REPROGRAMMING OF VISUAL BEHAVIOURS DURING FROG METAMORPHOSIS

Animals interpret visual stimuli based on their ecological context. For example, a tadpole is a conspecific to another tadpole, but prey to a frog. Such innate behaviours often originate in the retina, where stimulus-selective retinal ganglion cells (RGCs) project to brain regions that drive appropriate responses. However, since RGC types and target brain areas appear conserved within vertebrates, it remains unclear how identical stimuli gain divergent meanings. We investigate this in frogs, which turn from filter feeders into ambush predators during metamorphosis. We hypothesize that reprogramming of visual behaviours is caused by rewiring of visual circuits, which we test at the level of behaviour, structure and function.
Closed-loop behaviour tracking from late embryogenesis through metamorphosis revealed distinct behavioural changes: 1) frogs, but not tadpoles, remain under shelter; 2) looming stimuli trigger freezing in frogs but escapes in tadpoles; and 3) Frogs attack small dots while tadpoles do not. Notably, defensive behaviours change gradually, while predation appears suddenly at metamorphosis, suggesting different underlying mechanisms (a).
Tracing retinal projections reveals distinct retinal arborization fields (Afs, b), which in zebrafish link retinal feature channels to specific behaviours. We find that the same AFs are already present in both tadpoles and frogs and suspect that their function changes through RGC rewiring. Indeed, calcium imaging reveals that responses to looming stimuli decrease, while bright light responses increase in froglets, potentially explaining changes in phototaxis and looming responses (c).
Overall, we reveal profound behavioural changes across metamorphosis and propose changed stimulus representations as a potential substrate.