Structure of the Zebrafish Locomotor Repertoire Revealed with Unsupervised Behavioral Clustering

Abstract

An important concept in ethology is that complex behaviors can be constructed from a set of basic motor patterns. Identifying the set of patterns available to an animal is key to making quantitative descriptions of behavior that reflect the underlying motor system organization. We addressed these questions in zebrafish larvae, which swim in bouts that are naturally segmented in time. We developed a robust and general purpose clustering method (clusterdv) to ensure accurate identification of movement clusters and applied it to a dataset consisting of millions of swim bouts, captured at high temporal resolution from a comprehensive set of behavioral contexts. We identified a set of thirteen basic swimming patterns that are used flexibly in various combinations across different behavioral contexts and show that this classification can be used to dissect the sensorimotor transformations underlying larval social behavior and hunting. Furthermore, using the same approach at different levels in the behavioral hierarchy, we show that the set of swim bouts are themselves constructed from a basic set of tail movements and that bouts are executed in sequences specific to different behaviors.

Learning steers the ontogeny of an efficient hunting sequence in zebrafish larvae

“…At the final stage of the hunting sequence zebrafish larvae execute a capture manoeuvre, see Figure S15 . These capture manoeuvres vary in apparent vigour and distance to the prey from which they are initiated, and can be divided into at least two types based on tail posture and swim speed classification [31,34,43]. We therefore explored whether experience modifies capture strategy and whether this associates with the increased hunting performance of the LF group.…”

“…Overall our findings demonstrate that the frequency of fast capture swims, the distance-to-prey at capture initiation, and the speed-distance correlation increase as a result of rearing with live prey. For successful capture, the timing of mouth opening needs to be synchronized in relation to prey proximity such that prey enters the mouth cavity either via suction or engulfment [12,16,24,31]. One way of achieving precision in this timing would be to maintain a consistent distance to prey from where to execute capture swims [12].…”

“…The larval zebrafish is an ideal vertebrate model for the detailed study of behaviour and its associated circuits. They have a diverse behavioural repertoire that can be precisely measured [31,41], and neural activity can be recorded non-invasively and at single-neuron resolution throughout the whole brain [1,29,40,45,57]. Larval hunting appears as a distinct behavioural mode that is composed of several component actions chained together into a sequence [9,33,51].…”

Elements of a stochastic 3D prediction engine in larval zebrafish prey capture

“…Prey capture requires the fish to select, pursue, and ultimately consume fast moving singlecelled organisms swimming through their environment. Elegant work has been performed in documenting the types of body movements the fish use during prey capture and in the characterization of neurons responsible for prey perception (Johnson et al 2019, Marques et al 2018, Gahtan et al 2005, Bianco and Engert 2015, Muto et al 2013. Furthermore, foundational studies have led to an initial understanding of how fish choose their movements based on prey contingencies (Patterson et al 2013, Trivedi and Bollmann 2013, Bianco et al 2011.…”

Whole-organism behavioral profiling reveals a role for dopamine in state-dependent motor program coupling inC. elegans

“…Unsupervised learning can reveal the underlying states that generate observed behavioral variables (Berman et al, 2014;Marques et al, 2018;Wiltschko et al, 2015).…”