Sexually-Relevant Visual and Chemosensory Signals Induce Distinct Behaviors and Neural Activation Patterns in the Social African Cichlid, Astatotilapia burtoni

Across vertebrates, the use of multimodal (multiple sensory modalities) signals has evolved to convey important information to receivers. Information content of multimodal signals can be the same as or different from information in each unimodal signal, and are classified as redundant or non-redundant, respectively, based on receivers' behavioral responses. Despite the prevalence and importance of multimodal signaling across taxa, relatively little is known about how and where these signals are processed in the brains of receivers. We used the social African cichlid fish, Astatotilapia burtoni, to investigate how sexually-relevant visual and chemosensory uni- and multimodal signals from gravid (full of eggs) females influence behavior, brain activation patterns, and physiology in dominant males. We presented both visual and chemosensory signals either alone or together and found that males need sexually-relevant visual signals to engage in stereotypical courtship behaviors such as body quivers, waggles, and leads into spawning territories. However, the number of courtship behaviors was greater when males were exposed to multimodal visual-chemosensory signals, compared to either unimodal signal alone. When a female visual signal was absent, males increased swimming and overall activity in response to female-conditioned water compared to control water, suggesting that female-released chemosensory signals may stimulate male searching behavior and motivation. Importantly, we also tested anosmic (olfactory ablated) males to demonstrate that this behavior is primarily mediated by the olfactory system rather than gustation. Using the immediate early gene cfos as a proxy for neural activation, we also demonstrate differential activation in social and olfactory-relevant brain regions of dominant males exposed to unimodal and multimodal visual-chemosensory signals. We found at least one region that is preferentially activated by reception of signals from each sense, as well as regions that exhibit an additive effect on activation with multimodal visual-chemosensory stimulation. These data provide insight on how multimodal signals are processed in the brain and integrated with internal physiology of receivers to produce social behaviors, and lay the groundwork for future studies on the evolution of sensory perception.