Light‐ and dark‐dependent orexinergic neuronal signals promote neurodegenerative phenomena accounting for distinct behavioral responses in the teleost Thalassoma pavo

Abstract

The neuropeptides hypocretins/orexins (ORX) are known to control state-dependent activities such as sleep-wakefulness, energy homeostasis, thermoregulation, and maternal behaviors. To date, interests regarding environmental-related ORX-ergic neuronal functions have dealt with mammals; only recently is attention beginning to be directed toward aquatic vertebrates. Here, photoperiod-dependent effects of ORX-A on behavioral, neurodegenerative and transcriptional activities were evaluated in some forebrain areas of a teleost Labridae (ornate wrasse, Thalassoma pavo). The ornate wrasse, when treated intraperitoneally with a high physiological dose (100 ng/g) of ORX-A and exposed to a natural photoperiod (12L:12D), exhibited very high (P < 0.001) locomotion and feeding behaviors. ORX-A in the presence of a constant light photoperiod accounted for numerically even greater (>500%) feeding frequencies. Conversely, constant dark conditions very strongly reduced feeding habits and moderately (P < 0.05) increased resting states. In this case, the same ORX-A and photoperiodic conditions responsible for altered behaviors also induced neurodegenerative processes in the different hypothalamic, mesencephalic, and telencephalic neuronal fields. Interestingly, this ORX-A treatment seemed to be correlated to greater up-regulatory patterns of ORX receptor mRNA in these same brain areas, above all under constant light conditions rather than natural photoperiod. On the other hand, telencephalic sites provided a very active expression capacity during the dark phase. Overall, these results suggest for the first time that at least in the ornate wrasse, light- and dark-dependent ORX-ergic neuronal activities are able to cause short- and long-term abnormal motor behaviors, likely through neurodegenerative and transcriptional events in a brain regional manner.