Deconstructing hunting behavior reveals a tightly coupled stimulus-response loop

Abstract

23Animals build behavioral sequences out of simple stereotyped actions. A comprehensive 24 characterization of these actions and the rules underlying their temporal organization is necessary 25 to understand sensorimotor transformations performed by the brain. Here, we use unsupervised 26 methods to study behavioral sequences in zebrafish larvae. Generating a map of swim bouts, we 27 reveal that fish modulate their tail movements along a continuum. We cluster bouts that share 28 common kinematic features and contribute to similar behavioral sequences into seven modules. 29Behavioral sequences comprising a subset of modules bring prey into the anterior dorsal visual 30 field of the larvae. Fish then release a capture maneuver comprising a stereotyped jaw movement 31 and fine-tuned stereotyped tail movements to capture prey at various distances. We demonstrate 32 that changes to chaining dynamics, but not module production, underlie prey capture deficits in 33 two visually impaired mutants. Our analysis thus reveals the temporal organization of a vertebrate 34 hunting behavior, with the implication that different neural architectures underlie prey pursuit and 35 capture. 36 Patterson et al., 2013;Szigeti et al., 2015). In either case, actions must be chained into sequences 59 that reliably achieve the desired goal of the animal. Stereotyped, reproducible behavioral 60 sequences have been explained with serial models, in which one action triggers the next in the 61 chain via feed-forward neural mechanisms (Long et al., 2010). In contrast, flexible sequences, in 62 which the ordering of modules might be different each time the behavior occurs, have been 63 explained using hierarchical models. In hierarchical models, switching between behavioral 64 modules is stochastic, but may be influenced by longer-term behavioral states or sensory stimuli 65 received by the animal (Berman et al., 2016;Seeds et al., 2014;Tao et al., 2019; Wiltschko et al., 66 2015). 67 68Capturing prey is an essential behavior for the survival of many animals and is innate. The 69 behavior is also complex, requiring the localization, pursuit and capture of a prey object, often 70 encode bouts with similar postural dynamics. In this space, tight clusters would suggest that 131 larvae can only generate a limited number of stereotyped bout types, whereas a diffuse cloud 132 would suggest that larvae can continuously modulate the kinematics of their bouts. To distinguish 133 these possibilities, we developed a pipeline for determining the structure of the behavioral 134 manifold (Figure 2A; see Methods). Our algorithm consists of three steps: alignment, clustering 135 and embedding. In the first step, we calculate the distance between each pair of bouts in the 136 three-dimensional postural space using dynamic time warping (DTW) (Jouary and Sumbre, 2016; 137

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

“…Pursuit bouts are conducted until prey are positioned in a ‘strike zone’, which defines the termination condition for successful hunts in spherical coordinates relative to the fish: this zone is directly in front of, and considerably above the fish (Figure 2B; avg. 0.9° Prey Az, 17.4° Prey Alt, .870 mm Prey Dist; Mearns et al, 2019). We investigated whether displacements and rotations during pursuit bouts were influenced by 3D prey position before each bout.…”

“…The closest prey item in a random environment does not show the same distribution as selected prey in ( A ), indicating that the closest prey does not necessarily have to share the altitude and azimuth features of chosen prey. This suggests that somewhat specific prey features are preferred for entry into the hunting state, although transition probabilities governing hunting mode entry are also at play (Johnson et al, 2019; Mearns et al, 2019). Source data describing prey at hunt initiations.…”

“…The fish’s algorithm for transforming prey altitude biases the prey to ~18° above the fish, which aligns almost perfectly with the mean altitude coordinate at which they strike (17.4°, Figures 2, 3 and 5). The mechanics of the fish jaw necessitate this: to open its jaw widely for paramecium entrance into the mouth, the fish must tilt its head up due to torsional constraints (Mearns et al, 2019). Therefore, the fish’s entire sensation of prey altitude and its method of keeping the prey above it by biasing its bouts downward emerge from the way its jaw co-operates with the rest of its head.…”

Systems Neuroscience of Natural Behaviors in Rodents

“…Here, we echo this sentiment, but also note that ethology and behavioral ecology can in turn be improved by considering systems neuroscience. We will limit our remaining discussion by focusing on rodents, but we want to acknowledge similar efforts for other mammals (Ghazanfar & Hauser, 1999;Ulanovsky & Moss, 2007) , birds (Carr & Peña, 2016;Nottebohm, 2005) , fish (Krahe & Fortune, 2013;Mearns et al, 2019) , and invertebrates (Haberkern et al, 2019;Hamood & Marder, 2014;López-Cruz et al, 2019;Sakurai Akira Katz Paul, 2019) .…”