The Behavioral Space of Zebrafish Locomotion and Its Neural Network Analog

• Published in: PloS one Vol. 10; no. 7; p. e0128668
• Main Authors: Girdhar, Kiran, Gruebele, Martin, Chemla, Yann R.
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 01.07.2015; Public Library of Science (PLoS)
• Subjects: Animals; Behavior; Behavior, Animal; Biology; Biophysics; Cluster analysis; Clustering; Danio rerio; Fish; Fish behavior; Kinematics; Larva; Larvae; Locomotion; Neural networks; Neural Networks (Computer); Neurosciences; Physics; Posture; Scaling; Swimming; Swimming behavior; Trajectories; Vertebrates; Zebrafish; Zebrafish - physiology
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0128668

How simple is the underlying control mechanism for the complex locomotion of vertebrates? We explore this question for the swimming behavior of zebrafish larvae. A parameter-independent method, similar to that used in studies of worms and flies, is applied to analyze swimming movies of fish. The motion itself yields a natural set of fish "eigenshapes" as coordinates, rather than the experimenter imposing a choice of coordinates. Three eigenshape coordinates are sufficient to construct a quantitative "postural space" that captures >96% of the observed zebrafish locomotion. Viewed in postural space, swim bouts are manifested as trajectories consisting of cycles of shapes repeated in succession. To classify behavioral patterns quantitatively and to understand behavioral variations among an ensemble of fish, we construct a "behavioral space" using multi-dimensional scaling (MDS). This method turns each cycle of a trajectory into a single point in behavioral space, and clusters points based on behavioral similarity. Clustering analysis reveals three known behavioral patterns-scoots, turns, rests-but shows that these do not represent discrete states, but rather extremes of a continuum. The behavioral space not only classifies fish by their behavior but also distinguishes fish by age. With the insight into fish behavior from postural space and behavioral space, we construct a two-channel neural network model for fish locomotion, which produces strikingly similar postural space and behavioral space dynamics compared to real zebrafish.