Deep origins for the tectal visual processing centers in chordates

Ciona larvae have two distinct visuomotor behaviors - a looming shadow response and negative phototaxis. These are mediated by separate neural pathways that initiate from different clusters of photoreceptors. We report that input from both pathways is processed to generate fold-change detection (FCD) outputs - making the behavioral outputs reflective of relative changes in input, not absolute input values. Visual inputs from both pathways project first to the posterior brain vesicle (pBV). We find that the pBV shares hallmarks with the vertebrate midbrain optic tectum, including its anatomy, connectivity, function and gene expression - despite previous speculation that Ciona lacks a midbrain. The connectivity and properties (excitatory or inhibitory) of pBV interneurons conform to known FCD circuits, but with different circuit architectures for the two pathways. The negative phototaxis circuit forms an incoherent feedforward loop that involves interconnecting cholinergic and GABAergic interneurons. The looming shadow circuit uses the same cholinergic and GABAergic interneurons, but with different synaptic inputs to create a nonlinear integral feedback loop. Consequently, the two FCD circuits generate different behavioral profiles, with the negative phototaxis circuit resulting in a power-function relationship of behavioral output versus fold-change, while in the dimming response this relationship is linear.