSO 3 ) intracellular solution was actually used for these voltage-clamp recordings.

Cited by 13 publications

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Synergic Entrainment of Drosophila’s Circadian Clock by Light and Temperature

Synergic Entrainment of Drosophila’s Circadian Clock by Light and Temperature

Light Affects the Branching Pattern of Peptidergic Circadian Pacemaker Neurons in the Brain of the CockroachLeucophaea maderae

The opposing Chloride Cotransporters KCC and NKCC control locomotor activity in constant light and during long days

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