Artificial Embodied Circuits Uncover Neural Architectures of Vertebrate Visuomotor Behaviors

All brains evolve within specific sensory and physical environments1. Traditionally, neuroscience has focused on studying neural circuits in isolation, yet holistic characterization of their function requires integrative brain-body testing2,3. To investigate the neural and biomechanical mechanisms of sensorimotor transformations, we constructed realistic neuromechanical simulations (simZFish) of the larval zebrafish optomotor response, a visual stabilization behavior4,5. By computationally reproducing the body, physical body-water interactions, visual environments, and experimentally derived neural architectures, we closely replicated the behavior of real zebrafish6. Through systematic manipulation of physiological and circuit features, impossible in biological experiments, we demonstrate how embodiment shapes neural circuit architecture and behavior. When challenged with novel visual stimuli, simZFish predicted neuronal response types, which we identified via calcium imaging in the brain of real zebrafish and used to update the simZFish neural network. In virtual rivers, simZFish performed rheotaxis by using current-induced optic flow as navigational cues, compensating for the simulated water flow. Finally, a physical robot (ZBot) validated the role of embodied sensorimotor circuits in maintaining position in a real river with complex fluid dynamics and visual environments. Together, by iterating between simulations, behavioral observations, neural imaging, and robotic testing, we demonstrate the power of an integrative approach to investigating sensorimotor processing. Research HighlightsO_LIDeveloped simZFish, an open-source neuromechanical simulation modeling the zebrafish optomotor response (OMR). C_LIO_LIDemonstrated that simZFish visuomotor neural circuits are sufficient to maintain position in virtual water currents without additional sensory modalities. C_LIO_LIInvestigated how variations in eye geometry influence neural circuit functionality and behavior. C_LIO_LIConducted optic flow analysis of simulated visual input to identify retinal connectivity requirements, uncovering the factors that shape pretectal neurons preference for the lower posterior visual field. C_LIO_LIsimZFish predicted new neural response types confirmed via real zebrafish calcium imaging. C_LIO_LIValidated simZFish circuits with a physical robot, ZBot, performing rheotaxis in a natural river with rich visual and complex flow dynamics compared to idealized lab and simulation experiments. C_LI O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=137 SRC="FIGDIR/small/629427v1_ufig1.gif" ALT="Figure 1"> View larger version (63K): org.highwire.dtl.DTLVardef@11f2acforg.highwire.dtl.DTLVardef@133b1f3org.highwire.dtl.DTLVardef@e808bcorg.highwire.dtl.DTLVardef@1959616_HPS_FORMAT_FIGEXP M_FIG C_FIG Graphical abstractCombining data-driven neuromechanical simulations and robotic testing, we established an integrative framework for investigating embodied neural circuit functions. Leveraging the behavioral, neurobiological, and theoretical foundations of the visually guided optomotor response in larval zebrafish (blue, left), we developed a virtual zebrafish, simZFish (red, middle), to replicate realistic hydrodynamic, anatomical, sensory, neural, and behavioral aspects, permitting the investigation of emergent properties driven by embodiment. Validating these findings using a physical, zebrafish-inspired robot, ZBot (grey, right), in naturalistic environments informs further experiments, hypotheses, and robotic design.