Extending the analysis of zebrafish behavioral endophenotypes for modeling psychiatric disorders: Fear conditioning to conspecific alarm response

Maximino, Caio; Meinerz, Daniele L.; Fontana, Bárbara D.; Mezzomo, Nathana J.; Stefanello, Flavia V.; Prestes, Alessandro de Souza; Batista, Cibele Boeira; Rubin, Maribel Antonello; Barbosa, Nilda Vargas; Rocha, João Batista Teixeira da; Lima, Mônica Gomes

doi:10.1016/j.beproc.2018.01.020

Cited by 50 publications

(21 citation statements)

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“…The novel tank diving test is commonly used for analyzing exploratory and locomotor profiles. Moreover this task is often used to analyze anxiety-like behavior being sensitive to a range of anxiogenic and anxiolytic drugs in absence or presence of different aversive stimulus (Egan et al, 2009; Maximino et al, 2018; Mezzomo, Silveira, Giuliani, Quadros, & Rosemberg, 2016; Wong et al, 2010). Zebrafish ( n= 23 ) were placed individually in a novel tank (22 - 26 cm length x 15 cm height x 9 cm width) ( Fig.…”

Section: Methodsmentioning

confidence: 99%

Moderate early-life stress improves adult zebrafish (Danio rerio) spatial short-term memory but does not affect social and anxiety-like responses

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Gibbon

Sudwarts

et al. 2020

Preprint

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5Early-life stress (ELS) is defined as a short or chronic period of trauma, environmental or 3 6 social deprivation, which can affect different neurochemical and behavioral patterns during 3 7 adulthood. Zebrafish (Danio rerio) have been widely used as a model system to understand human 3 8 neurodevelopmental disorders and display translationally relevant behavioral and stress-regulating 3 9systems. In this study, we aimed to investigate the effects of moderate ELS by exposing young 4 0 animals (six weeks post-fertilization), for three consecutive days, to three stressors, and analyzing 4 1 the impact of this on adult zebrafish behavior (sixteen weeks post-fertilization). The ELS impact in 4 2 adults was assessed though analysis of performance on tests of unconditioned memory (free 4 3 movement pattern Y-maze test), exploratory and anxiety-related task (novel tank diving test) and 4 4 social cohesion (shoaling test). Here, we show for the first time that moderate ELS increases the 4 5 number of pure alternations compared to pure repetitions in the unconditioned Y-maze task, 4 6suggesting increased spatial short-term memory, but has no effect on shoal cohesion, locomotor 4 7 profile or anxiety-like behavior. Overall, our data suggest that moderate ELS may be linked to 4 8 adaptive flexibility which contributes to build 'resilience' in adult zebrafish by improving short-4 9 term spatial memory performance. 5 0 5 1

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Section: Methodsmentioning

confidence: 99%

Moderate early-life stress improves adult zebrafish (Danio rerio) spatial short-term memory but does not affect social and anxiety-like responses

Fontana

Gibbon

Sudwarts

et al. 2020

Preprint

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“…Although the organization of the zebrafish central nervous system (CNS) is simpler than those of mammals 12 , various brain structures of teleost fish are structurally homologous to those of mammals 13 , allowing the investigation of basic neural processes underlying complex behaviors (e.g., aggression, anxiety, and fear) 14 . Moreover, studies involving learning and memory processing reveal the growing utility of zebrafish to assess aversive conditioning [15][16][17] , spatial and aversive memories 18,19 , and positive reinforcement 20,21 .…”

