Simple Motor System of the Ascidian Larva: Neuronal Complex Comprising Putative Cholinergic and GABAergic/Glycinergic Neurons

Abstract

The ascidian larva is an excellent model for studies of the functional organization and neuronal circuits of chordates due to its remarkably simple central nervous system (CNS), comprised of about 100 neurons. To date, however, the identities of the various neurons in the ascidian larva, particularly their neurotransmitter phenotypes, are not well established. Acetylcholine, GABA, and glycine are critical neurotransmitters for locomotion in many animals. We visualized putative cholinergic neurons and GABAergic/glycinergic neurons in the ascidian larva by immunofluorescent staining using antibodies against vesicular acetylcholine transporter (VACHT) and vesicular GABA/glycine transporter (VGAT), respectively. Neurons expressing a cholinergic phenotype were found in the brain vesicle and the visceral ganglion. Five pairs of VACHT-positive neurons were located in the visceral ganglion. These putative cholinergic neurons extended their axons posteriorly and formed nerve terminals proximal to the most anterior muscle cells in the tail. VGAT-positive neurons were located in the brain vesicle, the visceral ganglion, and the anterior nerve cord. Two distinct pairs of VGAT-positive neurons, bilaterally aligned along the anterior nerve cord, extended axons anteriorly, near to the axons of the contralateral VACHT-positive neurons. Cell bodies of the VGAT-positive neurons lay on these nerve tracts. The neuronal complex, comprising motor neurons with a cholinergic phenotype and some of the GABA/glycinergic interneurons, has structural features that are compatible with a central pattern generator (CPG) producing a rhythmic movement of the tail. The simple CPG of the ascidian larva may represent the ancestral state of the vertebrate motor system.

Neuronal subtype specification in the spinal cord of a protovertebrate

“…These muscles contract in left/right alternation to produce the vigorous swimming behavior that aids in the dispersal of the larvae (Brown et al, 2005;Horie et al, 2010;Ohmori and Sasaki, 1977;Takamura et al, 2002). These neurons are thought to receive inputs from the sensory vesicle, as well as from the peripheral nervous system (Horie et al, 2008a;Takamura, 1998).…”

Neural tube patterning by Ephrin, FGF and Notch signaling relays

“…The MG contains five bilaterally symmetrical pairs of cholinergic neurons that project their axons along the muscle bands in the tail (Fig. 1A) (Horie et al, 2010;Takamura et al, 2002;Takamura et al, 2010). Together with commissural glycinergic inhibitory interneurons in the nerve cord, they drive the alternating left-right contractions of the tail that propel the tadpole forward.…”

A mechanism for graded motor control encoded in the channel properties of the muscle ACh receptor

“…The 4-5 pairs of cholinergic motor neurons located in the motor ganglion (or the visceral ganglion) have accounted for the swimming behavior ( Fig. S1) (7)(8)(9)(10). These cholinergic neurons project axons down the tail and innervate a part of the (mainly dorsal) muscle cells, whereas others receive excitation via gap junctions (8)(9)(10)(11).…”