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Confocal analysis of nervous system architecture in direct-developing juveniles of Neanthes arenaceodentata (Annelida, Nereididae)

Winchell, Christopher J. and Valencia, Jonathan E. and Jacobs, David K. (2010) Confocal analysis of nervous system architecture in direct-developing juveniles of Neanthes arenaceodentata (Annelida, Nereididae). Frontiers in Zoology, 7 (17). ISSN 1742-9994. https://resolver.caltech.edu/CaltechAUTHORS:20101026-121056905

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Abstract

Background: Members of Family Nereididae have complex neural morphology exemplary of errant polychaetes and are leading research models in the investigation of annelid nervous systems. However, few studies focus on the development of their nervous system morphology. Such data are particularly relevant today, as nereidids are the subjects of a growing body of "evo-devo" work concerning bilaterian nervous systems, and detailed knowledge of their developing neuroanatomy facilitates the interpretation of gene expression analyses. In addition, new data are needed to resolve discrepancies between classic studies of nereidid neuroanatomy. We present a neuroanatomical overview based on acetylated α-tubulin labeling and confocal microscopy for post-embryonic stages of Neanthes arenaceodentata, a direct-developing nereidid. Results: At hatching (2-3 chaetigers), the nervous system has developed much of the complexity of the adult (large brain, circumesophageal connectives, nerve cords, segmental nerves), and the stomatogastric nervous system is partially formed. By the 5-chaetiger stage, the cephalic appendages and anal cirri are well innervated and have clear connections to the central nervous system. Within one week of hatching (9-chaetigers), cephalic sensory structures (e.g., nuchal organs, Langdon's organs) and brain substructures (e.g., corpora pedunculata, stomatogastric ganglia) are clearly differentiated. Additionally, the segmental-nerve architecture (including interconnections) matches descriptions of other, adult nereidids, and the pharynx has developed longitudinal nerves, nerve rings, and ganglia. All central roots of the stomatogastric nervous system are distinguishable in 12-chaetiger juveniles. Evidence was also found for two previously undescribed peripheral nerve interconnections and aspects of parapodial muscle innervation. Conclusions: N. arenaceodentata has apparently lost all essential trochophore characteristics typical of nereidids. Relative to the polychaete Capitella, brain separation from a distinct epidermis occurs later in N. arenaceodentata, indicating different mechanisms of prostomial development. Our observations of parapodial innervation and the absence of lateral nerves in N. arenaceodentata are similar to a 19th century study of Alitta virens (formerly Nereis/Neanthes virens) but contrast with a more recent study that describes a single parapodial nerve pattern and lateral nerve presence in A. virens and two other genera. The latter study apparently does not account for among-nereidid variation in these major neural features.


Item Type:Article
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http://dx.doi.org/10.1186/1742-9994-7-17DOIUNSPECIFIED
http://www.frontiersinzoology.com/content/7/1/17PublisherUNSPECIFIED
Additional Information:© 2010 Winchell et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Received: 22 October 2009; Accepted: 16 June 2010; Published: 16 June 2010. We thank Donald Reish for supplying our initial Neanthes laboratory population, and Wei-Chung Chen for technical advice. This work was supported by a GAANN fellowship to CJW and NASA Astrobiology funding to DKJ. Authors' contributions: CJW collected and cultured Neanthes, carried out all aspects of specimen preparation, performed the CLSM, and drafted the manuscript. CJW conceived the study with DKJ, and DKJ contributed to writing of the manuscript. JEV scanned the specimens for SEM. All authors read and approved the final manuscript.
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Graduate Assistance in Areas of National Need (GAANN) fellowshipUNSPECIFIED
NASA AstrobiologyUNSPECIFIED
Issue or Number:17
Record Number:CaltechAUTHORS:20101026-121056905
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20101026-121056905
Official Citation:Winchell et al., Confocal analysis of nervous system architecture in direct-developing juveniles of Neanthes arenaceodentata (Annelida, Nereididae) Frontiers in Zoology 2010, 7:17
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:20541
Collection:CaltechAUTHORS
Deposited By: Jason Perez
Deposited On:26 Oct 2010 22:51
Last Modified:03 Oct 2019 02:11

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