From behavior to circuit modeling of light-seeking navigation in zebrafish larvae.

Sophia Karpenko,Julie Lafaye,Raphaël Candelier,Guillaume Le Goc,Thomas Panier,Volker Bormuth,Georges Debrégeas,Sebastien Wolf

doi:10.7554/elife.52882

Abstract

Bridging brain-scale circuit dynamics and organism-scale behavior is a central challenge in neuroscience. It requires the concurrent development of minimal behavioral and neural circuit models that can quantitatively capture basic sensorimotor operations. Here, we focus on light-seeking navigation in zebrafish larvae. Using a virtual reality assay, we first characterize how motor and visual stimulation sequences govern the selection of discrete swim-bout events that subserve the fish navigation in the presence of a distant light source. These mechanisms are combined into a comprehensive Markov-chain model of navigation that quantitatively predicts the stationary distribution of the fish's body orientation under any given illumination profile. We then map this behavioral description onto a neuronal model of the ARTR, a small neural circuit involved in the orientation-selection of swim bouts. We demonstrate that this visually-biased decision-making circuit can capture the statistics of both spontaneous and contrast-driven navigation.

Highlights

Animal behaviors are both stereotyped and variable: they are constrained at short time scale to a finite motor repertoire while the long-term sequence of successive motor actions displays apparent stochasticity
As we are mostly interested in the orientational dynamics, we extracted a discrete sequence of orientations an measured just before each swimming event n (Figure 1B–C) from which we computed the bout-induced reorientation angles dan 1⁄4 anþ1 À an
Sensorimotor transformation can be viewed as an operation of massive dimensionality reduction, in which a continuous stream of sensory and motor-related signals is converted into a discrete series of stereotyped motor actions

Summary

Introduction

Animal behaviors are both stereotyped and variable: they are constrained at short time scale to a finite motor repertoire while the long-term sequence of successive motor actions displays apparent stochasticity. This dual characteristic is immediately visible in the locomotion of small animals such as Nematodes (Stephens et al, 2008), Zebrafish (Girdhar et al, 2015) or Drosophila larvae (GomezMarin and Louis, 2012), which consists of just a few stereotyped maneuvers executed in a sequential way. These weak motor-related cues interfere with the innate motor program to cumulatively promote the exploration of regions that are more favorable for the animal (Tsodyks et al, 1999; Fiser et al, 2004)

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