Circadian Control of Dendrite Morphology in the Visual System of Drosophila melanogaster

Abstract

BackgroundIn the first optic neuropil (lamina) of the fly's visual system, monopolar cells L1 and L2 and glia show circadian rhythms in morphological plasticity. They change their size and shape during the day and night. The most pronounced changes have been detected in circadian size of the L2 axons. Looking for a functional significance of the circadian plasticity observed in axons, we examined the morphological plasticity of the L2 dendrites. They extend from axons and harbor postsynaptic sites of tetrad synaptic contacts from the photoreceptor terminals.Methodology/Principal FindingsThe plasticity of L2 dendrites was evaluated by measuring an outline of the L2 dendritic trees. These were from confocal images of cross sections of L2 cells labeled with GFP. They were in wild-type and clock mutant flies held under different light conditions and sacrified at different time points. We found that the L2 dendrites are longest at the beginning of the day in both males and females. This rhythm observed under a day/night regime (LD) was maintained in constant darkness (DD) but not in continuous light (LL). This rhythm was not present in the arrhythmic per01 mutant in LD or in DD. In the clock photoreceptor cryb mutant the rhythm was maintained but its pattern was different than that observed in wild-type flies.Conclusions/SignificanceThe results obtained showed that the L2 dendrites exhibit circadian structural plasticity. Their morphology is controlled by the per gene-dependent circadian clock. The L2 dendrites are longest at the beginning of the day when the daytime tetrad presynaptic sites are most numerous and L2 axons are swollen. The presence of the rhythm, but with a different pattern in cryb mutants in LD and DD indicates a new role of cry in the visual system. The new role is in maintaining the circadian pattern of changes of the L2 dendrite length and shape.

Circadian rhythms in the morphology of neurons in Drosophila

“…These findings, together with the observation of daily cycles in other morphological features of photoreceptors and visual interneurons (Pyza and Górska-Andrzejak 2008; Barth et al 2010), including the size of L2 dendrites (Weber et al 2009), L2 dendritic spines and cell nuclei in Drosophila (Górska-Andrzejak et al 2005), have firmly established that circadian plasticity includes waves of assembly and disassembly of synapses.…”

“…Bar 100 mm. Adapted from Weber et al 2009. b Cross-sectional areas of L1 and L2 in the proximal lamina during the day (ZT1 and ZT4) and during the night (ZT13 and ZT16) measured in LD.…”

Sleep, clocks, and synaptic plasticity

“…The axons of Drosophila L1 and L2 interneurons swell at the onsets of the light and dark periods, with a maximum observed at the latter time point [79]. The dendrites of L2 are larger at the beginning of the day with a unimodal circadian rhythm [81]. Small LNvs also show a rhythmic change in branching complexity along the day in LD and DD, with more complex branching early in the day in LD (relative to early night) and the same relationship when the flies are kept in DD [82].…”

A novel wide-field neuron with branches in the lamina of the Drosophila visual system expresses myoinhibitory peptide and may be associated with the clock

“…Nevertheless, neurons of the Drosophila lamina have been demonstrated to display cyclic variations in morphology and physiology that appear to be under the control of clock neurons (GorskaAndrzejak et al 2005(GorskaAndrzejak et al , 2009Meinertzhagen and Pyza 1999;Pyza and Meinertzhagen 1995, 1997Weber et al 2009), suggesting that other interneurons connect the oscillators to the periphery. One set of candidate neurons for the central modulation of lamina circuits was identified before the clock neurons had been localized.…”