Cyclic AMP‐regulated opposing and parallel effects of serotonin and dopamine on phototaxis in the Marmorkrebs (marbled crayfish)

Abstract

Phototactic behaviours are observed from prokaryotes to amphibians and are a basic form of orientation. We showed that the marbled crayfish displays phototaxis in which the behavioural response reversed from negative to positive depending on external light conditions. Animals reared in a 12-L/12-D light cycle showed negative phototaxis during daytime and positive phototaxis during night-time. Animals reared under constant light conditioning showed negative phototaxis during day- and night-time, while animals reared under constant dark conditioning showed positive phototaxis during day- and night-time. Injection of serotonin leads to a reversal of negative to positive phototaxis in both light/dark-reared and light/light-reared animals while injection of dopamine induced reversed negative phototaxis in dark/dark-reared animals. Four hours of dark adaptation were enough for light/dark-reared animals to reverse phototaxis from negative to positive. Injection of a serotonin 5HT receptor antagonist blocked the reverse phototaxis while serotonin 5HT receptor antagonists had no effects. Similarly, dark/dark-reared animals reversed to showing negative phototaxis after 4 h of light adaptation. Injection of a dopamine DA receptor antagonist blocked this reverse phototaxis, while dopamine DA receptor antagonists had no effects. Injection of a cAMP analogue into light/dark-reared animals blocked reverse phototaxis after dark adaptation, while adenylate cyclase inhibitor in dark/dark-reared animals blocked reverse phototaxis after light adaptation. These results strongly suggest that serotonin mediates positive phototaxis owing to decreased cAMP levels, while dopamine-mediated negative phototaxis occurs due to increased cAMP levels. Supporting this, the ratio of serotonin to dopamine in the brain was much higher in dark/dark-reared than light/dark-reared animals.

Aversive operant conditioning alters the phototactic orientation of the marbled crayfish

“…Many phototactic behaviours have been reported to reverse in sign (negative or positive) depending on the animal's internal state, such as developmental stage, growth or sex (Julian and Gronenberg, 2002;Lone et al, 2012;Miljeteig et al, 2014), or the environmental conditions, such as salinity or light intensity (Shirley and Shirley, 1988;Ziegler et al, 2010). Marbled crayfish show negative phototaxis in the daytime and positive phototaxis during the night (Shiratori et al, 2017). The present study is the first to report that phototaxis has plasticity and reverses according to associated learning experiences.…”

“…Marbled crayfish show a negative phototaxis; they avoid white light illumination (Shiratori et al, 2017). When marbled crayfish (five animals, 10 trials each) were released from the gate and chose either the white-lit exit or the unlit exit, the orientation rate to the white-lit exit was only 15.0±3.4% (Fig.…”

“…Marbled crayfish show negative phototaxis to white light illumination (Shiratori et al, 2017). They also show positive phototaxis to blue and green light illumination, but no phototaxis in response to red light illumination (C. Shiratori, personal observation).…”

“…The marbled crayfish, Procambarus virginalis Lyko 2017 (Vogt et al, 2015), is a parthenogenetic crayfish (Scholtz et al, 2003;Martin et al, 2007). Marbled crayfish show negative phototaxis to white light during the day (Shiratori et al, 2017). When using a T-maze with a white-lit exit on one side and an unlit exit on the other, animals prefer the unlit exit.…”

The effects of quality of shelters and prior residence on Marmorkrebs (marbled crayfish)

“…They produce genetically uniform clones and their central nervous system is probably similar to that of Procambarus clarkii (Faulkes, 2016), in which agonistic interactions and winner/loser effects have been well studied (Fujimoto et al, 2011;Sato and Nagayama, 2012;Momohara et al, 2016Momohara et al, , 2018Araki et al, 2013). Their behavioural plasticity and its neurochemical basis are well characterized (Kasuya and Nagayama, 2016;Shiratori et al, 2017). They also show a strong preference for shelter selection (Takahashi and Nagayama, 2016).…”