Abstract
Animals from insects to humans perform visual escape behavior in response to looming stimuli, and these responses habituate if looms are presented repeatedly without consequence. While the basic visual processing and motor pathways involved in this behavior have been described, many of the nuances of predator perception and sensorimotor gating have not. Here, we have performed both behavioral analyses and brain-wide cellular-resolution calcium imaging in larval zebrafish while presenting them with visual loom stimuli or stimuli that selectively deliver either the movement or the dimming properties of full loom stimuli. Behaviorally, we find that, while responses to repeated loom stimuli habituate, no such habituation occurs when repeated movement stimuli (in the absence of luminance changes) are presented. Dim stimuli seldom elicit escape responses, and therefore cannot habituate. Neither repeated movement stimuli nor repeated dimming stimuli habituate the responses to subsequent full loom stimuli, suggesting that full looms are required for habituation. Our calcium imaging reveals that motion-sensitive neurons are abundant in the brain, that dim-sensitive neurons are present but more rare, and that neurons responsive to both stimuli (and to full loom stimuli) are concentrated in the tectum. Neurons selective to full loom stimuli (but not to movement or dimming) were not evident. Finally, we explored whether movement- or dim-sensitive neurons have characteristic response profiles during habituation to full looms. Such functional links between baseline responsiveness and habituation rate could suggest a specific role in the brain-wide habituation network, but no such relationships were found in our data. Overall, our results suggest that, while both movement- and dim-sensitive neurons contribute to predator escape behavior, neither plays a specific role in brain-wide visual habituation networks or in behavioral habituation.
Highlights
For prey animals, avoiding approaching predators is crucial to survival, but unnecessary escape behavior is both energetically costly and disruptive to normal behavioral routines
We have identified the neuronal substrates for the visual habituation to luminance, movement, and looms, and show that loom habituation at the circuit level requires both components
It has previously been shown that drops in luminance, moving edges, and loom stimuli lead to different types and probabilities of visual startle behavior in zebrafish larvae
Summary
For prey animals, avoiding approaching predators is crucial to survival, but unnecessary escape behavior is both energetically costly and disruptive to normal behavioral routines. If the loom is sufficiently salient, it elicits a stereotyped escape response, which in larval zebrafish takes the form of a rapid body bend followed by a powerful swim sequence (Dunn et al, 2016; Bhattacharyya et al, 2017; Marques et al, 2018). The core sensorimotor circuitry responsible for visual escape in larval zebrafish has been described (reviewed in Marquez-Legorreta et al, 2020), involving the perception of motion and luminance by specialized retinal ganglion cells (RGCs) (Temizer et al, 2015), widespread and powerful loom responses in neurons belonging to the tectum (called the superior colliculus in mammals) contralateral to the stimulus (Helmbrecht et al, 2018), and downstream activation of reticulospinal neurons in the hindbrain (Sato et al, 2007; Yao et al, 2016). Many details about how particular components of the loom stimulus are detected and integrated, and how behaviors are gated, remain mysterious
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