Differences in neural activity, but not behavior, across social contexts in guppies, Poecilia reticulata

Abstract

Animals are continually faced with the challenge of producing context-appropriate social behaviors. In many instances, appropriate behaviors differ by social situation. However, in some instances, the same behaviors are employed across different social contexts, albeit in response to distinct stimuli and with distinct purposes. We took advantage of behavioral similarities across mating and aggression contexts in guppies, Poecilia reticulata, to understand how patterns of neural activity differ across social contexts when behaviors are nonetheless shared. While there is growing interest in understanding behavioral mechanisms in guppies, resources are sparse. As part of this study, we developed a neuroanatomical atlas of the guppy brain as a research community resource. Using this atlas, we found that neural activity in the preoptic area reflected social context, whereas individual differences in behavioral motivation paralleled activity in the posterior tuberculum and ventral telencephalon (teleost homologs of the mammalian ventral tegmental area and lateral septum, respectively). Our findings suggest independent coding of social salience versus behavioral motivation when behavioral repertoires are shared across social contexts.

Significance statement

Choosing behaviors appropriate to the current social situation is of central importance to animals. Interactions with different social partners (e.g., mates, competitors, or offspring) generally require distinct behavioral repertories. However, in some cases, similar behaviors are used across social contexts. The neural mechanisms underlying social behavior are particularly intriguing in these situations, where the same behaviors are produced in response to distinct social stimuli and for distinct purposes. We took advantage of behavioral similarities across mating and aggression interactions in Trinidadian guppies to explore how social information is reflected in the brain when fish perform a common set of behaviors across contexts. We found that activity in distinct brain regions reflects social context versus behavioral motivation, suggesting a means by which social inputs and behavioral outputs can be coded independently of one another.