Visually driven chaining of elementary swim patterns into a goal-directed motor sequence: a virtual reality study of zebrafish prey capture

Abstract

Prey capture behavior critically depends on rapid processing of sensory input in order to track, approach, and catch the target. When using vision, the nervous system faces the problem of extracting relevant information from a continuous stream of input in order to detect and categorize visible objects as potential prey and to select appropriate motor patterns for approach. For prey capture, many vertebrates exhibit intermittent locomotion, in which discrete motor patterns are chained into a sequence, interrupted by short periods of rest. Here, using high-speed recordings of full-length prey capture sequences performed by freely swimming zebrafish larvae in the presence of a single paramecium, we provide a detailed kinematic analysis of first and subsequent swim bouts during prey capture. Using Fourier analysis, we show that individual swim bouts represent an elementary motor pattern. Changes in orientation are directed toward the target on a graded scale and are implemented by an asymmetric tail bend component superimposed on this basic motor pattern. To further investigate the role of visual feedback on the efficiency and speed of this complex behavior, we developed a closed-loop virtual reality setup in which minimally restrained larvae recapitulated interconnected swim patterns closely resembling those observed during prey capture in freely moving fish. Systematic variation of stimulus properties showed that prey capture is initiated within a narrow range of stimulus size and velocity. Furthermore, variations in the delay and location of swim triggered visual feedback showed that the reaction time of secondary and later swims is shorter for stimuli that appear within a narrow spatio-temporal window following a swim. This suggests that the larva may generate an expectation of stimulus position, which enables accelerated motor sequencing if the expectation is met by appropriate visual feedback.

Differences in the morphology of spinal V2a neurons reflect their recruitment order during swimming in larval zebrafish

“…Thus, for ventral cells, a lower interneuron to motoneuron ratio could provide finer control of segmental musculature. This is consistent with the slower, more precise movements observed during visually guided prey capture movements in larval zebrafish (Patterson et al, ; Trivedi and Bollmann, ). For faster movements, such as escape maneuvers (Liu and Fetcho, ), the coarse control provided by higher premotor convergence to fewer, larger motoneurons may be more appropriate.…”

A high-throughput assay for quantifying appetite and digestive dynamics

“…At that age the larval yolk sac is depleted, and they start to depend on external food sources (13). One of their natural feeds are live paramecia, a unicellular protozoan, which they hunt with characteristic kinematic behaviors (5,11,39). Whether these complex prey capture maneuvers are simply triggered by a moving prey or actively regulated by a nutrient homeostatic state (i.e., hunger and satiation) is unknown.…”

Underwater Mixed Environments

“…2). Similar work can be found studying the larval zebra fish prey capture [64]. Immersive VR setup for studying fish behavior [13] A more elaborated underwater virtual environment, the Sub Sea Holodeck, uses seven displays with 14 megapixels to produce a high resolution visual aquatic environment [37] (see Fig.…”