Electrophysiology and transcriptomics reveal two photoreceptor classes and complex visual integration in Hirudo verbana
Abstract
Among animals with visual processing mechanisms, the leech Hirudo verbana is a rare example in which all neurons can be identified. However, little is known about its visual system, which is composed of several pigmented head eyes and photosensitive non-pigmented sensilla that are distributed across its entire body. Although several interneurons are known to respond to visual stimuli, their response properties are poorly understood. Among these, the S-cell system is especially intriguing: it is multimodal, spans the entire body of the leech and is thought to be involved in sensory integration. To improve our understanding of the role of this system, we tested its spectral sensitivity, spatial integration and adaptation properties. The response of the S-cell system to visual stimuli was found to be strongly dependent on the size of the area stimulated, and adaptation was local. Furthermore, an adaptation experiment demonstrated that at least two color channels contributed to the response, and that their contribution was dependent on the adaptation to the background. The existence of at least two color channels was further supported by transcriptomic evidence, which indicated the existence of at least two distinct groups of putative opsins for leeches. Taken together, our results show that the S-cell system has response properties that could be involved in the processing of spatial and color information of visual stimuli. We propose the leech as a novel system to understand visual processing mechanisms with many practical advantages.
Additional Information
© 2019 Published by The Company of Biologists Ltd. Received 15 February 2019; Accepted 22 June 2019. Published 7 August 2019. We wish to thank Elke Buschbeck and John Layne for the use of equipment and lab space. The authors declare no competing or financial interests. Author contributions: Conceptualization: A. Stowasser, D.A.W.; Methodology: A. Stowasser, J.B.B., D.A.W.; Software: D.A.W.; Formal analysis: A. Stowasser, A. Stahl, J.B.B., D.A.W.; Investigation: A. Stowasser, A. Stahl, J.B.B.; Resources: J.B.B.; Data curation: J.B.B., D.A.W.; Writing - original draft: A. Stowasser, J.B.B., D.A.W.; Writing - review & editing: A. Stowasser, J.B.B., D.A.W.; Visualization: A. Stowasser, J.B.B., D.A.W.; Supervision: D.A.W.; Project administration: D.A.W.; Funding acquisition: D.A.W. Funding was provided by the National Institute of Neurological Disorders and Stroke (NS094403, to D.A.W.) and by the Burroughs Wellcome Fund in the form of a Career Award at the Scientific Interface (to D.A.W.). Deposited in PMC for release after 12 months. Data availability: Illumina sequencing files have been deposited in the NCBI SRA: Bioproject PRJNA504032. Supplementary information: Supplementary information available online at http://jeb.biologists.org/lookup/doi/10.1242/jeb.201764.supplementalAttached Files
Published - jeb201764.full.pdf
Submitted - 552018.full.pdf
Supplemental Material - JEB201764supp.pdf
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Additional details
- Alternative title
- Photoreceptors and integration in H. verbana
- PMCID
- PMC6703701
- Eprint ID
- 92975
- Resolver ID
- CaltechAUTHORS:20190219-112051503
- NIH
- NS094403
- Burroughs Wellcome Fund
- National Institute of Neurological Disorders and Stroke (NINDS)
- Created
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2019-02-19Created from EPrint's datestamp field
- Updated
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2023-06-01Created from EPrint's last_modified field
- Caltech groups
- Tianqiao and Chrissy Chen Institute for Neuroscience