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The Plus Maze and Scototaxis Test Are Not Valid Behavioral Assays for Anxiety Assessment in the South African Clawed Frog

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The Plus Maze and Scototaxis Test Are Not Valid Behavioral Assays for Anxiety Assessment in the South African Clawed Frog Journal of Comparative Physiology A (2019) 205:567–582 https://doi.org/10.1007/s00359-019-01351-3 ORIGINAL PAPER The plus maze and scototaxis test are not valid behavioral assays for anxiety assessment in the South African clawed frog R. Boone Coleman1,2 · Kelsey Aguirre1 · Hannah P. Spiegel1 · Celina Pecos1 · James A. Carr1 · Breanna N. Harris1 Received: 23 October 2018 / Revised: 17 May 2019 / Accepted: 24 May 2019 / Published online: 29 May 2019 © Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract There are no behavioral models for testing anxiety in amphibians, a group of animals widely used for developmental, ecotoxi- cological, and genetic research. We aimed to validate two common rodent paradigms, the plus maze and the scototaxis test, for use in the aquatic African clawed frog (Xenopus laevis). We predicted: (a) that frogs would prefer the dark, vs. light, por- tions of the testing arenas (face validity), (b) that this behavior could be altered with acute administration of anxio-selective drugs (construct validity), and (c) that time spent in the dark portions of the arenas would be positively correlated (predictive validity). Prior to testing, frogs were treated with fuoxetine (selective serotonin reuptake inhibitor [SSRI]), desipramine (serotonin- and norepinephrine-reuptake inhibitor), cafeine (methylxanthine, adenosine receptor antagonist, phosphodies- terase inhibitor), saline, or were left unmanipulated. Each drug was administered acutely (1 h prior to testing; cafeine) or subacutely (24, 3, and 1 h prior to testing; fuoxetine, desipramine) at one of three doses. Plus maze and scototaxis testing were separated by 1 week; each frog completed both behavioral tasks and was treated with the same drug regimen prior to testing. Overall, both tests showed face validity, however, data suggest these paradigms lack both construct and predictive validity. Keywords Ecotoxicology · SSRI · Amphibian · Cafeine · PPCP Abbreviations environment (Perusini and Fanselow 2015; Clinchy et al. PPCP Pharmaceutical and personal care product 2011; Steimer 2011; Harris and Carr 2016), and this state RDoC Research Domain Criteria is experienced by multiple taxa, including nematode worms SSRI Selective serotonin reuptake inhibitor (Liu et al. 2018), crayfsh (Fossat et al. 2014), fsh (Stew- TCA​ Tricyclic antidepressant art et al. 2012), rodents (Walf and Frye 2007), and humans (Craske et al. 2017). Anxiety, however, can be difcult to defne clinically, and diagnosis is often based on subjective Introduction assessments, making studies of causes and consequences of anxiety difcult. The National Institute of Mental Health has Anxiety is a complex and evolutionarily conserved (emo- proposed the use of Research Domain Criteria (RDoC) to tional) state associated with predictable changes in behav- better classify and defne emotions and psychopathologies. ior that are generally dissociated from an external stimulus The RDoC framework uses multiple biomarkers to develop (McNaughton and Zangrossi 2008). A state of anxiety can specifc constructs associated with psychological conditions arise from potential physical or psychological dangers in the to better understand and diagnose the physiological pheno- types of human behaviors and mental disorders (Insel 2014). The goal of this framework is that, in the future, biomarkers Electronic supplementary material The online version of this will be used to understand the distinguishing etiology of article (https ://doi.org/10.1007/s0035 9-019-01351 -3) contains such conditions (Cuthbert and Insel 2013). It holds great supplementary material, which is available to authorized users. promise, but due to ethical and logistical constraints, it is * Breanna N. Harris often difcult to completely study the biological underpin- [email protected] nings of anxiety in humans. Thus, using animal models to manipulate and measure anxiety and corresponding bio- 1 Department of Biological Sciences, Texas Tech University, MS 3131, Lubbock, TX 79409, USA markers is critical (Blanchard et al. 2013; Anderzhanova et al. 2017). In addition, by developing multiple animal 2 Honors College, Texas Tech University, Lubbock, TX, USA Vol.:(0123456789)1 3 568 Journal of Comparative Physiology A (2019) 205:567–582 models of anxiety, and thus having evolutionary (cross-spe- should be sensitive to SSRIs (Borsini et al. 2002). Both the cies) validity, we will be able to elucidate the core traits and plus maze and the scototaxis test are clinical representations behaviors associated with various forms of anxiety (Kaluef of the most common form of anxiety: generalized