Cognitive ethology of nest building in a shell-dwelling cichlid

Abstract

Across animal taxa, nest-building behavior is performed using a generalizable and flexible mental representation of an action sequence - a schema. In order to accomplish its goal (a stable nest), the brain appears to compare intermediate steps in the process to stored mental images, or templates. Deviations from these templates drive progress, preferences, and corrections in the execution of this behavior. The stereotypy vs. plasticity of both schema and mental templates have rarely been defined in an experimentally accessible system. Here we investigated nest building by the cichlid Lamprologus ocellatus, a fish species that manipulates abandoned snail shells to build shelters for breeding and protection. We find that nest building is composed of a sequence of behaviors that are tied together by a series of stimulus-response loops, allowing for restarts and shortcuts as the behavioral program unfolds. The attraction to a shell object is innate, as is the final appearance of the nest. The behavior in an inexperienced animal is initially uncoordinated, but is fine-tuned by repeated building opportunities. Shells need to conform to rigid geometric criteria in order to be acceptable as a potential home. Nest building is accompanied by focused neural activity in brain regions homologous to the mammalian hippocampus and neocortex. In conclusion, we have uncovered the constraints and flexibility of cognitive template matching underlying an instinctive, goal-directed behavior.