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

Jan 4, 2008The Journal of neuroscience : the official journal of the Society for Neuroscience

Daily movement patterns controlled by pigment dispersing factor and other mechanisms

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Abstract

Approximately 60% of Drosophila exhibit two concurrent short- and long-period circadian activity bouts following altered electrical activity of PDF-expressing lateral ventral neurons (LNv).

Initial behavioral arrhythmicity occurs before the emergence of distinct circadian activity bouts.
Two subgroups of dorsal neurons (DN1 and DN2) show synchronized molecular oscillations that align with the activity bouts.
Other neuronal subgroups display a single peak of molecular oscillation corresponding to only one activity bout.
The novel pattern of synchrony in molecular oscillations does not coincide with changes in electrical activity of the LNv.
In PDF-null flies, altered LNv activity results in only a short-period circadian activity bout, suggesting the long-period component is PDF-dependent.

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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 approximately 60% 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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Pigment Dispersing Factor-Dependent and -Independent Circadian Locomotor Behavioral Rhythms

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