anxiety et al. 2012; Stewart and Kaluef 2015). disorder (Griebel and Holmes 2013). Given that general Behavioral paradigms to assess anxiety in rodents are anxiety disorder is routinely treated with serotonin-modi- common and include the elevated plus maze, open- feld fying drugs (e.g., SSRIs, 5HT-1A agonists, TCAs; Zohar test, light/dark (scototaxis) test, vogel confict, and condi- and Westenberg 2000; Griebel and Holmes 2013), and that tioned fear test (Griebel and Holmes 2013). The (elevated) acute and chronic administration of these drugs can be efec- plus maze test and the scototaxis (light/dark) test are the tive in rodent models (see Borsini et al. 2002; Griebel and most widely used and extensively validated unconditioned Holmes 2013), we chose to use an SSRI and a TCA in our response paradigms for studying the physiological and study. Additionally, SSRIs and TCAs are both efective in neural underpinnings of anxiety and the efects of anxio- the treatment of many types of anxiety and both are safer selective drugs in rodents (Pellow et al. 1985; Bourin and than benzodiazepines (Lembke et al. 2018), but SSRIs can Hascoët 2003; Carobrez and Bertoglio 2005; Maximino treat a wider range of anxiety types (Zohar and Westenberg et al. 2011; Griebel and Holmes 2013; Kumar et al. 2013). 2000). Cafeine is one of the most consumed psychoactive However, data from human and rodent studies cannot pin- drugs in the world (James 1997) and can act as an anxi- point the individual roles the prefrontal cortex and the limbic ogenic agent (Smith 2002). system play in aspects of anxiety as in these species both Thus, our goals were to determine whether (1) the plus brain regions are important for this emotional state (David- maze and scototaxis behavioral paradigms pass face valid- son 2002; Ressler and Mayberg 2007). In amphibians the ity in Xenopus laevis and (2) these behavioral paradigms limbic circuitry is conserved and operates independently of show construct and predictive validity in this species. Using a brain cortex, allowing us to examine in an isolated way the anxiolytic (one SSRI and one TCA) and anxiogenic (caf- subcortical pathways involved in initiating and maintaining feine) drugs, we determined if behavior in the plus maze anxiety (Sokolowski and Corbin 2012; Carr 2015). and scototaxis test can be predictably altered. In addition to To date, no amphibian anxiety behavioral paradigms time in light/dark and entries into sections, we measured air exist. Here, we aimed to validate two different anxiety gulps and thigmotaxis. We predicted that anxious animals behavior assays, the plus maze test and the scototaxis test, would take fewer air gulps, as data in goldfsh (Matsuda for use in the aquatic amphibian the African clawed frog, et al. 2013), zebrafsh (Egan et al. 2009; Sackerman et al. Xenopus laevis. Assessing the validity of an animal behav- 2010; Blaser and Rosemberg 2012), and X. laevis (Duggan ioral model is critical for making data comparable between et al. 2016) suggest that anxious aquatic animals spend more laboratories and across species, and thus is crucial for trans- time away from the surface. We chose to categorize loca- lational research (van der Staay et al. 2009; Maximino et al. tion position because thigmotaxic, or wall hugging, is typi- 2010a; Blanchard et al. 2013; Stewart and Kaluef 2015). cally assessed in anxiety assays as animals naturally tend Therefore, to develop any animal model/behavioral para- to stay closer toward walls and avoid the open spaces i.e. digm, we must frst assess its face, construct, and predictive they are centro-phobic (Simon et al. 1994; Treit et al. 2009; validity (Willner 1984; Treit et al. 2009; Nestler and Hyman Kumar et al. 2013). For example, larval zebrafsh exposed 2010; Belzung and Lemoine 2011; Goswami et al. 2013; to cafeine, versus controls, spent more time at the tank Steward and Kaluef 2015). To do so, we use the validity edge (Richendrfer et al. 2012). This behavior is relevant defnitions of Walf and Frye (2007). for zebrafsh (Maximino et al. 2010b) and likely relevant The plus maze and scototaxis are ethological confict-type for X. laevis as Prater and colleagues recently showed that tests (Kumar at el. 2013) and rely on innate light–dark pref- Xenopus injected with the anxiogenic peptide corticotropin- erence. For light–dark-based anxiety tests, validation studies releasing factor increased time on the edge of the tank com- typically involve administering anxiogenic (e.g., cafeine, pared to unmanipulated frogs (Prater et al. 2018). Overall, carbon dioxide, sodium lactate) or anxiolytic agents (e.g., we predicted that (1) control animals would spend the great- selective-serotonin reuptake inhibitors [SSRI], tricyclic est duration of time in the dark portion of the testing arenas antidepressants [TCA], benzodiazepines, or alcohol) prior and, in the scototaxis test, spend a higher proportion
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