Types of Learning and Memory in Zebrafish: History
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Jen Kit Tan
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Faris Hazwan Nazar
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Suzana Makpol
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Seong Lin Teoh

Cognition is the mental process of acquiring knowledge and understanding through thinking, learning, memorizing and sensing. Zebrafish display different learning abilities, such as associative, non-associative, social (shoaling) and motor learning. In social learning, a group of zebrafish learned faster than a single individual. In motor learning, zebrafish adapted locomotor commands to execute accurate movements that relied on sensory feedback 

  • zebrafish
  • pharmacological model
  • drug screening
  • learning and memory

1. Introduction

Zebrafish (Danio rerio) are tropical fish native to southern Asia and became a vertebrate model organism in developmental biology pioneered by George Streisinger in the 1970s at the University of Oregon. Since then, zebrafish have emerged as one of the animal models in preclinical studies for understanding various physiological processes and diseases. The growing interest is attributed to the favorable features offered by this species. These include ex vivo fertilization, transparent embryos and larvae (facilitate imaging), small size (2–5 cm for adult), easy maintenance, prolific nature (more than 100 eggs produced per fish), rapid development (larvae start to swim freely at 5 days post fertilization, dpf), their accessibility for genetic manipulations such as CRISPR and high homology (70%) to the human genome [1][2][3]. These features allow the setting up of laboratory facilities and experiments at a low cost [4]. Hence, zebrafish animal models provide an unprecedented opportunity for medium- to high-throughput screening in drug discovery for numerous disease models, such as cancer, organ regeneration and neurodegenerative disorders [3][5][6].
Dementia is the progressive deterioration of cognitive functions, including learning and memory processes, beyond the usual rate of aging. Age is the major risk factor for dementia. Alzheimer disease (AD) is the most prevalent form of dementia (60–70%) that affects more than 57 million people globally [7]. The two main classes of AD are familial AD and sporadic AD. Familial AD accounts for less than 5% of AD cases. Its main hallmarks are mutations involving amyloid precursor protein, presenilin 1 and presenilin 2. Sporadic AD is associated with environmental factors and genetic susceptibilities such as the apolipoprotein E genotype [8][9][10]. Despite the intensive efforts in drug development for AD, effective interventions remain limited. Some of the main challenges are the diverse etiology and complex risk factors in AD. Furthermore, the lack of biomarkers for early diagnosis means the disease has to progress to an advanced stage until the manifestation of signs and symptoms can be identified [11]. One of the main objectives of AD research is the development of medications that can slow or improve the main symptom of AD, i.e., memory lapses.
Zebrafish show a high degree of conservation in the neuroanatomical organization and neurotransmitter signaling pathways with humans [10][11]. The dorsal, medial and lateral pallium of zebrafish correspond to the isocortex, amygdala and hippocampus in mammals, respectively. The zebrafish encephalon is divided into diencephalon (forebrain), telencephalon (midbrain) and cerebellum (hindbrain). Zebrafish also retain the main excitatory glutamatergic and inhibitory GABAergic neurotransmissions and express muscarinic cholinergic receptors [10]. Neurobehaviors related to learning and memory were first reported over two decades ago [12]. Since then, a repertoire of behaviors comparable to a human, such as locomotor activity, anxiety-like behaviors, learning, memory retention, spatial and object recognition, fear responses and social preference and interaction, has been characterized in this animal [10]. These features have opened up the chance to engage zebrafish as an alternative vertebrate model in cognitive decline-related research, especially for drug discovery.
Non-human primates and rodents are the classical animal models for behavioral studies involving cognition [13]. Non-human primates have the closest neurobehavioral profiles to humans, but these studies are the costliest among other model organisms and are subject to strict ethical considerations. Rodents have been traditionally used as genetic and pharmacological models in cognitive research, but the experimental cost limits their application in large-scale drug screening. Non-mammalian organisms, such as teleost fish, fruit flies and honeybees, are being used as a complementary model because of their low costs, which are amenable to high-throughput screening [14]. Zebrafish is the most popular non-mammalian model for cognitive research because it is a vertebrate and displays a repertoire of neurobehaviors that can be related to humans. Nonetheless, findings from zebrafish studies require further validation in mammalian models before being translated into clinical trials.

