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Exploring Hallucinogen Pharmacology and Psychedelic Medicine with Zebrafish Models

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Exploring Hallucinogen Pharmacology and Psychedelic Medicine with Zebrafish Models ZEBRAFISH Volume 13, Number 5, 2016 Review Articles ª Mary Ann Liebert, Inc. DOI: 10.1089/zeb.2016.1251 Exploring Hallucinogen Pharmacology and Psychedelic Medicine with Zebrafish Models Evan J. Kyzar1 and Allan V. Kalueff2–6 Abstract After decades of sociopolitical obstacles, the field of psychiatry is experiencing a revived interest in the use of hallucinogenic agents to treat brain disorders. Along with the use of ketamine for depression, recent pilot studies have highlighted the efficacy of classic serotonergic hallucinogens, such as lysergic acid diethylamide and psilocybin, in treating addiction, post-traumatic stress disorder, and anxiety. However, many basic phar- macological and toxicological questions remain unanswered with regard to these compounds. In this study, we discuss psychedelic medicine as well as the behavioral and toxicological effects of hallucinogenic drugs in zebrafish. We emphasize this aquatic organism as a model ideally suited to assess both the potential toxic and therapeutic effects of major known classes of hallucinogenic compounds. In addition, novel drugs with hal- lucinogenic properties can be efficiently screened using zebrafish models. Well-designed preclinical studies utilizing zebrafish can contribute to the reemerging treatment paradigm of psychedelic medicine, leading to new avenues of clinical exploration for psychiatric disorders. Introduction requiring the use of both traditional (rodent) and novel model species.6 In this study, we briefly review the history of psy- allucinogenic drugs have been used by humans for chedelic medicine and the pharmacology of these drugs and centuries, exerting potent effects on thought, cognition, H discuss the effects of hallucinogenic drugs on larval and adult and behavior with little propensity for habit formation and zebrafish (Danio rerio). We highlight the utility of this aquatic addiction.1 In 1940s and 1950s, scientists began to realize the model organism in future experiments investigating the po- potential of these compounds in neuroscience and psychiatry. tential behavioral benefits and pharmacological toxicity of However, drug laws have categorized many hallucinogens in hallucinogenic compounds. the most strict regulatory groupings (e.g., Schedule I in the United States and Class A in the United Kingdom), leading to Psychedelic Medicine and Pharmacology a relative dearth of scientific inquiry into the biology of these compounds.2,3 Nonetheless, the last decade has seen a revival While the term hallucinogen often refers to different classes of hallucinogenic drug investigation,4,5 with a particular focus of drugs with mind-altering properties, this definition may be on identifying compounds that may have efficacy in treating overly broad and reliant on terminology that principally in- intractable psychiatric illnesses. volves visual phenomenology.7 Earlier studies have limited While the use of hallucinogens in medicine shows promise, this term to a more narrow definition, only ascribing to the these compounds are not without risk. The years of scientific word to classic serotonergic hallucinogens, such as lysergic dormancy caused, in part, by governmental regulation and acid diethylamide (LSD) and mescaline, with agonist proper- 7,8 societal taboo have left many unanswered questions regarding ties at the serotonin 5HT2A receptor. However, here, we the pharmacology and toxicity of hallucinogens in vivo.Thus, classify hallucinogens into three broader categories: (1) classic high-throughput screening techniques are needed to test for (serotonergic) psychedelics, (2) dissociatives, and (3) deliriants drug interactions and aberrant behavioral effects if hallucino- (Fig. 1). Classic serotonergic hallucinogens bind to serotonin gens are to gain traction as potential medicinal options, receptors and generally exhibit agonist properties. Previous 1Department of Psychiatry, College of Medicine, University of Illinois at Chicago, Chicago, Illinois. 2Research Institute for Marine Drugs and Nutrition, College of Food Science and Technology, Guangdong Ocean University (GDOU), Zhanjiang, China. 3ZENEREI Institute, Slidell, Louisiana. 4Institute of Translational Biomedicine, St. Petersburg State University, St. Petersburg, Russia. 5Institutes of Chemical Technology and Natural Sciences, Ural Federal University, Ekaterinburg, Russia. 6The International Zebrafish Neuroscience Research Consortium (ZNRC), Slidell, Louisiana. 