Probabilistic Models of Larval Zebrafish Behavior Reveal Structure on Many Scales

Johnson, Robert E.; Linderman, Scott W.; Panier, Thomas; Wee, Caroline Lei; Song, Erin; Herrera, Kristian J.; Miller, Andrew T.; Engert, Florian

doi:10.1016/j.cub.2019.11.026

Cited by 107 publications

(109 citation statements)

References 80 publications

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“…An advantage of using one-week-old zebrafish is that the repertoire of their swims has been described and can be clustered into movement types through automatic, unsupervised methods [Marques et al, 2018, Johnson et al, 2020, Mearns et al, 2020], enabling exact phenotyping of behavioral events. Using this technology, we found that larvae avoid each other by executing four types of large displacement bouts: burst swims [Severi et al, 2014], long capture swims [Marques et al, 2018], O-bends [Burgess and Granato, 2007b], and C-starts (LLCs and SLCs) [Burgess and Granato, 2007a].…”

Section: Discussionmentioning

confidence: 99%

“…Second, larvae are small and transparent enough to enable whole brain imaging with single neuron resolution in behaving animals [Feierstein et al, 2015], including freely moving fish [Kim et al, 2017, Marques et al, 2020, Cong et al, 2017], an ideal situation where animals can interact with each other. Finally, larval zebrafish organize their behaviors, including social interactions, in sequences of discrete bouts [Budick and O’Malley, 2000, Fero et al, 2011], which can be detected automatically and classified into types [Mirat et al, 2013, Marques et al, 2018, Mearns et al, 2020, Johnson et al, 2020], enabling precise behavioral phenotyping.…”

Section: Introductionmentioning

confidence: 99%

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Early-life social experience shapes social avoidance reactions in larval zebrafish

Groneberg

Marques

Martins

et al. 2020

Preprint

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Highlights:• Larval zebrafish raised in isolation show enhanced social avoidance reactions • Enhanced avoidance is composed of increased avoidance distances and usage of high acceleration escape swims• The lateral line sensory organ is necessary and sufficient for the increased usage of high acceleration escape swims Summary Social experiences greatly define successive social behavior. Lack of such experiences, especially during critical phases of development, can severely impede the ability to behave adequately in social contexts. To date it is not well characterized how early-life social isolation leads to social deficits and impacts development. In many model species, it is challenging to fully control social experiences, because they depend on parental care. Moreover, complex social behaviors involve multiple sensory modalities, contexts, and actions. Hence, when studying social isolation effects, it is particularly important to parse apart social deficits from general developmental effects, such as abnormal motor learning. Here, we characterized how social experiences during early development of zebrafish larvae modulate their social behavior, at one week of age, when social avoidance reactions can be measured as discrete swim events. We show that raising larvae in social isolation leads to enhanced social avoidance, in terms of reaction distance and reaction strength. Specifically, larvae raised in isolation use a high-acceleration escape swim bout, the short latency C-start, more frequently during social interactions. These behavioral differences are absent in non-social contexts. By ablating the lateral line and presenting the fish with local water vibrations, we show that lateral line inputs are both necessary and sufficient to drive enhanced social avoidance reactions. Taken together, our results show that social experience during development is a critical factor in shaping mechanosensory avoidance reactions in larval zebrafish.An important aspect of behavior is that it is adaptive and can change according to previous 2 outcomes of the actions of the self or others. During early development, as the nervous sys-3 tem builds and refines its connections, an animal is particularly sensitive to external sensory 4 input, or lack thereof (e.g. reviewed by Andersen [2003]). Social experiences during early 5 development can have long lasting effects on social and other behaviors, as shown by the dev-6

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Early-life social experience shapes social avoidance reactions in larval zebrafish

Groneberg

Marques

Martins

et al. 2020

Preprint

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“…Second, affecting complex behavioral states such as aggression, addiction, social behavior, or learning may improve resolution. We used a trivial readout for potentially high-dimensional movement behaviors, but tracking, 48 optic flow, 40 probabilistic models, 17 and deep learning 15 have been successful in analyzing similar data. Future studies will likely leverage advances in all these areas to improve the resolution of zebrafish behavioral profiling assays.…”

