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How external cues modulate the behavioral output of an animal: Immediate effects of light on rhythmic eclosion behavior in Drosophila

Subject Area Cognitive, Systems and Behavioural Neurobiology
Term from 2019 to 2023
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 420900883
 
Final Report Year 2023

Final Report Abstract

An appropriate daily timing of behavior is of critical importance for animal fitness. Light shapes the daily timing in two ways: (1) the cyclic change in light intensity acts as an entraining signal, synchronizing the endogenous (circadian) timing system to appropriately adjust an organism to the 24h environmental period; (2) light directly modulates behavior by increasing alertness, locomotion, body temperature and heart rate in diurnal animals including humans and by suppressing activity and promoting sleep in nocturnal animals . These immediate light effects are independent of the circadian clock and since they often obscure (“mask”) circadian behaviors, they are also called “masking” effects. The immediate light effects are essential for appropriate responses of the animal to changes in the environment and for sharpening the behavioral output. In mammals, the immediate light effects depend on blue light-sensitive melanopsin-expressing retinal ganglion cells directly connecting to the thalamus . In Drosophila melanogaster, the immediate light effects are most evident as a lights-on response in two well described behavioral rhythms of the fly – the emergence rhythm of the adult insect from the pupa, called eclosion, and the adult activity rhythm. Eclosion is gated by the circadian clock to the early day to prevent desiccation and enhance survival rate. A light stimulus induces a rapid increase in eclosion rate (lights-on effect) that is eliminated in eyeless and potentially in occelliless mutants . Even though the lights-on effect is gone, eclosion remains synchronized to the light-dark cycle in eyeless flies by the circadian blue-light photopigment Cryptochrome (CRY). Similarly, the locomotor activity rhythm of adult eyeless flies remains synchronized to the light-dark cycle due to entrainment by CRY, but the immediate increase of activity after lights-on, also known as “startle response” disappears after elimination of the eyes . The neuronal circuits that mediate the immediate light effects in adult flies are largely unknown. In this project, we aimed to identify the neuronal correlates of the immediate light effects that trigger specific behavioural responses counteracting or reinforcing circadian rhythms. For this, we used eclosion and locomotor activity as behavioral readouts to examine immediate light effects on circadian behaviors. We provide evidence that the immediate light effect on eclosion is mediated by blue light-sensitive photoreceptor cells of the compound eyes. Interestingly, the light effect on locomotor activity in the night is triggered by different light detecting cells and organs, that seem to compensate for the loss of each other. Thus, immediate effects of light on circadian behaviors seem to depend on different underlying neuronal networks. The project started to untangle the neuronal mechanisms underlying immediate light responses and thereby give novel insights into the fundamental principles of how external cues modulate the brain activity and, thus, the behavioral output of animals.

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