Feeding behaviors and ORXR–β-GABAAR subunit interactions in Carassius auratus

Orexins are one of the most potent orexigenic factors in fish that through their interaction with the GABAA receptor system assures the successful execution of feeding, motor and sleep–wake activities. In the present study, the effects of ORX-A (10 ng/g BW) very greatly enhanced (p < 0.001) the time spent in feeding behaviors while at the same time moderately increased (p < 0.05) food intake of the goldfish. It is worthy to note that the great variations of time spent in feeding behaviors induced by β GABAAR agonist (muscimol, MUS) and antagonist (bicuculline, BIC) did not result to be correlated to any significant variations of food intake. It was, however, a T-maze study allowing us to establish that learning and mnemonic events very likely also operated in an ORX-A + GABAAR-dependent fashion in our fish model. Indeed, animals conditioned by red/blue lights greatly reduced latency time in the presence of ORX-A while neither MUS nor BIC alone modified such a parameter, with the exception of ORX-A + MUS being responsible for a moderate decrease of latency time with respect to conditioned fish treated with a saline solution. Conversely, ORX-A + MUS/BIC seemed to interfere with ORX-A actions as shown by their very great increase in latency time. Moreover, T-maze results appeared to be strengthened by evident ORXR transcriptional variations especially by the very great mRNA densities detected in some telencephalic regions of animals treated with ORX-A. Of all telencephalic regions Dl, considered homologous to the mammalian hippocampus, proved to be a major target for ORX-A effects. Overall, these data suggest that it is mainly the ORXergic system that promotes feeding behaviors via reward pathways in teleost fish as in mammals. Surprisingly, β GABAAR drugs did not modify such behaviors when given alone while the inhibitory effect on cognitive/reward processes was evoked when given together with ORX-A, suggesting that more than β subunits other GABAAR subunits could be promoting mnemonically guided motor behaviors.

► ORX-A-dependent effects control feeding and cognitive behaviors.
► β GABAAR subunits are responsible for feeding behaviors.
► ORXR mRNA changes in telencephalic and hypothalamic areas are key targets of ORX-A effects.
► β GABAAR subunits interfere at both behavioral and molecular levels with ORX-A-dependent learning processes.