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Neuronal control of pedal sole cilia in the pond snail Lymnaea stagnalis appressa

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Abstract

5-HT (serotonin) is a ubiquitous neurotransmitter that produces ciliary beating in gastropods when applied topically, but ciliary beating caused by gastropod serotonergic neurons has been described in only three neuron pairs. We extend these results to the North American Lymnaea stagnalis appressa, which is a different species from the European Lymnaea stagnalis. We describe a non-serotonergic neuron pair, PeV1, which accelerates pedal sole mucociliary transport and a serotonergic neuron pair, PeD7, which slows mucociliary transport. We compare and discuss development and identified neurons in L. s. appressa and in L. stagnalis, which have homologs to L. s. appressa PeD7 and PeV1 neurons. In addition to PeD7 and PeV1 neurons, we test neurons immunoreactive to Tritonia pedal peptide antibodies with negative results for mucociliary transport. In characterizing PeD7 and PeV1 neurons, we find that PeV1 does not excite PeD7. In semi-intact preparations, a strong increase in PeD7 neuron activity occurs during tactile stimulation, but V1 neurons are inhibited during tactile stimulation. Following tactile stimulation, PeV1 neurons show strong activity. This suggests a distinct difference in function of the two neuron pairs, which both have their axons overlying pedal sole ciliary cells. Application of 5-HT to the pedal sole initiates mucociliary transport in 1.4–1.9 s with a time course similar to that seen when stimulating a PeV1 neuron. This result appears to be through a 5-HT1A-like receptor on the pedal sole. We describe a possible external source of 5-HT on the pedal sole from 5-HT immunoreactive granules that are released with mucus.

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Abbreviations

5-HT:

Serotonin

PeD7:

D7

PeV1:

V1

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Acknowledgments

We thank the Director of Friday Harbor Laboratories for use of the facilities, the staff of Friday Harbor Laboratories for assistance, and the Center for Cell Dynamics for use of the confocal microscope during this work. This work was supported in part by Pacific Sciences Institute.

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The authors declare that they have no conflict of interest.

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Experiments performed here comply with the current laws of the USA.

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  1. Friday Harbor Laboratories, 620 University Road, Friday Harbor, WA, 98250, USA

    Roger D. Longley & Misa Peterman

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  1. Roger D. Longley
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Correspondence to Roger D. Longley.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Fig. 1 Cobalt backfill of the ventromedian pedal nerve. (pdf, 90 kB) (PDF 91 kb)

359_2012_770_MOESM2_ESM.pdf

Supplementary Fig. 2 L. s. appressa pedal ganglia and nerves showing immunoreactivity to TPep antibodies. (pdf, 135 kB) (PDF 130 kb)

Supplementary Video 1 Carbon grain movement on the pedal sole after intracellular stimulation of V1, ventromedian pedal nerve connected to posterior part of foot, V1 action potentials on audio track. (Quicktime mov, 3.2 MB, view full screen) (MOV 3285 kb)

Supplementary Video 2 Carbon grain movement on the pedal sole and in the water column when the ventromedian nerve is stimulated, stimulus on audio track. (Quicktime mov, 3.3 MB, view full screen) (MOV 6116 kb)

Supplementary Video 3 Carbon grain movement on the pedal sole after application of 200 μM l−1 5-HT puffs. 5-HT solution contains a low concentration of blue dye. (Quicktime mov, 4.0 MB, view full screen) (MOV 5521 kb)

Supplementary video 4 Carbon grain movement on the pedal sole when neurons that move carbon grains on the lateral edges of the foot are stimulated intracellularly, axons in the inferior pedal nerves, action potentials are on audio track. (Quicktime mov, 4.8 MB, view full screen) (MOV 4669 kb)

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Longley, R.D., Peterman, M. Neuronal control of pedal sole cilia in the pond snail Lymnaea stagnalis appressa . J Comp Physiol A 199, 71–86 (2013). https://doi.org/10.1007/s00359-012-0770-x

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