Mechanisms of social buffering of fear in zebrafish

Abstract

Some humans thrive whereas others resign when exposed to threatening situations throughout life. Social support has been identified as an important modulator of these discrepancies in human behaviour, and other social animals also exhibit phenomena in which individuals recover better from aversive events when conspecifics are present – aka social buffering. Here we studied social buffering in zebrafish, by exposing focal fish to an aversive stimulus (alarm substance – AS) either in the absence or presence of conspecific cues. When exposed to AS in the presence of both olfactory (shoal water) and visual (sight of shoal) conspecific cues, focal fish exhibited a lower fear response than when tested alone, demonstrating social buffering in zebrafish. When separately testing each cue’s effectiveness, we verified that the visual cue was more effective than the olfactory in reducing freezing in a persistent threat scenario. Finally, we verified that social buffering was independent of shoal size and coincided with a distinct pattern of co-activation of brain regions known to be involved in mammalian social buffering. Thus, this study suggests a shared evolutionary origin for social buffering in vertebrates, bringing new evidence on the behavioural, sensory and neural mechanisms underlying this phenomenon.

Social information use in threat perception: Social buffering, contagion and facilitation of alarm responses

“…After showing that zebrafish decreased their fear response to alarm substance (AS, a known fear-inducing stimulus in this species) when in the joint presence of olfactory (shoal water) and visual (sight of shoal) cues of conspecifics, we exposed zebrafish to AS in the presence of olfactory or visual social cues separately. Our results showed that although both sensory modalities were equally effective in the short term, the visual cue was more effective in decreasing fear responses toward AS in a long-lasting exposure 8 . These differences may reflect the fact that olfactory and visual cues are refreshed at different rates in the environment, with olfactory information remaining invariable in the water for longer periods of time, hence limiting the rate at which it can be updated 8 .…”

“…In our study we investigated the mechanisms of social buffering of fear in zebrafish ( Danio rerio ) 8 . First, we assessed the influence of different sensory modalities to the same buffering episode and respective effectiveness in a long-lasting exposure to threat.…”

“…Secondly, we characterized the changes in brain activity associated with social buffering in zebrafish, using the transient expression of an immediate early gene ( c-fos ) as a marker of neuronal activity. We have shown that a set of brain nuclei that are putative homologues to those involved in social buffering in mammals were also active during social buffering in zebrafish, namely the medial part of the dorsal telencephalon (Dm, homolog of the mammalian pallial amygdala), the ventral nucleus of the ventral telencephalon (Vv, homolog of the mammalian nucleus accumbens and septum), and the preoptic area (POA, homolog of the mammalian preoptic area/paraventricular nucleus) 8 . In sum, our work indicates that multimodal social cues mediate social buffering in zebrafish and that these are integrated and processed in homologous brains areas to those previously identified in mammals to ameliorate the response to threat.…”

Sensory ecology of ostariophysan alarm substances

“…On the other hand, CAS was not able to increase antipredator responses to a sympatric predator (although the predator was not in the same tank as the receiver) in D. rerio (Speedie & Gerlai, ), although CAS increased survival of P. promelas placed in an experimental tank with a predator (Mathis & Smith, ). Moreover, D. rerio given visual and olfactory access to conspecifics show less freezing when exposed to CAS (Faustino et al ., ), an effect that has been termed social buffering. This observation, as well as the fact that D. rerio tested in groups are less likely to freeze, suggest that conspecific communication is the main function of CAS.…”

The Aversive Brain System of Teleosts: Implications for Neuroscience and Biological Psychiatry

“…Interestingly, as reported above, this work also found increased cfos in the Dm, Vv, and 188 POA. Importantly, control animals showed functional connectivity between these regions, while 189 exposure to CAS decreased these correlations; in fact, animals exposed to CAS showed only co-190 activation of Dm-Vs and Vv-Vs (Faustino et al, 2017). The precise mechanism for this decreased 191…”