Early-life social experience shapes social avoidance reactions in larval zebrafish

Abstract

Highlights:• Larval zebrafish raised in isolation show enhanced social avoidance reactions • Enhanced avoidance is composed of increased avoidance distances and usage of high acceleration escape swims• The lateral line sensory organ is necessary and sufficient for the increased usage of high acceleration escape swims Summary Social experiences greatly define successive social behavior. Lack of such experiences, especially during critical phases of development, can severely impede the ability to behave adequately in social contexts. To date it is not well characterized how early-life social isolation leads to social deficits and impacts development. In many model species, it is challenging to fully control social experiences, because they depend on parental care. Moreover, complex social behaviors involve multiple sensory modalities, contexts, and actions. Hence, when studying social isolation effects, it is particularly important to parse apart social deficits from general developmental effects, such as abnormal motor learning. Here, we characterized how social experiences during early development of zebrafish larvae modulate their social behavior, at one week of age, when social avoidance reactions can be measured as discrete swim events. We show that raising larvae in social isolation leads to enhanced social avoidance, in terms of reaction distance and reaction strength. Specifically, larvae raised in isolation use a high-acceleration escape swim bout, the short latency C-start, more frequently during social interactions. These behavioral differences are absent in non-social contexts. By ablating the lateral line and presenting the fish with local water vibrations, we show that lateral line inputs are both necessary and sufficient to drive enhanced social avoidance reactions. Taken together, our results show that social experience during development is a critical factor in shaping mechanosensory avoidance reactions in larval zebrafish.An important aspect of behavior is that it is adaptive and can change according to previous 2 outcomes of the actions of the self or others. During early development, as the nervous sys-3 tem builds and refines its connections, an animal is particularly sensitive to external sensory 4 input, or lack thereof (e.g. reviewed by Andersen [2003]). Social experiences during early 5 development can have long lasting effects on social and other behaviors, as shown by the dev-6

The zebrafish histamine H3 receptor modulates aggression, neural activity and forebrain functional connectivity

“…Interestingly, a similar finding has been made in socially isolated zebrafish larvae. When exposed to a social interaction, these larvae show enhanced social avoidance using high‐acceleration escape swim bouts and a short latency C‐start to escape from the situation, 60 similar to our data. At larval stages, hrh3 expression is strongest in the telencephalon, 25 indicating that this area may mediate the observed phenotypic differences.…”

The Effects of Early Life Stress on the Brain and Behaviour: Insights From Zebrafish Models

“…Larval zebrafish are known to alter their behaviour in response to an acute stressor (De Marco et al, 2013Lopez-Luna et al, 2017;Lee et al, 2019) and following exposure to a physical stimulus (Castillo-Ramírez et al, 2019). Zebrafish larvae display a variety of behaviours that can be quantified (Kalueff et al, 2013;De Marco et al, 2014Groneberg et al, 2015;Karpenko et al, 2020) and exhibit social behaviour (Engeszer et al, 2007;Dreosti et al, 2015;Groneberg et al, 2020), some of which can be modulated by stressor exposure (Eachus et al, 2017;Shen et al, 2020). In the adult zebrafish, a wide variety of behavioural paradigms have been established including tests for anxiety (Egan et al, 2009;Maximino et al, 2010;Stewart et al, 2012), social behaviour (Green et al, 2012;Carreño Gutiérrez et al, 2019), fear (Faustino et al, 2017), and aggression (Oliveira et al, 2011;Carreño Gutiérrez et al, 2018).…”

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

“…In nature, zebrafish aggregate and form social groups, called “shoals.” 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 ; Miller and 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 ).…”

“…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.…”

“…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 ).…”