Glutamatergic networks in the Ciona intestinalis larva

Abstract

Glutamate is a major neurotransmitter in the excitatory synapses of both vertebrate and invertebrate nervous systems and is involved in many neural processes including photo-, mechano-, and chemosensations, neural development, motor control, learning, and memory. We identified and characterized the gene (Ci-VGLUT) encoding a member of the vesicular glutamate transporter subfamily, a specific marker of glutamatergic neurons, in the ascidian Ciona intestinalis. The Ci-VGLUT gene is expressed in the adhesive organ, the epidermal neurons, and the brain vesicle, but not in the visceral ganglion. The Ci-VGLUT promoter and an anti-Ci-VGLUT antibody were used to analyze the distribution and axonal connections of prospective glutamatergic neurons in the C. intestinalis larva. The green fluorescent protein (GFP) reporter driven by the 4.6-kb upstream region of Ci-VGLUT recapitulated the endogenous gene expression patterns and visualized both the cell bodies and neurites of glutamatergic neurons. Papillar neurons of the adhesive organs, almost all epidermal neurons, the otolith cell, and ocellus photoreceptor cells were shown to be glutamatergic. Each papillar neuron connects with a rostral epidermal neuron. Axons from rostral epidermal neurons, ocellus photoreceptor cells, and neurons underlying the otolith terminate in the posterior brain vesicle. Some caudal epidermal neurons also send long axons toward the brain vesicle. The posterior brain vesicle contains a group of Ci-VGLUT-positive neurons that send axons posteriorly to the visceral ganglion. Our results suggest that glutamatergic neurotransmission plays a major role in sensory systems and in the integration of the sensory inputs of the ascidian larva.

A neurochemical map of the developing amphioxus nervous system

“…Glutamate is also one of the major neurotransmitters used in the vertebrate retina pathway, with the three VGLUTs being differentially expressed in specific classes of retina neurons [54]. Glutamate is further known to be present in the vestibular hair cells of different vertebrates [55-57] as well as in mechanosensory neurons of invertebrates [58]. In C. intestinalis , one VGLUT gene has been identified, which is expressed in both the central and the peripheral nervous system (Figure 13) [58].…”

“…Glutamate is further known to be present in the vestibular hair cells of different vertebrates [55-57] as well as in mechanosensory neurons of invertebrates [58]. In C. intestinalis , one VGLUT gene has been identified, which is expressed in both the central and the peripheral nervous system (Figure 13) [58]. More specifically, VGLUT is found in sensory organs (photoreceptor cells of ocellus and otolith) and interneurons of the posterior sensory vesicle.…”

The synapsin gene family in basal chordates: evolutionary perspectives in metazoans

“…In histological sections, the distribution of Ci-Syn transcripts in this area is characteristically uneven and probably labels specific subpopulations of neurons whose function is still to be investigated. Notably, in this area several types of chemically-identified neuronal types have been reported, including glutamatergic [69], cholinergic [43] and GABAergic neurons [35]. To account for the high number of neurons described in this region, neurons may be present also in Ci-Syn -negative areas.…”

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). It has been shown that swimming behavior is modulated by light and gravity (Horie et al, 2008b;Jiang et al, 2005;Tsuda et al, 2003), and that the response of the larvae to these stimuli can change over time (Kajiwara and Yoshida, 1985).…”