Learning steers the ontogeny of an efficient hunting sequence in zebrafish larvae

Abstract

The success of goal-directed behaviours relies on the coordinated execution of a sequence of component actions. In young animals, such sequences may be poorly coordinated, but with age and experience, behaviour progressively adapts to efficiently exploit the animal's ecological niche. How experience impinges on the developing neural circuits of behaviour is an open question. As a model system, larval zebrafish (Danio rerio) hold enormous potential for studying both the development of behaviour and the underlying circuits, but no relevant experience-dependent learning paradigm has yet been characterized. To address this, we have conducted a detailed study of the effects of experience on the ontogeny of hunting behaviour in larval zebrafish. We report that larvae with prior prey experience consume considerably more prey than naive larvae. This is mainly due to increased capture success that is also accompanied by a modest increase in hunt rate. We identified two components of the hunting sequence that are jointly modified by experience. At the onset of the hunting sequence, the orientation strategy of the turn towards prey is modified such that experienced larvae undershoot prey azimuth. Near the end of the hunt sequence, we find that experienced larvae are more likely to employ high-speed capture swims initiated from longer distances to prey. Combined, these modified turn and capture manoeuvrers can be used to predict the probability of capture success and suggest that their development provides advantages specific to larvae feeding on live-prey. Our findings establish an ethologically relevant paradigm in zebrafish for studying how the brain is shaped by experience to drive the ontogeny of efficient behaviour.

Experience, circuit dynamics, and forebrain recruitment in larval zebrafish prey capture

“…Thus, experience of live prey may contribute to the ontogeny of prey capture behavior, where older (and therefore more "experienced") fish have more fluid capture maneuvers and hunt prey from a wider angular range [51]. Our finding is consistent with a recent study [52], which showed that differences in hunting kinematics result in higher hunting efficiency in experienced fish.…”

“…Thus, the prey-capture circuit is hard-wired in the novice hunter's brain. Nonetheless, experience of live prey may shape the circuit as shown in this work and the work mentioned above [52], and as it appears to do in juvenile fish raised in the dark who learn to forage using their lateral line system [56].…”