title: Light evokes rapid circadian network oscillator desynchrony followed by gradual phase retuning of synchrony.
abstract: Circadian neural circuits generate near 24-hr physiological rhythms that can be entrained by light to coordinate animal physiology with daily solar cycles. To examine how a circadian circuit reorganizes its activity in response to light, we imaged period (per) clock gene cycling for up to 6 days at single-neuron resolution in whole-brain explant cultures prepared from per-luciferase transgenic flies. We compared cultures subjected to a phase-advancing light pulse (LP) to cultures maintained in darkness (DD). In DD, individual neuronal oscillators in all circadian subgroups are initially well synchronized but then show monotonic decrease in oscillator rhythm amplitude and synchrony with time. The small ventral lateral neurons (s-LNvs) and dorsal lateral neurons (LNds) exhibit this decrease at a slower relative rate. In contrast, the LP evokes a rapid loss of oscillator synchrony between and within most circadian neuronal subgroups, followed by gradual phase retuning of whole-circuit oscillator synchrony. The LNds maintain high rhythmic amplitude and synchrony following the LP along with the most rapid coherent phase advance. Immunocytochemical analysis of PER shows that these dynamics in DD and LP are recapitulated in vivo. Anatomically distinct circadian neuronal subgroups vary in their response to the LP, showing differences in the degree and kinetics of their loss, recovery and/or strengthening of synchrony, and rhythmicity. Transient desynchrony appears to be an integral feature of light response of the Drosophila multicellular circadian clock. Individual oscillators in different neuronal subgroups of the circadian circuit show distinct kinetic signatures of light response and phase retuning.
authors.affiliation: Department of Physiology and Biophysics, University of California, Irvine, Irvine, CA 92697, USA.
authors.forename: Logan
authors.initials: L
authors.lastname: Roberts
authors.affiliation: Department of Mathematics and Statistics, Amherst College, Amherst, MA 01002, USA.
authors.forename: Tanya L
authors.initials: TL
authors.lastname: Leise
authors.affiliation: Department of Psychiatry and Center for Circadian Biology, University of California, San Diego, La Jolla, CA 92093, USA.
authors.forename: Takako
authors.initials: T
authors.lastname: Noguchi
authors.affiliation: Department of Physiology and Biophysics, University of California, Irvine, Irvine, CA 92697, USA.
authors.forename: Alexis M
authors.initials: AM
authors.lastname: Galschiodt
authors.affiliation: Department of Physiology and Biophysics, University of California, Irvine, Irvine, CA 92697, USA.
authors.forename: Jerry H
authors.initials: JH
authors.lastname: Houl
authors.affiliation: Department of Psychiatry and Center for Circadian Biology, University of California, San Diego, La Jolla, CA 92093, USA; Veterans Affairs San Diego Healthcare System, San Diego, CA 92161, USA.
authors.forename: David K
authors.initials: DK
authors.lastname: Welsh
authors.affiliation: Department of Physiology and Biophysics, University of California, Irvine, Irvine, CA 92697, USA. Electronic address: tholmes@uci.edu.
authors.forename: Todd C
authors.initials: TC
authors.lastname: Holmes
mesh_terms: D000818:Animals; D030801:Animals, Genetically Modified; D057906:Circadian Clocks / Q000502:physiology*; D002940:Circadian Rhythm / Q000502:physiology*; D003624:Darkness; D004330:Drosophila / Q000502:physiology; D029721:Drosophila Proteins / Q000378:metabolism; D008027:Light; D009415:Nerve Net / Q000502:physiology*; D009474:Neurons / Q000378:metabolism*; D056950:Period Circadian Proteins / Q000378:metabolism*; D013997:Time Factors; D020651:Ventral Thalamic Nuclei / Q000166:cytology
chemical_list: D029721:Drosophila Proteins; D056950:Period Circadian Proteins