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

Author:

Oldfield Claire S1,Grossrubatscher Irene1ORCID,Chávez Mario2,Hoagland Adam3,Huth Alex R1,Carroll Elizabeth C3,Prendergast Andrew245,Qu Tony3,Gallant Jack L16ORCID,Wyart Claire245ORCID,Isacoff Ehud Y137ORCID

Affiliation:

1. Helen Wills Neuroscience Institute and Graduate Program, University of California Berkeley, Berkeley, United States

2. CNRS-UMR, Paris, France

3. Department of Molecular and Cell Biology, University of California Berkeley, Berkeley, United States

4. INSERM UMRS, Paris, France

5. Institut du Cerveau et de la Moelle épinière (ICM), Hôpital de la Pitié-Salpêtrière, Paris, France

6. Department of Psychology, University of California, Berkeley, Berkeley, United States

7. Bioscience Division, Lawrence Berkeley National Laboratory, Berkeley, United States

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.

Funder

Defense Advanced Research Projects Agency

National Institutes of Health

ERC

EMBO

Boehringer Ingelheim Fonds

Embassy of France

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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