Early-Life Social Experience Shapes Social Avoidance Reactions in Larval Zebrafish

Groneberg, Antonia H.; Marques, João C.; Martins, A. Lucas; Corral, Ruth Díez del; Polavieja, Gonzalo G. de; Orger, Michael B.

doi:10.1016/j.cub.2020.07.088

Cited by 48 publications

(63 citation statements)

References 87 publications

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“…A social preference experiment by Engeszer et al (2004) demonstrated that when striped wildtype (WT) zebrafish and non-striped nacre zebrafish (lacking stripes due to mutation in the mitfa gene) were reared either with their genotype or the opposite (WT raised with nacre and vice versa), the experimental fish preferred the phenotype they were reared with, regardless of their genotype. Lastly, zebrafish raised in complete social isolation were found to stay significantly further away from shoal mates and showed diminished social preference compared to zebrafish raised in normal social conditions, demonstrating that lack of access to social stimuli during early development leads to abnormal social response (Engeszer et al, 2004;Shams et al, 2018;Groneberg et al, 2020). Preliminary studies of our own also suggest that enriched social and/or physical environment may rescue embryonic alcohol exposure-induced social behavioral deficits in zebrafish.…”

Section: The Development Of Shoaling Behaviormentioning

confidence: 58%

“…The dynamics of this group forming behavior is highly complex and debated to this day. Numerous environmental factors play roles in shoal formation, including vegetation, water flow speed, temperature, age of the fish, geographical location, existing shoal size, predation, early life experience, and food availability, to name a few (Ruhl and McRobert, 2005;Gerlai, 2007, 2011;Arganda et al, 2012;Suriyampola et al, 2016;Orger and de Polavieja, 2017;Groneberg et al, 2020). For example, zebrafish in still waters are more likely to form smaller shoals compared to fast-moving water, where shoals of upwards of 300 individuals have been observed (Suriyampola et al, 2016).…”

Section: Zebrafish Shoaling Behaviormentioning

confidence: 99%

“…Similarly in humans and rodents, glutamate is the most common excitatory neurotransmitter in the zebrafish brain and is involved in neuronal communication across a complex neuronal network with many different functions, including neurodevelopment, movement, and learning (Horzmann and Freeman, 2016). While glutamate is not the main neurotransmitter that comes to mind concerning social behavior, it is important to remember that learning plays a crucial role in the expression of social behavior, and restricting access to social stimuli during early development has been shown to result in abnormal social behavior in adulthood (Shams et al, 2018;Groneberg et al, 2020). Studies by Maaswinkel et al (2013) and Dreosti et al (2015) have shown that administration of MK-801 (an NDMA receptor antagonist) decreased shoaling behavior, an effect that was rescued by administration of the oxytocin agonist, carbetocin (Zimmermann et al, 2016).…”

Section: Future Directionsmentioning

confidence: 99%

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Zebrafish Shoaling, Its Behavioral and Neurobiological Mechanisms, and Its Alteration by Embryonic Alcohol Exposure: A Review

Facciol

2020

Front. Behav. Neurosci.

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Social cognition and social behaviors are complex phenomena that involve numerous brain areas and underlying neurobiological mechanisms. Embryonic alcohol exposure may lead to the development of Fetal Alcohol Spectrum Disorder (FASD), a disorder that manifests with varying symptoms including abnormal social behavior and other cognitive deficits. Animal models have been utilized to mimic aspects of the disease and to study potential underlying mechanisms. The zebrafish is a relative newcomer in this field but has been suggested as an optimal compromise between system complexity and practical simplicity for modeling FASD. Importantly, due to external fertilization and development of the embryo outside the mother and subsequent lack of parental care, this species allows precise control of the timing and dose of alcohol delivery during embryonic development. Furthermore, the zebrafish is a highly social species and thus may be particularly appropriate for the analysis of embryonic alcohol-induced alterations in this context. Here, we provide a succinct review focusing on shoaling, a prominent form of social behavior, in zebrafish. We summarize what is known about its behavioral mechanisms and underlying neurobiological processes, and how it is altered by exposure to ethanol during embryonic development. Lastly, we briefly consider possible future directions of research that would help us better understand the relationship between the behavioral expression and molecular basis of embryonic ethanol-induced social deficits in fish and humans.

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Section: The Development Of Shoaling Behaviormentioning

confidence: 58%

Section: Zebrafish Shoaling Behaviormentioning

confidence: 99%

Section: Future Directionsmentioning

confidence: 99%

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Zebrafish Shoaling, Its Behavioral and Neurobiological Mechanisms, and Its Alteration by Embryonic Alcohol Exposure: A Review

Facciol

2020

Front. Behav. Neurosci.

