Zebrafish Adjust Their Behavior in Response to an Interactive Robotic Predator

Abstract

Zebrafish (Danio rerio) constitutes a valuable experimental species for the study of the biological determinants of emotional responses, such as fear and anxiety. Fear-related test paradigms traditionally entail the interaction between focal subjects and live predators, which may show inconsistent behavior throughout the experiment. To address this technical challenge, robotic stimuli are now frequently integrated in behavioral studies, yielding repeatable, customizable, and controllable experimental conditions. While most of the research has focused on open-loop control where robotic stimuli are preprogrammed to execute a priori known actions, recent work has explored the possibility of two-way interactions between robotic stimuli and live subjects. Here, we demonstrate a "closed-loop control" system to investigate fear response of zebrafish in which the response of the robotic stimulus is determined in real-time through a finite-state Markov chain constructed from independent observations on the interactions between zebrafish and their predator. Specifically, we designed a 3D-printed robotic replica of the zebrafish allopatric predator red tiger Oscar fish (Astronotus ocellatus), instrumented to interact in real-time with live subjects. We investigated the role of closed-loop control in modulating fear response in zebrafish through the analysis of the focal fish ethogram and the information-theoretic quantification of the interaction between the subject and the replica. Our results indicate that closed-loop control elicits consistent fear response in zebrafish and that zebrafish quickly adjust their behavior to avoid the predator's attacks. The augmented degree of interactivity afforded by the Markov-chain-dependent actuation of the replica constitutes a fundamental advancement in the study of animal-robot interactions and offers a new means for the development of experimental paradigms to study fear.

Simulating more realistic predation threat using attack playbacks

“…We attempted to design visual predator cues that are as similar to an actual encounter as possible. While robotic models have been shown to hold potential (Krause, Winfield & Deneubourg, 2011; Ladu et al, 2015; Landgraf et al, 2016; Porfiri et al, 2019), they may not always be easily accessible. We propose a technically simple method of simulating a predator attack, which can be produced with ease and in a short time.…”

Decoding collective communications using information theory tools

“…To determine whether one random variable is actually influenced by another, rather than merely correlated with it, one can instead use an IT metric called transfer entropy (TE) [49]. This metric has been used to measure how movement information cascades through simulated [25,58] and real [27,59] systems, to study interactions between animals and robots [29,60,61], and to establish hierarchy in leader-follower experiments [23,44].…”

Role of dissolved oxygen on behavioural and stress response of golden mahseer, Tor putitora

“…The duration (S) of movement around the centre point of arena explored area was maximum in the high dissolved oxygen content group as compared to other groups, indicating that the oxygen content plays an important role in the activity of the fishes. The different types of fish behavioural activity such as movement, average speed, exploration by the Zebrafish along the X axis in the arena was studied by using robotics as a source of artificial intelligence (Spinello et al, 2019). The normalised average area of exploration within the arena were in the 2 2 control (0.81±0.005 cm ), low dissolved oxygen (0.63±0.015 cm ) 2 and high dissolved oxygen (2.02±0.01 cm ).…”