Covert attention to obstacles biases escapes via the Mauthner cell

Abstract

To study the evolutionary origins of object perception, we investigated whether a primitive vertebrate, the larval zebrafish, is sensitive to the presence of obstacles. The zebrafish, which has become a useful model to study brain-wide circuit dynamics, executes fast escape swims when in danger of predation. We posited that collisions with solid objects during escape would be maladaptive to the zebrafish, and therefore the direction of escape swims should be informed by the locations of barriers. To answer this question, we developed a novel closed-loop high-speed imaging rig outfitted with barriers of various qualities. Using this system, we show that when larval zebrafish escape in response to a non-directional vibrational stimulus, they use visual scene information to avoid collisions with obstacles. Our study demonstrates that fish compute absolute distance to obstacles, as distant barriers outside of collision range elicit less bias than nearby collidable barriers that occupy the same visual field. The computation of barrier features is covert, as the fishs reaction to barriers during routine swimming does not predict that they will avoid barriers when escaping. Finally, through two-photon laser ablations, we suggest the presence of an excitatory input from the visual system to Mauthner cells in the brainstem escape network that is responsible for escape direction bias. We propose that zebrafish construct "object solidity" via an integrative visual computation that is more complex than retinal occupancy alone, suggesting a primitive understanding of object features and possibly the origins of a structured model of the physical world.