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Biologically Inspired Microrobots

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Front. Robot. AI | doi: 10.3389/frobt.2019.00038

Zebrafish adjust their behavior in response to an interactive robotic predator

  • 1Department of Mechanical and Aerospace Engineering and Department of Biomedical Engineering, Tandon School of Engineering, New York University, United States
  • 2Department of Mechanical and Aerospace Engineering, Tandon School of Engineering, New York University, United States
  • 3School of Mechanical Engineering, Key Laboratory of Mechanism Theory and Equipment Design of Ministry of Education, Tianjin University, China
  • 4Department of Mechanical and Aerospace Engineering, Tandon School of Engineering, New York University, United States
  • 5Centre for Behavioural Sciences and Mental Health, Istituto Superiore di Sanità, Italy

Zebrafish (Danio rerio) constitute 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 responses 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.

Keywords: danio rerio, ethorobotics, Fear, interactive robots, transfer entropy

Received: 24 Mar 2019; Accepted: 30 Apr 2019.

Edited by:

Islam S. Khalil, University of Twente, Netherlands

Reviewed by:

Mohamed Mitwally, German University in Cairo, Egypt
Jiachen Zhang, Max Planck Institute Stuttgart, Germany  

Copyright: © 2019 Porfiri, Spinello, Yang and Macrì. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Prof. Maurizio Porfiri, Tandon School of Engineering, New York University, Department of Mechanical and Aerospace Engineering and Department of Biomedical Engineering, Brooklyn, 11201, New York, United States, mporfiri@nyu.edu