Circuit Homology between Decussating Pathways in the Ciona Larval CNS and the Vertebrate Startle-Response Pathway

Comparing synaptic circuits and networks between brains of different animal groups helps us derive an understanding of how nervous systems might have evolved. The circuits of the startle response pathway in the brains of tailed vertebrates are known from electrophysiological studies on the giant reticulospinal Mauthner cells (M-cells). To identify morphological counterparts in chordate tunicates, a sister group of vertebrates [1, 2], we have compiled a densely reconstructed connectome (defined in [3]) for the CNS in the tadpole larva of Ciona intestinalis (L.), using ssEM [4]. The dorsal, tubular CNS of the ∼1-mm tadpole larva is built on a similar plan to vertebrates, its neurons distributed rostrocaudally in three centers, a brain vesicle, motor ganglion, and caudal nerve cord [5]. A single pair of descending decussating neurons, ddNs, found in the motor ganglion, have similarities to reticulospinal neurons descending from the vertebrate hindbrain to the spinal cord. The pre- and postsynaptic connections and circuits of these ddNs support their homology with decussating vertebrate M-cells. Network analysis reveals that, like M-cells, ddNs receive mechanosensory input from the peripheral nervous system and provide input to motoneurons, premotor interneurons, and ascending commissural inhibitory neurons (ACINs). These circuits uncover a putative homologous startle network in the Ciona tadpole. However, differences in circuits, including a lack of bilateral symmetry in their network, and convergence of inputs from left and right sides, raise questions about the relationship between form and function, and are a possible outcome of the tiny number of neurons in ascidian larvae. •Serial electron microscopy of Ciona larval connectome reveals its motor pathways•These highlight neurons with network homology to vertebrate reticulospinal neurons•Their synaptic networks resemble those that underlie fish startle responses•They include two identified descending decussating neurons with input to motoneurons Ryan et al. report the synaptic network of motor pathways in the CNS of a tunicate tadpole larva. This reveals hitherto unreported sensory input to premotor neurons. The network shows likely homology to pathways in the brain of tailed vertebrates that mediate startle responses through the Mauthner cells.