Alarm cues and alarmed conspecifics: neural activity during social learning from different cues in Trinidadian guppies

Abstract

Learning to respond appropriately to novel dangers is often essential to survival and success, but carries risks. Learning about novel threats from others (social learning) can reduce these risks. Many species, including the Trinidadian guppy ( Poecilia reticulata ), respond defensively to both conspecific chemical alarm cues and conspecific anti-predator behaviours, and in other fish such social information can lead to a learned aversion to novel threats. However, relatively little is known about the neural substrates underlying social learning and the degree to which different forms of learning share similar neural mechanisms. Here, we explored the neural substrates mediating social learning of novel threats from two different conspecific cues (i.e. social cue-based threat learning). We first demonstrated that guppies rapidly learn about threats paired with either alarm cues or with conspecific threat responses (demonstration). Then, focusing on acquisition rather than recall, we discovered that phospho-S6 expression, a marker of neural activity, was elevated in guppies during learning from alarm cues in the putative homologue of the mammalian lateral septum and the preoptic area. Surprisingly, these changes in neural activity were not observed in fish learning from conspecific demonstration. Together, these results implicate forebrain areas in social learning about threat but raise the possibility that circuits contribute to such learning in a stimulus-specific manner.

Quantifying the Neural and Behavioral Correlates of Repeated Social Competition in the Fighting Fish Betta splendens

“…These neural mechanisms are incredibly conserved across a diverse set of taxa [26,29]. There are a growing number of studies on the neural mechanisms of cognition and social behavior in other fish species [30][31][32][33]. But, to our knowledge, the current study is the first to investigate brain regions within the Social Decision-Making Network in Betta splendens.…”

“…Labeling PS6 identifies ribosomal proteins that have been phosphorylated in roughly the previous hour, thus corresponding to an increase in translation [51,52]. Previous studies in other fish species have immunohistochemically labeled for PS6 to assess neural responses [31,32,53,54]. Following euthanasia, the whole head tissue was stored in 4% paraformaldehyde for four hours.…”

Insights into adaptive behavioural plasticity from the guppy model system

“…Individually, guppies can solve and learn mazes [28], learn preferences for familiar individuals [32] and learn to numerically discriminate [27]. Socially, guppies readily learn from others about foraging sites and predation threats [30,31,33]. When exploring a novel environment, plasticity in shoaling behaviour may allow guppies to group with heterospecifics, potentially providing anti-predator and foraging benefits [34].…”

“…In guppies, the forebrain is implicated in learning responses to environmental changes, but the forebrain regions involved can be differentially activated depending on cue type (e.g. [33]). We suggest that guppy populations that differ in environmental conditions can be tested for differences in activity across brain regions and neural systems and levels of behavioural plasticity.…”