2. Types of Learning and Memory in Zebrafish

Cognition is the mental process of acquiring knowledge and understanding through thinking, learning, memorizing and sensing. The cognitive process includes sensation, perception, motor skills, attention, memory, executive function, language and processing speed [15]. Learning and memory performance is one of the most commonly assessed cognitive domains in AD research for drug discovery. Learning is the process of acquiring new information through the formation of memory, while memory is the process of consolidating, storing and recalling the acquired information [16]. Learning and memory are not the same, but both terms are often used interchangeably, especially in animal studies, because both processes are highly interdependent and difficult to distinguish and interpret alone.
Zebrafish display different learning abilities, such as associative, non-associative, social (shoaling) and motor learning. In social learning, a group of zebrafish learned faster than a single individual [17]. In motor learning, zebrafish adapted locomotor commands to execute accurate movements that relied on sensory feedback [18]. This section will only focus on associative and non-associative learning because their paradigms (especially associative learning) are widely used to assess learning and memory performance in zebrafish pharmacological models (Table 1).
Table 1. Types of non-associative and associative learning.
Category Subcategory Paradigm Further Subcategory Behavioral Response Example Reference
Non-associative learning
Habituation - Continuous exposure of stimulus - Decrease Reduced zebrafish startle response to repeated sound stimulus [19]
Sensitization - - Increase Repeated nicotine exposure increased locomotor activity and sensitivity of zebrafish [20]
Associative learning
Classical (Pavlovian) Appetitive conditioning Association of favorable stimulus with cue - Increase/Decrease
(involuntary response)		 Increased dog salivation upon hearing sound of bell that was previously paired with food -
Aversive conditioning Association of unfavorable stimulus with cue - Increase/Decrease
(involuntary response)		 Decreased zebrafish distance traveled in tank that was previously paired with electric shock (Increased contextual fear response) [21]
Increased zebrafish freezing time and erratic movement in tank that was previously paired with electric shock (Increased contextual fear response) [22]
Operant (Instrumental) Positive reinforcement Association of behavioral response with administration of appetitive stimulus - Increase Increased zebrafish approach to a response key that was equipped with a sensor to dispense brine shrimp eggs [23]
Negative reinforcement Association of behavioral response with removal of aversive stimulus Escape learning
(Engage a behavior to remove the existing aversive stimulus)		 Increase Increased rodent crossing response from a compartment with existing foot shock to the opposite compartment in a shuttle box -
Active avoidance
(Engage a behavior to prevent the occurrence of aversive stimulus)		 Increased zebrafish crossing response to a compartment without electric shock upon the presentation of light signal that was previously paired with administration of the shock [24]
Passive (inhibitory) avoidance
(Suppress an innate behavior to prevent the occurrence of aversive stimulus)		 Increased zebrafish latency to enter dark (preferred) compartment that was previously paired with electric shock [25]
Positive punishment Association of behavioral response with administration of aversive stimulus - Decrease Refrained from pressing a lever that will lead to foot shock for a rodent -
Negative punishment Association of behavioral response with removal of appetitive stimulus - Decrease Decreased the undesired behavior by taking away the reward in a dog training -

2.1. Non-Associative Learning

Non-associative learning is a general lasting change in response strength toward a stimulus due to repeated exposure. Non-associative learning is further categorized into habituation and sensitization. Habituation is the decrease while sensitization is the increase in the animal’s response to a sensory stimulus upon continuous exposure. The changes in responses could be in the short- and long-term. Habituation has been regarded as an evolutionarily conserved behavior for optimal survival. Habituation allows the animal to disregard repeated stimuli while focusing on important stimuli such as potential predators and danger in the environment [1][19]. In the laboratory setting, prolonged exposure to a series of acoustic stimuli [19] and reduced light of the surrounding environment [26] reduced the startle response in zebrafish larvae. The larvae were habituated to the sensory stimuli and could exhibit non-associative learning as early as 5 to 7 dpf. In contrast, sensitization is not commonly reported in zebrafish studies. A previous study has used sensitization to assess drug addiction. Pisera-Fuester and coworkers showed that repeated administration of nicotine and cocaine at sub-threshold doses increased the zebrafish locomotor activity and sensitivity in a subsequent paradigm known as conditioned place preference (a contextual associative conditioning with appetitive stimulus) [20]. The sensitization procedure has potentiated the induction of addiction in the animal.

2.2. Associative Learning

Associative learning is the process of acquiring new information by linking two elements. This type of learning is more commonly assessed than non-associative learning in zebrafish studies. The two forms of associative learning are classical (Pavlovian) and operant (instrumental) conditioning [1][16][27]. In classical conditioning, an initially neutral stimulus is repeatedly paired with an unconditional stimulus (US) that elicits an involuntary reflex response (unconditioned response) until the neutral stimulus triggers the response upon subsequent exposure. The neutral stimulus has become the conditional stimulus (CS) that initiates the conditioned response when the animal learns to associate the CS with the US after repeated pairing.
In operant conditioning, an animal learns to correlate its voluntary behavioral responses with their consequences [28]. The term was first introduced by B.F. Skinner in 1937 to define associative learning made between a behavior and its consequence, which differed from classical conditioning [29]. The delivery of an US is determined by the behavioral response to modify (strengthen or weaken) the operant behavior. The US can be paired with a neutral stimulus until the administration of the neutral stimulus alone can trigger the conditioned response. In the end, the behavioral responses that result in favorable consequences are reinforced, whereas those that lead to undesirable outcomes are weakened.

