Effects of different acute stressors on the regulation of appetite genes in the carp (Cyprinus carpioL.) brain

Abstract

Our understanding of the timing of stress responses and specific roles of different regulatory pathways that drive stress responses is incomplete. In particular, the regulation of appetite genes as a consequence of exposure to different stressors has not been studied in sufficient detail in fish. Therefore, a stress trial was conducted with koi carp, aiming at identifying typical effects of stress on regulation of appetite genes. The stressors tank manipulation, air exposure and feed rewarding were chosen. The responses to these stressors were evaluated 10, 30 and 60 min after the stressors were applied. Orexigenic and anorexigenic genes were investigated in four different brain regions (telencephalon, hypothalamus, optic tectum and rhombencephalon). The results show that, apart from the typical appetite regulation in the hypothalamus, the different brain regions also display pronounced responses of appetite genes to the different stressors. In addition, several genes in the serotonergic, dopaminergic and gaba-related pathways were investigated. These genes revealed that rearing in pairs of two and opening of the tank lid affected anorexigenic genes, such as cart and cck, which were not changed by air exposure or feed rewarding. Moreover, distress and eustress led to limited, but distinguishable gene expression pattern changes in the investigated brain regions.

Multiple faces of stress in the zebrafish (Danio rerio) brain

“…The functions of the telencephalon have long been regarded solely to be olfactory ( Aronson, 1967 ), but more recent research has confirmed its important role in the expression of emotional and motivational behavior and in stress responses in teleosts ( Lau et al, 2011 ; von Trotha et al, 2014 ; Pawlak et al, 2022 ). In addition, the hypothalamus plays an important role in energy homeostasis and appetite regulation, which may also be affected by stress ( Pawlak et al, 2023 ). The optic tectum not only is essential for visually mediated behaviors in teleosts ( Kramer et al, 2019 ) but also receives input from other brain areas, such as the hypothalamus and cerebellum ( Heap et al, 2013 ; Filosa et al, 2016 ).…”

“…In the case of isotocin, it has been assumed that a non-genomic pathway mediates the effects of cortisol ( Kalamarz-Kubiak, 2018 ). Furthermore, isotocin signaling in fish is involved in social behaviors, stress responses, and aggression ( Semsar et al, 2001 ; Salek et al, 2002 ; Kulczykowska et al, 2009 ; Pawlak et al, 2023 ).…”

“…Stress influences appetite regulation and feeding behavior in teleosts ( Höglund et al, 2007 ; Leal et al, 2011 ; Pawlak et al, 2023 ); therefore, appetite-regulating genes have also been included in the present study. Furthermore, it has been shown that the administration of dopamine decreases gene expression of the agouti-related protein ( agouti ) but not of pomc and neuropeptide y ( npy ; He et al, 2018 ).…”

“…The serotonergic system is widely distributed in the fish brain, and the functions of serotonin (5-HT) in the zebrafish brain have been described by Lillesaar (2011) . Serotonin uptake variations influence anxiety and modulate the vocal–acoustic circuitry and behavior in teleosts ( Simmons et al, 2017 ; Timothy and Forlano, 2020 ) and may also play a role in stress responses ( Pawlak et al, 2023 ). Furthermore, the serotonin precursor tryptophan affects serotonin signaling and interferes with stress-induced anorexia in the rainbow trout, Oncorhynchus mykiss ( Höglund et al, 2007 ; 2019 ).…”

“…Increasing evidence has shown that stress-induced analgesia also exists in zebrafish ( Thomson et al, 2020 ). Furthermore, acute stress affecting appetite regulation is in parallel to the changes in the expression of opioid receptor delta in common carp ( Pawlak et al, 2023 ).…”