PT  - JOURNAL ARTICLE
AU  - Cezar Borba
AU  - Shea Schwennicke
AU  - Matthew J. Kourakis
AU  - William C. Smith
TI  - Deep origins for the tectal visual processing centers in chordates
AID  - 10.1101/2020.06.13.150151
DP  - 2020 Jan 01
TA  - bioRxiv
PG  - 2020.06.13.150151
4099  - http://biorxiv.org/content/early/2020/06/14/2020.06.13.150151.short
4100  - http://biorxiv.org/content/early/2020/06/14/2020.06.13.150151.full
AB  - Visuomotor 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.Competing Interest StatementThe authors have declared no competing interest.