Photoreceptor specialization and the visuomotor repertoire of the primitive chordate Ciona

Abstract

The swimming tadpole larva of has one of the simplest central nervous systems (CNSs) known, with only 177 neurons. Despite its simplicity, the CNS has a common structure with the CNS of its close chordate relatives, the vertebrates. The recent completion of a larval CNS connectome creates enormous potential for detailed understanding of chordate CNS function, yet our understanding of larval behavior is incomplete. We show here that larvae have a surprisingly rich and dynamic set of visual responses, including a looming-object escape behavior characterized by erratic circular swims, as well as negative phototaxis characterized by sustained directional swims. Making use of mutant lines, we show that these two behaviors are mediated by distinct groups of photoreceptors. The connectome predicts that these two behavioral responses should act through distinct, but overlapping, visuomotor pathways, and that the escape behavior is likely to be integrated into a broader startle behavior.

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.…”

“…Little is known about the extent of nervous system development in the larvae of M. occulta and other species with non-swimming larvae. The typical tunicate larva has a minimal nervous system dedicated to controlling its swimming and settlement behavior in response to sensory cues such as light, gravity, and mechanical stimuli (Jiang et al, 2005;Rudolf et al, 2018;Salas et al, 2018;Zega et al, 2006). The larval nervous system of the tunicate Ciona intestinalis has been completely mapped, revealing 177 neurons in a dorsal central nervous system (CNS) and 54 peripheral sensory neurons distributed throughout the epidermis (Ryan et al, 2016(Ryan et al, , 2018Ryan and Meinertzhagen, 2019).…”

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

“…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).…”

Parallel Visual Circuitry in a Basal Chordate

“…As larvae, ascidians are tasked with locating a suitable settling substrate while avoiding predation. Among the described behaviors of Ciona larvae are geotaxis, a mechanosensory/touch response, an escape response mediated by light dimming, and negative phototaxis [15][16][17][18]. Several sensory systems are found in the BV, including the geotactic otolith and the photosensitive ocellus.…”

“…The first photoreceptor group (PR-I) is comprised of 23 cells and clustered around the pigment cell ( Figure 1). The opsin-containing outer segments of the PR-Is project into the cup-shaped pigment cell making this group sensitive to the direction of incident light, thereby mediating negative phototaxis [17,20]. The second group of ocellus photoreceptors (PR-II, Figure 1) contains seven cells and is adjacent and anterior to the PR-Is, and is not associated with the pigment cell.…”