Abstract
The zebrafish larva stands out as an emergent model organism for translational studies involving gene or drug screening thanks to its size, genetics, and permeability. At the larval stage, locomotion occurs in short episodes punctuated by periods of rest. Although phenotyping behavior is a key component of large-scale screens, it has not yet been automated in this model system. We developed ZebraZoom, a program to automatically track larvae and identify maneuvers for many animals performing discrete movements. Our program detects each episodic movement and extracts large-scale statistics on motor patterns to produce a quantification of the locomotor repertoire. We used ZebraZoom to identify motor defects induced by a glycinergic receptor antagonist. The analysis of the blind mutant atoh7 revealed small locomotor defects associated with the mutation. Using multiclass supervised machine learning, ZebraZoom categorized all episodes of movement for each larva into one of three possible maneuvers: slow forward swim, routine turn, and escape. ZebraZoom reached 91% accuracy for categorization of stereotypical maneuvers that four independent experimenters unanimously identified. For all maneuvers in the data set, ZebraZoom agreed with four experimenters in 73.2–82.5% of cases. We modeled the series of maneuvers performed by larvae as Markov chains and observed that larvae often repeated the same maneuvers within a group. When analyzing subsequent maneuvers performed by different larvae, we found that larva–larva interactions occurred as series of escapes. Overall, ZebraZoom reached the level of precision found in manual analysis but accomplished tasks in a high-throughput format necessary for large screens.
Highlights
Locomotor events were segregated subjectively in the training set (n = 201). This machine learning approach relied on associating dynamic parameters extracted from the tail-bending angle over time with each maneuver type identified in the training set (Figure 4A and Methods)
Compared to other genetic models, zebrafish locomotion is difficult to analyze because larvae initiate maneuvers intermittently and during these short events, the larvae swim at a high speed with tail-beat frequency (TBF) ranging from 15–100 Hz
The approach we developed here could be expanded to include directionality of the turns, sequences of maneuvers such as those occurring during prey tracking, and subcategories of escapes
Summary
We developed ZebraZoom, a program to automatically track larvae and identify maneuvers for many animals performing discrete movements. Using multiclass supervised machine learning, ZebraZoom categorized all episodes of movement for each larva into one of three possible maneuvers: slow forward swim, routine turn, and escape.
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