Nonvisual Photoreceptors in Arthropods with Emphasis on Their Putative Role as Receptors of Natural Zeitgeber Stimuli

Abstract

In various insect and arachnid species, three different types of photoreceptors that do not serve image processing have been discovered and analyzed by means of neurobiological methods: They can be found for example: (1) as lamina and lobula organs (LaOs and LoOs) next to the optic neuropils in the optic lobes of holo‐ and hemimetabolous insects; (2) inside the last ganglia of the cord of the scorpion and a marine midge; and (3) as modified visual photoreceptors in metamorphosized larval stemmata and the lateral eyes of scorpions, which have been compound eyes in fossil scorpion relatives. Immunocytology with various antibodies against proteins of the phototransduction cascade, the rhabdom turnover cycle and neurotransmitters of afferent and efferent pathways, was combined with light‐ and ultrastructural investigations in well‐defined adaptational states, in order to study their photoreceptive function and neuronal wiring. Pilot chronobiological experiments with a newly developed twilight simulating lamp, behavioral studies, and model calculations provide evidence that these photoreceptors may well serve a role in the complex task of detecting time cues out of natural dawn and dusk.

“…Clearly more work will be necessary before truly informed judgements can be made about the functional significance of the diversity in photoreception for entrainment. A first step will be the precise identification of photoreceptors and investigations of the mechanisms of transduction, processing and transmission of temporal information provided by the daily light cycle.…” ()

• Circadian clock
• Circatidal rhythm
• Extraretinal photoreceptor
• Ocelli
• Stemmata

Notes

^aIn literature, the term “ocellus” is used with different meanings: (1) the general construction plan of a photoreceptor with one corneal lens in contrast to a “compound eye” with a multitude of densely packed tiny corneal lenses; (2) the (dorsal) ocelli of insects with well‐defined target zones of their receptor afferents in the midbrain area; (3) the (larval) ocelli of holometabolous insects, also named stemmata, which also have the ocellar shape. They have their first neuropils in the optic lobes.

^bMethods and Experimental Animals: Our studies are mainly based on desert beetle and scorpion species as model organisms, selected for their robust endurance of extreme climatic conditions by strict nocturnality and sometimes weeks or months of subterranean lifestyle—self‐selected constant DD conditions without food and water intake. These results have lead us to successful comparative neurobiological studies in cockroaches, crickets, grasshoppers, and marine midges, all well‐established model systems in chronobiological research. Neurobiological methods have been adapted to serve the special needs of the project work ([Fleissner et al., 2001a]; [Schuchardt et al., 2002]; [Thomas et al., 2003). Immunocytological investigations with partly noncommercial antibodies mainly followed protocols of B. Battelle (St. Augustine, USA) ([Battelle et al., 2001).

^cThe paper is part of a progress report on projects funded by the DFG priority program.

^dBetter analyzed and often described are the other visual and nonvisual systems of both arachnids. The visual receptors are the median eyes in scorpions, and the lateral compound eyes in Limulus. Nonvisual receptors are the lateral eyes of scorpions ([Fleissner, 1977c) and a complex set of receptors in Limulus: “median ocelli,” a set of ventral photoreceptors, and a rudimentary lateral eye next to the lateral compound eyes may serve as photic Zeitgeber receptors (for review: [Renninger and Chamberlain, 1993). The sensitivity of all these visual and nonvisual photoreceptors in both model systems is clock controlled by efferent fibers and all can separately phase‐shift the clock (for further details see below: Type 3 photoreceptors).

^eInvestigating the equilibrium system of fish, [von Holst and Mittelstaedt (1950)] postulated reafferent processes, which enable the organism to distinguish between externally and internally induced retinal motion. Signals that control locomotion are present in the visual system as induced retinal motion; signals that control locomotion are present in the visual system as feedback information. This reafference principle seems to be verified in many different organisms, including humans.