Similarities between Ciona Dorsal Motor Ganglion and Vertebrate Cerebellum: Did a Chordate Ancestor Already Show D/V Subdivision within a Hindbrain Precursor?

The cerebellum, a major structure of the vertebrate central nervous system, forms the dorsal region of the hindbrain. While evidence from connectomics, neuron classification, and gene expression analyses suggests that the major CNS divisions of forebrain, midbrain, hindbrain, and spinal cord predate the vertebrate/tunicate divergence, it is unknown if the subdivision of the hindbrain into a cerebellum, or cerebellum precursor structure, does as well. In fact, conflicting views exist over whether even the most basal vertebrates, the cyclostomes, have a cerebellum homolog. We report here that the motor ganglion (MG), a structure that has been homologized to the vertebrate hindbrain in the chordate Ciona (a tunicate), has functionally distinct dorsal and ventral domains, similar to the generalized hindbrain of vertebrates. In Ciona, the dorsal MG functions as an ascending relay and processing center for peripheral sensory neurons, while the ventral domain processes and relays descending sensorimotor commands. These differences are reflected in distinct neuron classes present in the two domains, as well as in gene expression. While the dorsal MG of Ciona and HB of vertebrates differ in function and complexity, they share a number of similarities. Thus, while it is likely that the cerebellum proper evolved within vertebrates, our findings support the hypothesis that a simpler, dorsally positioned antecedent was present before the tunicate-vertebrate divergence.