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

Claire S Oldfield,Irene Grossrubatscher,Ehud Y Isacoff,Alex R Huth,Claire Wyart,Jack L Gallant,Elizabeth C Carroll,Adam Hoagland,Mario Chávez,Andrew Prendergast,Tony Qu

doi:10.7554/elife.56619

Abstract

Experience influences behavior, but little is known about how experience is encoded in the brain, and how changes in neural activity are implemented at a network level to improve performance. Here we investigate how differences in experience impact brain circuitry and behavior in larval zebrafish prey capture. We find that experience of live prey compared to inert food increases capture success by boosting capture initiation. In response to live prey, animals with and without prior experience of live prey show activity in visual areas (pretectum and optic tectum) and motor areas (cerebellum and hindbrain), with similar visual area retinotopic maps of prey position. However, prey-experienced animals more readily initiate capture in response to visual area activity and have greater visually-evoked activity in two forebrain areas: the telencephalon and habenula. Consequently, disruption of habenular neurons reduces capture performance in prey-experienced fish. Together, our results suggest that experience of prey strengthens prey-associated visual drive to the forebrain, and that this lowers the threshold for prey-associated visual activity to trigger activity in motor areas, thereby improving capture performance.

Highlights

To transform sensory input into an optimal behavioral response, animals must extract relevant perceptual information from their environment, interpret it within their internal and external contexts, and translate it into a motor output
At day seven prey capture behavior was tested in both groups by quantifying behavioral steps of the prey capture sequence: (a) pursuits that are aborted before a capture swim is attempted, (b) capture swim attempts that fail, and (c) successful captures (Figure 1A bottom and Figure 1—video 1)
We compared hunting of paramecia between zebrafish larvae with two days of experience of live prey and sibling fish with experience of inert dry food, which are exposed to paramecia for the first time

Summary

Introduction

To transform sensory input into an optimal behavioral response, animals must extract relevant perceptual information from their environment, interpret it within their internal and external contexts, and translate it into a motor output. Prior experience modulates how this transformation occurs and whether the response is successful. A large body of work has studied how enriching or depriving sensory experience affects perceptual encoding, with both morphological and molecular changes (Feldman, 2009). Teaching an animal to fear or expect a stimulus alters properties of the circuits recruited in response to the cue (e.g., Letzkus et al, 2011; Matsumoto and Hikosaka, 2009). Most studies of experience-dependent changes rely on drastic manipulation such as depriving animals of all sensory input in one modality, inducing fear association with a noxious stimulus, or depriving animals of food or water to achieve sufficient motivation to assure a response. Neurons respond differently to ethologically-relevant stimuli (Felsen and Dan, 2005; Theunissen and Elie, 2014), and the question of how natural experience influences brain activity and downstream native behavior (Sommerfeld and Holzman, 2019) is becoming increasingly relevant

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