Experience, circuit dynamics and forebrain recruitment in larval zebrafish prey capture
- University of California, Berkeley, United States
- CNRS-UMR-7225, France
- Hôpital Pitié-Salpêtrière, Sorbonne Universités, UPMC Univ Paris 06, Inserm, CNRS, France
- Institut du Cerveau et la Moelle épinière, Hôpital Pitié-Salpêtrière, Sorbonne Universités, UPMC Univ Paris 06, Inserm, CNRS, France
Abstract
Experience strongly 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. To explore the underlying neural basis, we studied the effects of prior experience of live prey on behavior and brain activity. In response to live prey, animals with and without prior experience of live prey all 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 also have greater visually-evoked activity in two forebrain areas: the telencephalon and the habenula. Consistent with the contribution of the forebrain to prey capture, disruption of neurons in the habenula reduced prey 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.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for all figures.
Article and author information
Author details
Funding
Defense Advanced Research Projects Agency (N66001-17-C-4015)
- Ehud Y Isacoff
National Institutes of Health (2PN2EY018241)
- Ehud Y Isacoff
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee (ACUC) of the University of California, Berkeley.protocol ID: UP-2015-06-7705-1, last approval date 11/20/2019).
Reviewing Editor
- Yuichi Iino, University of Tokyo, Japan
Publication history
- Received: March 4, 2020
- Accepted: September 26, 2020
- Accepted Manuscript published: September 28, 2020 (version 1)
- Version of Record published: October 15, 2020 (version 2)
- Version of Record updated: October 20, 2020 (version 3)
Copyright
© 2020, Oldfield et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 2,668
- Page views
-
- 377
- Downloads
-
- 8
- Citations
Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Experience, circuit dynamics and forebrain recruitment in larval zebrafish prey capture
eLife 9:e56619.
https://doi.org/10.7554/eLife.56619
Further reading
-
- Neuroscience
The adult human visual system maintains the ability to be altered by sensory deprivation. What has not been considered is whether the internal neural states modulate visual sensitivity to short-term monocular deprivation. In this study we manipulated the internal neural state and reported changes in intrinsic neural oscillations with a patched eye open or closed. We investigated the influence of eye open/eye closure on the unpatched eye's contrast sensitivity and ocular dominance (OD) shifts induced by short-term monocular deprivation. The results demonstrate that internal neural states influence not only baseline contrast sensitivity but also the extent to which the adult visual system can undergo changes in ocular dominance.
-
- Neuroscience
- Physics of Living Systems
Naturally occurring body movements and collective neural activity both exhibit complex dynamics, often with scale-free, fractal spatiotemporal structure. Scale-free dynamics of both brain and behavior are important because each is associated with functional benefits to the organism. Despite their similarities, scale-free brain activity and scale-free behavior have been studied separately, without a unified explanation. Here we show that scale-free dynamics of mouse behavior and neurons in visual cortex are strongly related. Surprisingly, the scale-free neural activity is limited to specific subsets of neurons, and these scale-free subsets exhibit stochastic winner-take-all competition with other neural subsets. This observation is inconsistent with prevailing theories of scale-free dynamics in neural systems, which stem from the criticality hypothesis. We develop a computational model which incorporates known cell-type-specific circuit structure, explaining our findings with a new type of critical dynamics. Our results establish neural underpinnings of scale-free behavior and clear behavioral relevance of scale-free neural activity.
