Defining the role of Drosophila lateral neurons in the control of circadian rhythms in motor activity and eclosion by targeted genetic ablation and PERIOD protein overexpression

Mar 27, 2001The European journal of neuroscience

How specific brain cells in fruit flies control daily activity and emergence timing by removing them or increasing a key clock protein

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Abstract

Genetic ablation of ventral lateral neurons in Drosophila results in the loss of robust 24-hour activity rhythms.

Ablation of LNvs leads to a phase advance in light-dark conditions and a weak short-period rhythm in constant darkness.
Disco1 mutants also display reduced numbers of lateral neurons that fail to express the PER protein, mirroring LNv-ablated behavioral phenotypes.
Weak short-period rhythms observed in LNv-ablated and disco1 flies may originate from dorsal neurons that do not express PDF.
Overexpression of the per gene in LNs disrupts both activity and eclosion rhythms, indicating the importance of PER cycling in these neurons.
Flies with PER overexpression in LNs do not exhibit weak short-period rhythms, highlighting the dominant role of LNs in regulating behavioral rhythms.
Expression of a synaptic toxin in the LNvs does not affect activity rhythms, suggesting that PDF-expressing neurons may not rely on specific synaptic transmission mechanisms.

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The ventral lateral neurons (LNvs) of the Drosophila brain that express the period (per) and pigment dispersing factor (pdf) genes play a major role in the control of circadian activity rhythms. A new P-gal4 enhancer trap line is described that is mostly expressed in the LNvs This P-gal4 line was used to ablate the LNvs by using the pro-apoptosis gene bax, to stop PER protein oscillations by overexpressing per and to block synaptic transmission with the tetanus toxin light chain (TeTxLC). Genetic ablation of these clock cells leads to the loss of robust 24-h activity rhythms and reveals a phase advance in light-dark conditions as well as a weak short-period rhythm in constant darkness. This behavioural phenotype is similar to that described for disconnected1 (disco1) mutants, in which we show that the majority of the individuals have a reduced number of dorsally projecting lateral neurons which, however, fail to express PER. In both LNv-ablated and disco1 flies, PER cycles in the so-called dorsal neurons (DNs) of the superior protocerebrum, suggesting that the weak short-period rhythm could stem from these PDF-negative cells. The overexpression of per in LNs suppresses PER protein oscillations and leads to the disruption of both activity and eclosion rhythms, indicating that PER cycling in these cells is required for both of these rhythmic behaviours. Interestingly, flies overexpressing PER in the LNs do not show any weak short-period rhythms, although PER cycles in at least a fraction of the DNs, suggesting a dominant role of the LNs on the behavioural rhythms. Expression of TeTxLC in the LNvs does not impair activity rhythms, which indicates that the PDF-expressing neurons do not use synaptobrevin-dependent transmission to control these rhythms.

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Defining the role of Drosophila lateral neurons in the control of circadian rhythms in motor activity and eclosion by targeted genetic ablation and PERIOD protein overexpression

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