Establishment of left‐right asymmetric innervation in the lancelet oral region

Abstract

Lancelets (amphioxus) exhibit a remarkable asymmetric development in the anterior body region, which is reflected in the peripheral nervous system even at adulthood. Not all of the anterior nerves are involved, but the left third to fifth nerves are clearly asymmetric. To trace the developmental process responsible for asymmetric innervation, the peripheral nerves in the anterior region were studied in pre- and mid-metamorphic larvae, 1-cm-long juveniles, and in adults by using whole-mount immunostaining. The mouth changes in size and location during larval life before moving ventrally and, in conjunction with this change, nerves in the oral region are also modified. The left second nerve initially innervates the oral region, but this connection is secondarily lost. As the mouth expands and shifts posteriorly, the left fifth to ninth nerves join the left third and fourth in the innervation of the oral region. The left third to sixth nerves anastomose with the oral nerve ring, which encircles the mouth on the left side. In the juveniles and adults, there are two nerve plexuses that run parallel to the margin of the oral hood. The innermost of these, the "inner oral-hood nerve plexus", is asymmetrically connected with the left third to fifth nerves on both sides. The other, the "outer oral-hood nerve plexus", is ipsilaterally connected with the third to seventh nerves on both sides. The velar nerve ring is also innervated asymmetrically by the left fourth and fifth nerves. From these observations, we suggest that the oral nerve ring is the precursor of both the inner oral-hood nerve plexus and the velar nerve ring, and that the asymmetric innervation retained in adult lancelets is related to the early anastomosis of the left nerves with the oral nerve ring. We also show that, contrary to the persistent asymmetric innervation, the axonal patterns of the anterior peripheral nervous system in developing lancelets can change.

Sensory Systems in Amphioxus: A Window on the Ancestral Chordate Condition

“…Somewhat later, a class of neurons can be identified in the larval rostrum and oral region whose unusually large size suggests a role in early developmental events, possibly in tract formation. These are the extrinsic neurons described by see also Lacalli, 2002b;Kaji et al, 2001], but whether they are the same as the structures identified by Yasui et al [1998] is not clear. What one can say is that the development of a Fig.…”

Characterization of novel GPCR gene coding locus in amphioxus genome: Gene structure, expression, and phylogenetic analysis with implications for its involvement in chemoreception

“…Although the sensory cells of the peripheral nervous system of amphioxus have been studied extensively by microscopy (Frantz, 1923;Schulte and Riehl, 1977;Bone and Best, 1978;Baatrup, 1981Baatrup, , 1982Lacalli and Hou, 1999;, immunostaining (Yasui et al, 1998;Kaji et al, 2001), cell labeling and axon tracing by DiI (Holland and Yu, 2002), and gene expression Mazet et al, 2004), it is not known conclusively whether they are mechanosensory or chemosensory cells.…”

Neuronal organization of the brain in the adult amphioxus (Branchiostoma lanceolatum): A study with acetylated tubulin immunohistochemistry

“…The Journal of Comparative Neurology | Research in Systems Neuroscience acetylated a-tubulin, and it has been used for demonstrating cilia, nerve fibers, and neurons from many invertebrates and vertebrates that are frequently studied in the laboratory, including amphioxus (Yasui et al, 1998;Kaji et al, 2001Kaji et al, , 2009) and lampreys (Kuratani et al, 1997). It stains a single 55-kD band on Western blot of lysates of cell lines from mammals (supplier data).…”

“…The aim of the present study is to analyze the organization and distribution of neuron types in the brain of the adult amphioxus by means of immunohistochemistry with an antiacetylated tubulin antibody. This panneuronal marker was used previously to study the early development of the peripheral nervous system of amphioxus (Yasui et al, 1998;Kaji et al, 2001Kaji et al, , 2009), revealing both cell perikarya and fibers. Here, the use of this marker has revealed the shape, size, and distribution of numerous types of neuron, allowing a reevaluation of the size and distribution of neuronal populations of the adult brain.…”