Section: Introductionmentioning

confidence: 99%

Exploring Object Discrimination in Zebrafish: Behavioral Performance and Scopolamine-Induced Cognitive Deficits at Different Retention Intervals

et al. 2019

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The object discrimination test allows the testing of different memory retention periods. However, few behavioral endpoints have been measured in fish species such that retention is often assessed using a single parameter (time spent in object area). Here, we aimed to explore the object discrimination test in zebrafish by assessing their behavioral performance after 1 h or 24 h retention interval periods. To characterize putative interaction-like behaviors, fish were tested in the absence or presence of scopolamine (1 h before test session). Zebrafish were habituated for three consecutive days in the experimental tank and training session was performed for 10 min using two identical nonpreferred objects (black cube or sphere). After the retention intervals, a familiar object was replaced by a novel object (test session, 10 min). Fish were also exposed to the novel tank diving test to assess locomotion and anxiety-like behaviors. At 1 h retention interval, animals performed more circular-like investigation near the familiar object, whereas 24 h after training session, a prominent rapid investigation was observed when animals explore the non-familiar object. Because scopolamine abolished these phenotypes, as well as the increased time spent in the novel object area during the test without changing locomotion and anxiety-related parameters, the behavioral responses described here may predictively reflect interaction-like behaviors involved in object discrimination memory in zebrafish models.

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“…These two research traditions rarely cross‐fertilized each other; however, good ethological validation, ecological relevance and adequate knowledge of the neural bases of a given behavioural function are crucial for its use as a model system in the behavioural neurosciences and neuropharmacology (van der Staay, ; Maximino & van der Staay, ). As a result, and as a consequence of the ascension of D. rerio as a model organism in the field (Kalueff et al ., ; Shams et al ., ; Stewart, Yang, et al ., ), more focus has been given on the applications of CAS as an aversive stimulus in many different paradigms, from aversive conditioning (Maximino et al ., ; Ruhl et al ., ) to behavioural models in psychopathology (§ 5).…”

Section: Discussionmentioning

confidence: 98%

“…The application of the kin‐selection hypothesis to the evolution of CAS necessitates at least two assumptions (Smith, ): first, there should be evidence that CAS release increases the receiver's fitness; secondly, it should be shown that individuals in a given species associate mainly with kin. There is now ample evidence that CAS increases vigilance, leading to antipredator behaviour such as that described here (§ 5), as well as long‐term alterations in foraging (Oswald & Robison, ), fear‐induced analgesia (Maximino, ; Maximino et al ., ) and avoidance of areas in which CAS is detected (Chivers & Smith, ; Wisenden et al ., ) or which were previously associated with CAS (Ruhl et al ., ; Maximino et al ., ). Poecilia reticulata exposed to CAS are more attentive to visual cues (Stephenson, ) and D. rerio exposed to CAS show increased risk assessment in the light–dark test (Maximino et al ., ; Quadros et al ., ), suggesting that CAS increases alertness to threatening cues in other sensory modalities.…”

Section: Adaptive and Evolutionary Issues For Alarm Signalsmentioning

confidence: 97%

“…These adjustments include fear‐induced analgesia (Maximino, ; Maximino et al ., ), an inhibition of nocifensive behaviour that is thought to allow receivers to flee even when they are injured. Moreover, CAS also serves as a platform for learning, as animals learn to avoid areas or cues which were previously associated with schreckstoff exposure (Hall & Suboski, , 1995b; Maximino et al ., ; Ruhl et al ., ). Finally, as appears to be the case with predator odours in rodents (Blanchard et al ., ), CAS can also produce long‐term (time‐dependent) sensitization of defensive responses (Lima et al ., , ), suggesting a basis for the creation of models for post‐traumatic stress disorder (Section 10).…”

Section: What Are the Behavioural Effects Of Cas?mentioning

confidence: 99%

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Sensory ecology of ostariophysan alarm substances

Maximino

Silva

Campos

et al. 2018

Journal of Fish Biology

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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.

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Extending the analysis of zebrafish behavioral endophenotypes for modeling psychiatric disorders: Fear conditioning to conspecific alarm response

Cited by 50 publications

References 49 publications

Moderate early-life stress improves adult zebrafish (Danio rerio) spatial short-term memory but does not affect social and anxiety-like responses

Moderate early-life stress improves adult zebrafish (Danio rerio) spatial short-term memory but does not affect social and anxiety-like responses

Exploring Object Discrimination in Zebrafish: Behavioral Performance and Scopolamine-Induced Cognitive Deficits at Different Retention Intervals

Sensory ecology of ostariophysan alarm substances

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