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

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. © 2008 Wiley‐Liss, Inc.