Neural circuits underlying habituation of visually evoked escape behaviors in larval zebrafish

Larval zebrafish that are exposed repeatedly to dark looming stimuli will quickly habituate to these aversive signals and cease to respond with their stereotypical escape swims. A dark looming stimulus can be separated into two independent components: one that is characterized by an overall spatial expansion, where overall luminance is maintained at the same level, and a second, that represents an overall dimming within the whole visual field in the absence of any motion energy. Using specific stimulation patterns that isolate these independent components, we first extracted the behavioral algorithms that dictate how these separate information channels interact with each other and across the two eyes during the habituation process. Concurrent brain wide imaging experiments then permitted the construction of circuit models that suggest the existence of two separate neural pathways. The first is a looming channel which responds specifically to expanding edges presented to the contralateral eye and relays that information to the brain stem escape network to generate directed escapes. The second is a dimming-specific channel that could be either monocular or binocularly responsive, and that appears to specifically inhibit escape response when activated. We propose that this second channel is under strong contextual modulation and that it is primarily responsible for the incremental silencing of successive dark looming-evoked escapes.