A common CNS architecture is observed in all chordates, from vertebrates to basal chordates like the ascidian Ciona. Ciona stands apart among chordates in having a complete larval connectome. Starting with visuomotor circuits predicted by the Ciona connectome, we used expression maps of neurotransmitter use with behavioral assays to identify two parallel visuomotor circuits that are responsive to different components of visual stimuli. The first circuit is characterized by glutamatergic photoreceptors and responds to the direction of light. These photoreceptors project to cholinergic motor neurons, via two tiers of cholinergic interneurons. The second circuit responds to changes in ambient light and mediates an escape response. This circuit uses GABAergic photoreceptors which project to GABAergic interneurons, and then to cholinergic interneurons. Our observations on the behavior of larvae either treated with a GABA receptor antagonist or carrying a mutation that eliminates photoreceptors indicate the second circuit is disinhibitory.

Highlights d Negative gravitaxis in Ciona larvae is triggered by dimming illumination d Inhibitory input from the visual system suppresses gravitaxis until dimming d Output from the gravitaxis organ results in asymmetric motor inhibition d Reorientation behavior is evoked in downward-but not upward-facing larvae

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Visual processing transforms the complexities of the visual world into useful information. Ciona, an invertebrate chordate and close relative of the vertebrates, has one of the simplest nervous systems known, yet has a range of visuomotor behaviors. This simplicity has facilitated studies linking behavior and neural circuitry. Ciona larvae have two distinct visuomotor behaviors – a looming shadow response and negative phototaxis. These are mediated by separate neural circuits that initiate from different clusters of photoreceptors, with both projecting to a CNS structure called the posterior brain vesicle (pBV). We report here that inputs from both circuits are processed to generate fold change detection (FCD) outputs. In FCD, the behavioral response scales with the relative fold change in input, but is invariant to the overall magnitude of the stimulus. Moreover, the two visuomotor behaviors have fundamentally different stimulus/response relationships – indicative of differing circuit strategies, with the looming shadow response showing a power relationship to fold change, while the navigation behavior responds linearly. Pharmacological modulation of the FCD response points to the FCD circuits lying outside of the visual organ (the ocellus), with the pBV being the most likely location. Consistent with these observations, the connectivity and properties of pBV interneurons conform to known FCD circuit motifs, but with different circuit architectures for the two circuits. The negative phototaxis circuit forms a putative 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 putative non-linear integral feedback loop. These differing circuit architectures are consistent with the behavioral outputs of the two circuits. Finally, while some reports have highlighted parallels between the pBV and the vertebrate midbrain, suggesting a common origin for the two, others reports have disputed this, suggesting that invertebrate chordates lack a midbrain homolog. The convergence of visual inputs at the pBV, and its putative role in visual processing reported here and in previous publications, lends further support to the proposed common origin of the pBV and the vertebrate midbrain.

SummaryVisuomotor inputs are processed to extract salient features. In vertebrates, the retina projects to processing centers in the midbrain optic tectum (OT; the superior colliculus in mammals) and the lateral geniculate nucleus, with the OT thought to be the more ancient [1]. The advent of the OT in chordates has been clouded by the reported absence of a midbrain homolog in the sister group to the vertebrates, the tunicates [2–7]. The best characterized tunicate nervous system is that of the Ciona larva, which, despite having only 177 central nervous system (CNS) neurons, has extensive homology with vertebrates CNSs [8,9]. Here we present anatomical, molecular, behavioral and connectomic data that the larval posterior brain vesicle (pBV) of Ciona shares homology with the vertebrate midbrain OT, suggesting their common ancestor possessed a tectum precursor. Moreover, we report that the conservation between the pBV and the OT extends to a role in visual processing. Ciona larvae have two distinct visuomotor behaviors – a looming shadow response and negative phototaxis [10]. These are mediated by separate neural pathways that initiate from different clusters of photoreceptors, both projecting to the pBV [11,12]. We report that inputs from both pathways are processed to generate fold-change detection (FCD) outputs [13]. However, the FCD responses differ between the two pathways, with the looming shadow response showing a power relationship to fold-change, while the navigation pathway responds linearly. Significantly, the connectivity and properties of pBV interneurons conform to known FCD circuit motifs, 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. These differing circuit architectures are reflected in the differing behavioral outputs.