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Immunochemical and electrophysiological analyses of magnetically responsive neurons in the mollusc Tritonia diomedea

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Abstract

Tritonia diomedea uses the Earth’s magnetic field as an orientation cue, but little is known about the neural mechanisms that underlie magnetic orientation behavior in this or other animals. Six large, individually identifiable neurons in the brain of Tritonia (left and right Pd5, Pd6, Pd7) are known to respond with altered electrical activity to changes in earth-strength magnetic fields. In this study we used immunochemical, electrophysiological, and neuroanatomical techniques to investigate the function of the Pd5 neurons, the largest magnetically responsive cells. Immunocytochemical studies localized TPeps, neuropeptides isolated from Pd5, to dense-cored vesicles within the Pd5 somata and within neurites adjacent to ciliated foot epithelial cells. Anatomical analyses revealed that neurites from Pd5 are located within nerves innervating the ipsilateral foot and body wall. These results imply that Pd5 project to the foot and regulate ciliary beating through paracrine release. Electrophysiological recordings indicated that, although both LPd5 and RPd5 responded to the same magnetic stimuli, the pattern of spiking in the two cells differed. Given that TPeps increase ciliary beating and Tritonia locomotes using pedal cilia, our results are consistent with the hypothesis that Pd5 neurons control or modulate the ciliary activity involved in crawling during orientation behavior.

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Abbreviations

ASW:

Artificial seawater

BSA:

Bovine serum albumin

CFG:

Cold-fish gelatin

CNS:

Central nervous system

LPd5:

Left pedal 5

LPd6:

Left pedal 6

RPd7:

Right pedal 7

μT:

MicroTesla

NGS:

Normal goat serum

PTA:

Phosphate-buffered saline with TritonX-100 and sodium azide

PB:

Phosphate buffer

PBS:

Phosphate buffered saline

RPd5:

Right pedal 5

RPd6:

Right pedal 6

LPd7:

Left pedal 7

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Acknowledgements

We thank O.M. Woodward, R.C. Wyeth, and A.O.D. Willows for reviewing and commenting on the work and manuscript. In addition, we thank A.O.D. Willows for providing research space at The Friday Harbor Laboratories. This work was supported by NSF grant IBN-9631951 to K.J.L., a UNC- Dissertation Completion Fellowship to S.D.C., and a Sigma Xi Grant-in-Aid of Research to S.D.C. The research reported here complied with the “Principles of animal care”, publication No. 86–23, revised 1985 of the National Institutes of Health and the current animal care laws of the USA.

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  1. Shaun D. Cain

    Present address: Friday Harbor Laboratories, University of Washington, 620 University Rd, Friday Harbor, WA, 98250, USA

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  1. Department of Biology, University of North Carolina, Chapel Hill, NC, 27599-3280, USA

    Shaun D. Cain, John H. Wang & Kenneth J. Lohmann

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  1. Shaun D. Cain
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Correspondence to Shaun D. Cain.

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Cain, S.D., Wang, J.H. & Lohmann, K.J. Immunochemical and electrophysiological analyses of magnetically responsive neurons in the mollusc Tritonia diomedea . J Comp Physiol A 192, 235–245 (2006). https://doi.org/10.1007/s00359-005-0063-8

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