Section: Discussionmentioning

confidence: 99%

Simultaneous analysis of neuroactive compounds in zebrafish

Myers-Turnbull

Taylor

Helsell

et al. 2020

Preprint

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Purpose: Compounds that act on the central nervous system (CNS) are crucial tools in drug discovery and neuroscience. To discover compounds with novel mechanisms of action, researchers have developed behavioral screens in larval zebrafish including various methods to identify and classify hit compounds. However, these methods typically do not admit intuitive numerical scores of screen performance. This study describes methods to classify compounds simultaneously in zebrafish and quantify screen performance.Methods: We collected randomized, highly replicated data for two sets of compounds: 16 quality-control (QC) compounds and a reference set of 648 known CNS ligands. Machine learning models were trained to discriminate between compound-induced phenotypes, compare performance between protocols, and detect hit compounds.Results: Classification accuracy on the QC set was 94.3%. In addition, 106 of 648 CNS ligands were identified as phenotypically active, and hits were enriched for dopaminergic and serotonergic targets. The raw data is included to facilitate replication and data mining.Significance: This study describes methods to evaluate behavioral phenotyping assays, which can be used to facilitate comparison and standardization of data within the zebrafish phenotyping community.

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“…Motifs correspond to recurring sequences of elementary locomotor episodes of arbitrary length. A well-established motif for larval zebrafish corresponds to the sequence of locomotor episodes consisting of a J-turn followed by pursuit and capture swims deployed for hunting prey [17,25,26]. BASS considers sequences rather than individual locomotor episodes and has the following advantages: 1) BASS does not need to know the sensory information perceived by the animal, 2) BASS captures extended responses that last much longer than a typical locomotor episode, 3) BASS identifies conserved sequences despite them rarely occurring in the behavioral recording.…”

Section: Introductionmentioning

confidence: 99%

“…In order to survive, five days old zebrafish larvae actively explore their environment avoiding toxic cues and searching for food using stereotypical locomotor episodes consisting of bouts of activity lasting few hundreds of milliseconds separated by distinct pauses [16,17,25,33].…”

Section: Introductionmentioning

confidence: 99%

A lexical approach for identifying behavioral action sequences

Reddy¹,

Desban

Tanaka

et al. 2020

Preprint

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Animals display characteristic behavioral patterns when performing a task, such as the spiraling of a soaring bird or the surge-and-cast of a male moth searching for a female. Identifying such conserved patterns occurring rarely in noisy behavioral data is key to understanding the behavioral response to a distributed stimulus in unrestrained animals. Existing models seek to describe the dynamics of behavior or segment individual locomotor episodes rather than to identify occasional, transient irregularities that make up the behavioral response. To fill this gap, we develop a lexical, hierarchical model of behavior. We designed an unsupervised algorithm called “BASS” to efficiently identify and segment conserved behavioral action sequences transiently occurring in long behavioral recordings. When applied to navigating larval zebrafish, BASS extracts a dictionary of remarkably long, non-Markovian sequences consisting of repeats and mixtures of slow forward and turn bouts. Applied to a novel chemotaxis assay, BASS uncovers conserved chemotactic strategies deployed by zebrafish to avoid aversive cues consisting of sequences of fast large-angle turns and burst swims. In a simulated dataset of soaring gliders climbing thermals, BASS finds the spiralling patterns characteristic of soaring behavior. In both cases, BASS succeeds in identifying action sequences that are highly conserved but transient in the behavior deployed by freely moving animals. BASS can be easily incorporated into the pipelines of existing behavioral analyses across diverse species, and even more broadly used as a generic algorithm for pattern recognition in low-dimensional sequential data.

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Probabilistic Models of Larval Zebrafish Behavior Reveal Structure on Many Scales

Cited by 107 publications

References 80 publications

Early-life social experience shapes social avoidance reactions in larval zebrafish

Early-life social experience shapes social avoidance reactions in larval zebrafish

Simultaneous analysis of neuroactive compounds in zebrafish

A lexical approach for identifying behavioral action sequences

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