2.2.1. Classical Conditioning

Classical conditioning can be further divided into appetitive and aversive conditioning based on the nature of the US. Appetitive conditioning utilizes favorable stimuli as the US. Sison and Gerlai demonstrated that zebrafish are capable of associative learning by using food as the reward and a red card as the visual cue [30]. After the conditioning, the zebrafish spent more time in the target arm based on the position of the red card that was previously paired with the food during the training session. Although the authors classified the learning as classical conditioning, the preference was scored based on the time spent in the targeted arm. Precisely, the response should be considered as voluntary, such that the zebrafish had to perform the behavior (choose the correct arm) to receive the outcome. There is hardly any paradigm that actually evaluates the classical appetitive conditioning in zebrafish, because the involuntary responses toward rewards (food or sight of conspecific) in zebrafish have not been well-characterized so far.
In aversive conditioning, the CS is paired with a fear-inducing US that leads to a fear-related conditioned response when the CS is administered alone. The nature of the CS can be contextual (location or environment) or cued (sensory like visual cues). The most commonly used aversive US in zebrafish studies is the application of electric shock (ES). Fear conditioning is the most common form of classical learning assessed in zebrafish. Valente and colleagues demonstrated that both larval and adult zebrafish could perform cued fear conditioning in a paradigm that associated a checkerboard pattern (CS) with the ES (US) [31]. After training, the fish exhibited a conditioned fear response by preferring the non ES-paired area when the visual cue was administered alone. The classical learning started as early as 3 weeks post fertilization (wpf), and the performance reached a level comparable to 1 year-old adult fish by 6 wpf. Although the authors considered this form of learning as classical conditioning, the performance index was scored based on the animal’s position and turning behavior that should be regarded as voluntary responses.
In contextual fear conditioning, a novel environment is associated with the US. Kenney and colleagues showed that contextual fear conditioning in zebrafish lasted for at least 14 days and varied in the fear extinction rates among different strains [21]. Extinction is a process in associative learning such that repeated exposure to the CS without the US will eventually reduce the conditioned response. The fear response was evaluated based on the distance traveled in the tank (locomotion activity) which can be considered as an involuntary behavior. Classical fear conditioning of TU zebrafish strain extinguished more quickly than AB and TL background strains.
Fear-related responses include freezing (immobility), erratic movements (zigzagging), bottom-dwelling, a tighter shoal, leaping (jumping) and thigmotaxis [32]. In the study by Baker and Wong, they used the alarm substance released from the fish skin when injured as an olfactory cue (US) to trigger anti-predatory (fear) responses such as freezing duration and erratic movements [22]. Interestingly, contextual fear learning and memory in zebrafish differed by the stress coping styles. Fear memory was acquired faster in zebrafish with a reactive stress coping style than in proactive fish. The authors postulated that a faster learning rate in reactive fish might facilitate memory encoding. The reactive fish are more sensitive to environmental cues by perceiving the fear stimulus as more threatening and becoming more risk-averse. This may lead to longer fear memory retention in the reactive fish as observed in the study. At the molecular level, the influence of stress coping styles on learning and memory performance could be explained by the difference in the transcriptomic state of the zebrafish brain. The reactive fish brain showed increased expression of genes related to synaptic plasticity and neurotransmission [33]. Maximino et al. reported that neurotransmitters such as epinephrine and norepinephrine in the autonomic nervous system and extracellular serotonin levels in the zebrafish brain increased after the exposure of conspecific alarm substance [34]. The study demonstrated that fear-induced responses and sympathetic activation were mediated by the serotonin transporter.