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“…The ability to perform such socially relevant sensorimotor transformations, and thereby the ability to form groups, differ between different genetic backgrounds [8][9][10][11] and are modified by hunger [12][13][14] and innate "personalities'' of individual fish 15,16,17,18 . Further, while inputs from several sensory modalities, such as lateral line mechanoreception 19,20 , olfaction 21,22 and vision, all likely play a role in this process, vision is critical to certain attributes, such as the rapidity of turning responses, the necessary integration of distal cues, and the precision of the alignment responses 11,23,24 . Mapping out the algorithmic rules and neurophysiology underlying collective behaviors can be more readily accomplished in larval zebrafish when the brain is transparent and circuits are simpler than in adults 25 .…”

Section: Introductionmentioning

confidence: 99%

“…Mapping out the algorithmic rules and neurophysiology underlying collective behaviors can be more readily accomplished in larval zebrafish when the brain is transparent and circuits are simpler than in adults 25 . However, while reflexive responses to stimuli emanating from conspecifics have been described in various contexts 19,20 , there has been no evidence of either shoaling or schooling-like behavior in zebrafish larvae younger than ~20 days post fertilization (dpf) 26,17 .…”

Section: Introductionmentioning

confidence: 99%

Collective behavior emerges from genetically controlled simple behavioral motifs in zebrafish

Aspiras

Harpaz

Chambule

et al. 2021

Preprint

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Coordinated movement of animal groups is essential to species survival. It is not clear whether there are simple interactions among the individuals that account for group behaviors, nor when they arise during development. Zebrafish at the early larval stage do not manifest obvious tendencies to form groups, but we find here that they have already established mechanisms to regulate proximity and alignment with respect to their neighbors, which are the two key ingredients of shoaling and schooling. Specifically, we show that two basic reflexes are sufficient to explain a large part of emerging collective behaviors. First, young larvae repel away from regions of high visual clutter, leading to a dispersal of the group. At later developmental stages, this dispersal reflex shifts to attraction and aggregation behaviors. Second, larvae display a strong tendency to move along with whole field motion stimuli, a well-described behavior known as the optomotor reflex (OMR). When applied to individuals swimming within a group, this reflex leads to an emergence of mutual alignment between close neighbors and induces collective motion of the whole group. The combined developmental maturation of both reflexes can then explain emergent shoaling and schooling behavior. In order to probe the link between single genetic mutations and emergent collective motion, we select fish with mutations in genes orthologous to those associated with human behavioral disorders and find that these mutations affect the primitive visuomotor behaviors at a very young age and persist over development. We then use model simulations to show that the phenotypic manifestations of these mutations are predictive of changes in the emergent collective behaviors of mutant animals. Indeed, models based solely on these two primitive motor reflexes can synergistically account for a large fraction of the distinctive emergent group behaviors across ages and genetic backgrounds. Our results indicate that complex interactions among individuals in a group are built upon genetically defined primitive sensorimotor "motifs", which are evident even in young larvae at a time when the nervous system is far less complex and more directly accessible to detailed analysis.

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Unveiling social distancing mechanisms via a fish-robot hybrid interaction

Romano

Stefanini

2021

Biol Cybern

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Pathogen transmission is a major limit of social species. Social distancing, a behavioural-based response to diseases, has been regularly reported in nature. However, the identification of distinctive stimuli associated with an infectious disease represents a challenging task for host species, whose cognitive mechanisms are still poorly understood. Herein, the social fish Paracheirodon innesi, was selected as model organism to investigate animal abilities in exploiting visual information to identify and promote social distancing towards potentially infected conspecifics. To address this, a robotic fish replica mimicking a healthy P. innesi subject, and another mimicking P. innesi with morphological and/or locomotion anomalies were developed. P. innesi individuals were attracted by the healthy fish replica, while they avoided the fish replica with morphological abnormalities, as well as the fish replica with an intact appearance, but performing locomotion anomalies (both symptoms associated with a microsporidian parasite infesting P. innesi and other fish). Furthermore, the fish replica presenting both morphology and locomotion anomalies in conjunction, triggered a significantly stronger social distancing response. This confirms the hypothesis that group living animals overgeneralize cues that can be related with a disease to minimize transmission, and highlights the important role of visual cues in infection risk contexts. This study prompts more attention on the role of behavioural-based strategies to avoid pathogen/parasite diffusion, and can be used to optimize computational approaches to model disease dynamics.

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Early-Life Social Experience Shapes Social Avoidance Reactions in Larval Zebrafish

Cited by 48 publications

References 87 publications

Zebrafish Shoaling, Its Behavioral and Neurobiological Mechanisms, and Its Alteration by Embryonic Alcohol Exposure: A Review

Zebrafish Shoaling, Its Behavioral and Neurobiological Mechanisms, and Its Alteration by Embryonic Alcohol Exposure: A Review

Collective behavior emerges from genetically controlled simple behavioral motifs in zebrafish

Unveiling social distancing mechanisms via a fish-robot hybrid interaction

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