Current theories on the role of serotonin (5-HT) in vertebrate defensive behavior suggest that this monoamine increases anxiety but decreases fear, by acting at different levels of the neuroaxis. This paradoxical, dual role of 5-HT suggests that a serotonergic tone inhibits fear responses, while an acute increase in 5-HT would produce anxiety-like behavior. However, so far no evidence for a serotonergic tone has been found. Using zebrafish alarm responses, we investigate the participation of phasic and tonic 5-HT levels in fear-like behavior, as well as in behavior after stimulation.Conspecific alarm substance (CAS) increased bottom-dwelling and erratic swimming, and animals transferred to a novel environment after CAS exposure (post-exposure behavior) showed increased bottom-dwelling and freezing. Clonazepam blocked CAS effects during and after exposure. Acute fluoxetine dose-dependently decreased fear-like behavior, but increased post-exposure freezing. Metergoline had no effect on fear-like behavior, but blocked the effects of CAS on post-exposure behavior; similar effects were observed with para-chlorophenylalanine. Finally, CAS was shown to decrease the activity of monoamine oxidase in the zebrafish brain after exposure.These results suggest that phasic and tonic serotonin encode an aversive expectation value, switching behavior toward cautious exploration/risk assessment/anxiety when the aversive stimulus is no longer present. K E Y W O R D Salarm substance, fear, panic, serotonin, zebrafish | INTRODUC TI ONThe neurocircuitry of defensive reactions involves regulation by a plethora of neuromodulators, including monoamines and peptides (Maximino, 2012). In vertebrates, the monoamine serotonin (5-HT) is produced in specific brain nuclei, including the raphe, and is thought to inhibit fear/escape responses to proximate threat by acting on more caudal structures of the aversive brain system (Deakin & Graeff, 1991; S U PP O RTI N G I N FO R M ATI O N Additional supporting information may be found online in the Supporting Information section. How to cite this article: Lima-Maximino M, Pyterson MP, do Carmo Silva RX, et al. Phasic and tonic serotonin modulate alarm reactions and post-exposure behavior in zebrafish. J. Neurochem. 2020;153:495-509.https://doi.
Current theories on the role of serotonin (5-HT) in vertebrate defensive behavior suggest that this monoamine increases anxiety but decreases fear, by acting at different levels of the neuroaxis. This paradoxical, dual role of 5-HT suggests that a serotonergic tone inhibits fear responses, while an acute increase in 5-HT would produce anxiety-like behavior. However, so far no evidence for a serotonergic tone has been found. Using zebrafish alarm responses, we investigate the participation of phasic and tonic 5-HT levels in fear-like behavior, as well as in behavior after stimulation.Conspecific alarm substance (CAS) increased bottom-dwelling and erratic swimming, and animals transferred to a novel environment after CAS exposure (post-exposure behavior) showed increased bottom-dwelling and freezing. Clonazepam blocked CAS effects during and after exposure. Acute fluoxetine dose-dependently decreased fear-like behavior, but increased post-exposure freezing.Metergoline had no effect on fear-like behavior, but blocked the effects of CAS on post-exposure behavior; similar effects were observed with pCPA. Finally, CAS was shown to decrease the activity of monoamine oxidase in the zebrafish brain after exposure. These results suggest that phasic and tonic serotonin encode an aversive expectation value, switching behavior towards cautious exploration/risk assessment/anxiety when the aversive stimulus is no longer present. zebrafish, 5-HT 1A and 5-HT 1B receptor antagonists decrease anxiety-like behavior (Maximino et al. ,635 was not able to alter anxiety-like behavior after exposure, the drug blocked the increased geotaxis during CAS exposure, both in the first minutes of exposure and in the last minutes (Nathan et al. 2015). Blocking 5-HT 2 -type receptors with methysergide did not affect these responses,
Chemical communication of predation risk has evolved multiple times in fish species, with conspecific alarm substance (CAS) being the most well understood mechanism. CAS is released after epithelial damage, usually when prey fish are captured by a predator and elicits neurobehavioural adjustments in conspecifics which increase the probability of avoiding predation. As such, CAS is a partial predator stimulus, eliciting risk assessment‐like and avoidance behaviours and disrupting the predation sequence. The present paper reviews the distribution and putative composition of CAS in fish and presents a model for the neural processing of these structures by the olfactory and the brain aversive systems. Applications of CAS in the behavioural neurosciences and neuropharmacology are also presented, exploiting the potential of model fish [e.g., zebrafish Danio rerio, guppies Poecilia reticulata, minnows Phoxinus phoxinus) in neurobehavioural research.
21Chemical communication of predation risk has evolved multiple times in fish species, with the 22 conspecific alarm substance (CAS) contemporaneously being the most well understood mechanism. 23 CAS is released after epithelial damage, usually when prey fish is captured by a predator, and elicits 24 neurobehavioral adjustments in conspecifics which increase the probability of avoiding predation. 25As such, CAS is a partial predator stimulus, eliciting risk assessment-like and avoidance behaviors, 26 and disrupting the predator sequence. The present paper reviews the distribution and putative 27 composition of CAS in fish, and presents a model for the neural processing of these structures by 28 the olfactory and the brain aversive systems. Applications of CAS in the behavioral neurosciences 29 and neuropharmacology are also presented, exploiting the potential of model fish (e.g., zebrafish, 30 guppies, minnows) on neurobehavioral research. 31
Chemical communication of predation risk has evolved multiple times in fish species, with the conspecific alarm substance (CAS) contemporaneously being the most well understood mechanism. CAS is released after epithelial damage, usually when prey fish is captured by a predator, and elicits neurobehavioral adjustments in conspecifics which increase the probability of avoiding predation. As such, CAS is a partial predator stimulus, eliciting risk assessment-like and avoidance behaviors, and disrupting the predator sequence. The present paper reviews the distribution and putative composition of CAS in fish, and presents a model for the neural processing of these structures by the olfactory and the brain aversive systems. Applications of CAS in the behavioral neurosciences and neuropharmacology are also presented, exploiting the potential of model fish (e.g., zebrafish, guppies, minnows) on neurobehavioral research.
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