Parallel visual circuitry in a basal chordate

Abstract

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.

Neuron subtype-specific effector gene expression in the Motor Ganglion of Ciona

“…In addition to cholinergic transmission, GABAergic transmission has been proposed to play a minor role in the negative phototactic pathway, and a major role in the shadow response pathway Kourakis et al, 2019). We detected enrichment of transcripts from the GABA receptor subunit delta-encoding gene Gabrd (KH.C1.1254, LogFC = 2.6) in MGIN2, which we confirmed by ISH (Fig 6B).…”

“…We designed an ISH probe based on the KYOTOGRAIL.2005.771.2.1 gene model, which revealed highly specific expression in differentiating MGIN2s (Fig 6A). According to the C. intestinalis connectome, MGIN2 receives synaptic inputs primarily from Photoreceptor Relay Neurons (prRNs), which in turn receive inputs primarily from Group I photoreceptors (Kourakis et al, 2019;Ryan et al, 2016). Recent experimental evidence suggests that the negative phototactic behavior of Ciona larvae is mediated by directional light detected Group I photoreceptors, while Group II photoreceptors mediate a light dimming "shadow response".…”

“…Like the ddNs, they also form conspicuous electrical synapses with MN2s, but receive synaptic inputs mainly from photoreceptor relay neurons and other interneurons of the brain, where the larval light-and gravity-sensing organs are located. Thus, these two MG neurons subtypes might modulate asymmetric swimming behaviors in response to sensory cues processed by distinct thigmotactic (ddNs) and phototactic/geotactic (MGIN2s) pathways (Kourakis et al, 2019;Rudolf et al, 2019;Salas et al, 2018).…”

Antagonistic Inhibitory Circuits Integrate Visual and Gravitactic Behaviors

“…The two glutamatergic antenna cells are the sole sensory afferents of the gravity-sensing apparatus and project their axons to a cluster of eleven interneurons in the posterior BV named antenna relay neurons (antRNs) ( Figures 1 and S1) [21]. The antRNs express vesicular GABA transporter (VGAT) and are likely GABAergic and inhibitory [37]. The antRNs send their projections through the narrow neck region of the CNS (thought to be homologous to the vertebrate midbrain/hindbrain boundary) to the motor ganglion (MG), which is thought to be homologous to the vertebrate hindbrain (CNS homologies reviewed in [30]).…”

A cis-regulatory change underlying the motor neuron-specific loss of terminal selector gene expression in immotile tunicate larvae

“…In the Ciona MG connectome, three pairs of descending interneurons are predicted to play an important role in both the rhythmicity of swimming movements and their modulation by inputs from the (Kourakis et al, 2019;Ryan et al, 2016;Salas et al, 2018). Of these, the best studied are MGIN1 and MGIN2 (referred to from now on as IN1 and IN2 respectively), which flank MN1.…”