2.2.2. Operant Conditioning

Operant conditioning can be classified as reinforcement or punishment, such that the paradigm increases or decreases the response to modify the strength of the response over the course of training. The reinforcement in operant conditioning can be positive (addition of reward as a reinforcer) or negative (removal of aversive stimulus as a reinforcer). Both positive and negative reinforcement paradigms are aimed at strengthening the behavioral response.
Positive reinforcement administers the appetitive US after the animal performs a behavioral response to strengthen the response. Manabe and co-workers developed an automated operant device for positive reinforcement conditioning in zebrafish. The response key was equipped with a sensor that dispenses brine shrimp eggs when it was approached by zebrafish [23]. In the paradigm, the red LED attached to the response key was first illuminated and then switched off when the fish approached the response key, followed by the dispensation of food.
Negative reinforcement removes the aversive US when the animal engages in a behavioral response. This type of conditioning can be further divided into escape learning and avoidance (active and passive). Escape learning refers to the animal engages a behavior to terminate the ongoing aversive stimulus. For example, the crossing response of rodents will be increased from a compartment with existing foot shock to the opposite compartment in a shuttle box. The active avoidance paradigm requires the presentation of a cue (visual/auditory/contextual) prior to the administration of an aversive stimulus. Active avoidance was performed to prevent the happening of the aversive stimulus. Xu and colleagues demonstrated that zebrafish increased crossing response to a compartment without ES upon presenting a light signal previously paired with the administration of ES [24]. In passive avoidance, also known as inhibitory avoidance, the conditioning suppresses an innate behavior to avoid the occurrence of an aversive stimulus. For example, zebrafish have an innate response to enter a dark environment (scototaxis) [25]. In the paradigm, the ES was applied when the fish entered the dark compartment of a tank. After the conditioning, the latency to enter the dark compartment was increased [25][35].
Similarly, punishment-based operant conditioning is divided into positive (impose punishment) and negative (remove appetitive stimulus as punishment). Both positive and negative punishment paradigms are aimed at weakening the behavioral response. For positive punishment, an aversive US is administered when a behavioral response is engaged, eventually leading to a decreased behavioral response. The difference between positive punishment, escape learning and avoidance is that the behavior response in positive punishment leads to the administration of an aversive stimulus, while the behavioral response in the latter two negative reinforcement results in the removal/prevention of an aversive stimulus. For example, in positive punishment conditioning, a rodent learns to refrain from pressing a lever that will lead to foot shock.
For negative punishment, an appetitive US is removed when the animal performs a behavioral response. For instance, this conditioning is used in dog training to correct undesired behavior by taking away the reward (food or toy). Both positive and negative punishments have not been engaged in pharmacological studies using zebrafish as models to assess cognitive performance.

2.3. Remarks on Leaning Conditionings in Zebrafish

In summary, zebrafish are capable of performing both non-associative and associative learning tasks. This allows the researcher to assess the zebrafish’s cognitive performance using various tests. From a survival perspective, operant learning allows the animals to find a safe and rewarding outcome while avoiding danger in a complex environment. Unsurprisingly, operant conditioning is pervasive in zebrafish studies because task performance could be enhanced by adding an operant component [31]. Nevertheless, not all types of operant conditioning can be assessed in zebrafish as in the rodent models due to lack of a suitable operant box that can be accessed by many laboratories, In addition, the nature (involuntary and voluntary) of some behaviors, especially for classical conditioning, in zebrafish is not clearly defined (for example, location preference, time spent). In a review by Pritchett and Brenna, the authors considered that many behavioral tasks in zebrafish are actually a hybrid of classical and operant conditioning [27].

2.4. Memory

Memory can be classified mainly into sensory, short-term and long-term [36][37]. Sensory memory is further divided into haptic (based on sight stimuli), echoic (based on auditory stimuli) and iconic (based on touch stimuli) memory. Based on the duration of holding, memory is divided into short- and long-term. Working memory is a form of short-term memory that not only temporarily retains but manipulates the information for cognition, including learning, reasoning and language comprehension. Long-term memory can be further grouped as declarative (explicit or conscious) and non-declarative (implicit or unconscious) memory. There are two types of declarative memory, namely episodic (stores personal experience) and semantic (stores facts and conceptual knowledge) memory. The four types of non-declarative memory include procedural (recalling motor and executive skills), associative, non-associative and priming (influence of a pre-exposed/suggested stimulus on response to the next stimulus) memory.
Not all forms of memory can be evaluated in zebrafish as model organisms. Similar to rodent models, the most common types of memory assessed in zebrafish for cognitive studies are spatial, recognition and associative memory. To score the memory retention index, a time delay between the training (familiarization) and test (probe) phases is required. Spatial memory in zebrafish is assessed based on the preference of zebrafish for new space/area. The cue to a novel place could be contextual or visual (such as geometric cues of circle, triangle and square around the tank). Cognato et al. showed that spatial memory in zebrafish lasted up to 3 h after the familiarization session and diminished after 6 h of exposure [38]. Objective recognition memory in zebrafish refers to the preference of zebrafish for a new object. By using virtual objects presented via iPod, Braida et al. demonstrated that object recognition memory lasted up to 24 h post-familiarization session [39]. Interestingly, Madeira and Oliveira reported that zebrafish were capable of social recognition memory, i.e., the preference for new conspecifics, in a social discrimination paradigm [40]. The zebrafish were exposed to two conspecifics via perforated partitions such that the recognition relied on visual and olfactory cues. Zebrafish had increased exploration time toward novel conspecifics than familiar conspecifics after 24 h post-familiarization session. Associative memory in zebrafish based on passive avoidance [25] and appetitive conditioning [41] has been reported. Previous studies also explored other more complex forms of memory such as working memory [42][43] and episodic-like memory [44] in zebrafish. As these forms of memory are challenging to be defined and tested in animals, more evidence is required to confirm the presence of these forms of memory in zebrafish.

This entry is adapted from the peer-reviewed paper 10.3390/molecules27217374

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