A one-trial inhibitory avoidance task to zebrafish: Rapid acquisition of an NMDA-dependent long-term memory

Blank, Martina; Guerim, Laura D.; Cordeiro, Reinaldo F.; Vianna, Mônica Ryff Moreira Roca

doi:10.1016/j.nlm.2009.07.001

Cited by 189 publications

(160 citation statements)

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“…Studies have shown that adult zebrafish are good learners, both using food as an appetitive reward (Williams et al 2002;Colwill et al 2005) and noxious electroshock stimuli (Pradel et al 1999;Rawashdeh et al 2007;Xu et al 2007;Blank et al 2009), some of these uncovering potential anatomical pharmacological and neurochemical components of the system where learning occurs (Pradel et al 2000;Xu et al 2007;Blank et al 2009;Jesusathan 2011;Okamoto et al 2011). We have developed computer-based automated behavioral assays which we can easily control and comprehensively analyze.…”

Section: Discussionmentioning

confidence: 99%

Ontogeny of classical and operant learning behaviors in zebrafish

Valente

Huang²,

Portugues³

et al. 2012

Learn. Mem.

162

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The performance of developing zebrafish in both classical and operant conditioning assays was tested with a particular focus on the emergence of these learning behaviors during development. Strategically positioned visual cues paired with electro-shocks were used in two fully automated assays to investigate both learning paradigms. These allow the evaluation of the behavioral performance of zebrafish continuously throughout development, from larva to adult. We found that learning improves throughout development, starts reliably around week 3, and reaches adult performance levels at week 6. Adult fish quickly learned to perform perfectly, and the expression of the learned behavior is manifestly controlled by vision. The memory is behaviorally expressed in adults for at least 6 h and retrievable for at least 12 h. [Supplemental material is available for this article.] The ability to associate two environmental cues, as in classical conditioning, or to correlate one's behavior with its consequences , as in operant conditioning, are processes often essential for an animal's survival (Skinner 1984). While there are studies that have followed the ontogeny of learning behaviors in animal model systems of classical conditioning paradigms (Campbell and Ampuero 1985; Moye and Rudy 1985; Paczkowski et al. 1999; Raineki et al. 2009), the ontogeny of operant learning, in particular , remains much less explored. The ability for classical conditioning is pervasive across the animal kingdom and often interpreted as the most basic and robust form of associative learning; however, it has been shown that adding an operant component to a learning task may increase performance, or show it where it was not present before (Heisen-berg et al. 2001; Moore 2004). Zebrafish is an exceptional model of vertebrate neural development and amenable both to forward genetics and genetic manipulation (Neuhauss 2003). The transparent larvae are uniquely suited to functional imaging and have recently served to uncover fundamental mechanisms in fish locomotor control (Orger et al. 2008; Portugues and Engert 2009). Behavior is the ultimate functional readout of neural activity; indeed, behavior is the ultimate evolutionary reason for the existence of brains and the changes in behavior during development should reflect the changes the nervous system undergoes as the larval organism develops into the adult. While there are well-established learning paradigms for Drosophila and rodent experimental models, zebra-fish still lacks a systematic learning characterization. We describe here an approach to implement and test such a learning assay that utilizes the fact that zebrafish can see and track visual stimuli and clearly perform visually evoked locomotor behaviors as early as 5 d post-fertilization (dpf) (Easter and Nicola 1996; Budick and O'Malley 2000). To that end we use visually guided stimuli combined with a noxious electroshock to control learning behaviors. We characterize these assays and specifically obtain a full ontoge-ny of operant learning fr...

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Section: Discussionmentioning

confidence: 99%

Ontogeny of classical and operant learning behaviors in zebrafish

Valente

Huang²,

Portugues³

et al. 2012

Learn. Mem.

162

View full text Add to dashboard Cite

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“…For inhibitory avoidance learning, a previously described protocol was used (Blank et al, 2009;Manuel et al, 2014) with one modification: not one shock but two were given (see Fig. 4B).…”

Section: Inhibitory Avoidance Protocolmentioning

confidence: 99%

“…Unpredictable chronic stress (UCS) impedes inhibitory avoidance learning in a single-trial inhibitory avoidance paradigm in the AB zebrafish strain (Piato et al, 2011). In this paradigm, fish learn to avoid swimming from a white to a black compartment to avoid an electric shock (Blank et al, 2009;Ng et al, 2012). Recently, we studied the effects of different shock intensities on inhibitory avoidance learning in an in-house-reared Tuebingen long-fin (TLF) zebrafish strain and showed associated changes in the regulation of a number of genes involved in anxiety, fear, learning and memory when measured 2 h following the task, including grα (Manuel et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Unpredictable chronic stress decreases inhibitory avoidance learning in Tuebingen Long-Fin zebrafish (Danio rerio Hamilton): stronger effects in the resting phase than in the active phase

Manuel

Gorissen

Zethof

et al. 2014

Journal of Experimental Biology

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Zebrafish (Danio rerio Hamilton) are increasingly used as a model to study the effects of chronic stress on brain and behaviour. In rodents, unpredictable chronic stress (UCS) has a stronger effect on physiology and behaviour during the active phase than during the resting phase. Here, we applied UCS during the daytime (active phase) for 7 and 14 days or during the night-time (resting phase) for 7 nights in an in-house-reared Tuebingen long-fin (TLF) zebrafish strain. Following UCS, inhibitory avoidance learning was assessed using a 3 day protocol where fish learn to avoid swimming from a white to a black compartment where they will receive a 3 V shock. Latencies of entering the black compartment were recorded before training (day 1; first shock) and after training on day 2 (second shock) and day 3 (no shock, tissue sampling). Fish whole-body cortisol content and expression levels of genes related to stress, fear and anxiety in the telencephalon were quantified. Following 14 days of UCS during the day, inhibitory avoidance learning decreased (lower latencies on days 2 and 3); minor effects were found following 7 days of UCS. Following 7 nights of UCS, inhibitory avoidance learning decreased (lower latency on day 3). Whole-body cortisol levels showed a steady increase compared with controls (100%) from 7 days of UCS (139%), to 14 days of UCS (174%) to 7 nights of UCS (231%), suggestive of an increasing stress load. Only in the 7 nights of UCS group did expression levels of corticoid receptor genes (mr, grα, grβ) and of bdnf increase. These changes are discussed as adaptive mechanisms to maintain neuronal integrity and prevent overload, and as being indicative of a state of high stress load. Overall, our data suggest that stressors during the resting phase have a stronger impact than during the active phase. Our data warrant further studies on the effect of UCS on stress axis-related genes, especially grβ; in mammals this receptor has been implicated in glucocorticoid resistance and depression.

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“…Behavioral studies have shown that zebrafish are capable of learning various tasks such as spatial alteration, active avoidance conditioning, and plus maze (Pradel et al, 1999(Pradel et al, , 2000Swain et al, 2004;Xu et al, 2009;Sison and Gerlai, 2010). In addition, major neurotransmitters present in the rat brain play a role in the zebrafish brain function; for example, blockade of NMDA receptor activation that is crucial in the learning process in rats blocks acquisition of passive avoidance learning in zebrafish (Blank et al, 2009).…”

Section: Introductionmentioning

confidence: 99%