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Evolution of a polymodal sensory response network

Srinivasan, Jagan and Durak, Omer and Sternberg, Paul W. (2008) Evolution of a polymodal sensory response network. BMC Biology, 6 . Art. No. 52. ISSN 1741-7007. PMCID PMC2636771. https://resolver.caltech.edu/CaltechAUTHORS:20090419-212757124

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Abstract

Background: Avoidance of noxious stimuli is essential for the survival of an animal in its natural habitat. Some avoidance responses require polymodal sensory neurons, which sense a range of diverse stimuli, whereas other stimuli require a unimodal sensory neuron, which senses a single stimulus. Polymodality might have evolved to help animals quickly detect and respond to diverse noxious stimuli. Nematodes inhabit diverse habitats and most nematode nervous systems are composed of a small number of neurons, despite a wide assortment in nematode sizes. Given this observation, we speculated that cellular contribution to stereotyped avoidance behaviors would also be conserved between nematode species. The ASH neuron mediates avoidance of three classes of noxious stimuli in Caenorhabditis elegans. Two species of parasitic nematodes also utilize the ASH neuron to avoid certain stimuli. We wanted to extend our knowledge of avoidance behaviors by comparing multiple stimuli in a set of free-living nematode species. Results: We used comparative behavioral analysis and laser microsurgery to examine three avoidance behaviors in six diverse species of free-living nematodes. We found that all species tested exhibit avoidance of chemo-, mechano- and osmosensory stimuli. In C. elegans, the bilaterally symmetric polymodal ASH neurons detect all three classes of repellant. We identified the putative ASH neurons in different nematode species by their anatomical positions and showed that in all six species ablation of the ASH neurons resulted in an inability to avoid noxious stimuli. However, in the nematode Pristionchus pacificus, the ADL neuron in addition to the ASH neuron contributed to osmosensation. In the species Caenorhabditis sp. 3, only the ASH neuron was required to mediate nose touch avoidance instead of three neurons in C. elegans. These data suggest that different species can increase or decrease the contribution of additional, non-ASH sensory neurons mediating osmosensation and mechanosensation. Conclusion: The overall conservation of ASH mediated polymodal nociception suggests that it is an ancestral evolutionarily stable feature of sensation. However, the finding that contribution from non-ASH sensory neurons mediates polymodal nociception in some nematode species suggests that even in conserved sensory behaviors, the cellular response network is dynamic over evolutionary time, perhaps shaped by adaptation of each species to its environment.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://www.biomedcentral.com/1741-7007/6/52PublisherArticle
http://dx.doi.org/10.1186/1741-7007-6-52DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2636771/PubMed CentralArticle
ORCID:
AuthorORCID
Srinivasan, Jagan0000-0001-5449-7938
Sternberg, Paul W.0000-0002-7699-0173
Additional Information:© 2008 Srinivasan et al; licensee BioMed Central Ltd. This article is published under license to 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: 26 September 2008. Accepted: 15 December 2008. Published: 15 December 2008. We thank the Bargmann Lab and the Hart Lab for advice, and Krisha Begalla and Dorota Korta for help with the behavioral assays, Alon Zaslaver for suggesting the cluster analysis and help in generating Figure 7. We thank Karin Kiontke for the C. tripartitum (SB202) strain and advice on phylogeny. Some nematode strains were provided by the Caenorhabditis Genetics Center. We also thank Cori Bargmann, Ryan Baugh, Takao Inoue, Elissa Hallem, Marie-Anne Felix, Ralf J. Sommer and Karin Kiontke for discussions and comments on the manuscript. JS is an Associate and PWS is an Investigator of the Howard Hughes Medical Institute, which supported this research. OD was supported in part by a Summer Undergraduate Fellowship from Caltech.
Funders:
Funding AgencyGrant Number
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Caltech Summer Undergraduate Research Fellowship (SURF)UNSPECIFIED
Subject Keywords:nematode caenorhabditis-elegans; stercoralis infective larvae; sodium-chloride gradient; strongyloides-stercoralis; c-elegans; amphidial neurons; pristionchus-pacificus; haemonchus-contortus; parasitic nematode; ash neurons
PubMed Central ID:PMC2636771
Record Number:CaltechAUTHORS:20090419-212757124
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20090419-212757124
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:14019
Collection:CaltechAUTHORS
Deposited By: Joy Painter
Deposited On:21 Apr 2009 21:48
Last Modified:03 Oct 2019 00:46

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