379 380 KYZAR AND KALUEFF FIG. 1. Summary of principal pharmacological and behavioral effects of selected classes of hallucinogenic drugs. ‘‘Mixed’’ drugs that have high affinity for more than receptor shown here (e.g., ibogaine) are not included in the present chart. Note that all drugs listed possess some binding affinity for other receptors. LSD, lysergic acid diethylamide; PCP, phencyclidine. studies have suggested that agonism at the 5HT2A receptor, as nogen combining pharmacological properties of several well as substitution for the prototypical hallucinogen 2,5- classes of psychoactive drugs.18 dimethoxy-4-methylamphetamine (DOM) in discrimination Humans have long been using hallucinogenic drugs for tasks, be a requisite for inclusion in this category.8,9 Classic spiritual and religious purposes, utilizing natural plants and serotonergic hallucinogens can be further divided into two products that produce psychoactive effects when ingested.19 structural classes— indoleamines (including LSD and N,N- For example, an ayahuasca preparation consisting of Banis- dimethyltryptamine [DMT]) and phenylalkylamines (includ- teriopsis caapi vines brewed with leaves from members of the ing mescaline, DOM, and the ‘‘2C’’ class of drugs, such as 2,5- genus Psychotria is consumed by tribal people of the Amazon dimethoxy-4-bromophenethylamine [2C-B]). Basin in a ritualistic and sacramental context.20,21 Arguably, Clinically, dissociative hallucinogens produce a profound the Western conceptualization of hallucinogenic drugs began state of disconnection from reality and the surrounding en- in the late 1800s, when Arthur Heffter isolated mescaline from vironment.10 Ketamine and phencyclidine (PCP), the most the peyote cactus (Lophophora williamsii) and confirmed its commonly recognized drugs in this category, produce their subjective effects through self-experimentation.22 This was effects through antagonism at the N-methyl-D-aspartate followed by the chance discovery of LSD by Albert Hofmann (NMDA) receptor.11 Although acting through j-opioid in 1943,23 and his subsequent isolation of psilocybin from agonism rather than NMDA receptors, salvinorin A (the ac- ‘‘magic mushrooms’’ in 1958.24 tive hallucinogenic component of the plant Salvia divinorum) These early studies coalesced with growing countercul- is also considered a dissociative hallucinogen.12 tural influences, leading to a period of rapid growth in both The third group is defined by delirium-inducing agents scientific and social testing of hallucinogenic compounds. Of principally composed of alkaloids derived from plants, such particular interest was the use of LSD in psychotherapy, gi- as Atropa belladonna (deadly nightshade) and Datura stra- ven the ability of this drug to evoke experiences described as monium (Jimson weed), which act as anticholinergic ‘‘otherworldly’’ that may confer long-lasting changes to pa- agents.13,14 Typical deliriant drugs, including atropine and tients’ behavior.25 Beginning in the 1950s, numerous ex- scopolamine, cause vivid hallucinations along with physical periments probed the benefits of LSD-assisted psychotherapy symptoms of anticholinergic toxicity (e.g., dry mouth, dia- in disease states ranging from alcoholism to terminal cancer phoresis, tachycardia, and death) that are usually unpleasant diagnoses.26–29 Other studies investigated the potential cog- in nature, leaving many recreational users unwilling to repeat nitive enhancement effects of psychedelic drugs, such as the the experience. Some drugs that are considered hallucino- ability to improve creativity and problem solving.30 genic do not comfortably fit in one of the above categories. Although some early studies utilizing LSD and other hal- For example, the drug ibogaine is a naturally occurring al- lucinogenic drugs resulted in positive clinical outcomes, re- kaloid that can be isolated from members of the Apocynaceae search into psychedelic medicine halted in the early 1970s family of plants. Ibogaine possesses binding affinity for both with the passage of the United States Controlled Substances 5HT2A and NMDA receptors, as well as activity at other Act and the United Kingdom Misuse of Drugs Act. Nearly all serotonergic, opioidergic, cholinergic, and sigma recep- hallucinogenic drugs were placed in Schedule I (United tors,15–17 therefore representing a ‘‘mixed-action’’ halluci- States) or Class A (United Kingdom), implying that these PSYCHEDELIC MEDICINE AND ZEBRAFISH 381 agents have no recognized medical use. This restriction led to creased anxiety-like behavior) along with whole-body cor- a period of relatively little scientific inquiry into the biology tisol and brain c-fos expression (serving as a marker of and potential therapeutic effects of hallucinogens. Despite neuronal activation).51 The dissociation between observed this period of stagnation, a revival of scientific inquiry into behavioral anxiolysis and cortisol levels is interesting and the beneficial effects of hallucinogenic drugs has begun5,31 in may be related to increased serotonergic tone and subse- both the basic6,8 and clinical laboratories.32 The striking
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