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Integration of ocular and non-ocular photosensory information in the brain of the terrestrial slug Limax

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Abstract

In the terrestrial slugs Limax, most of the photosensory information is thought to be acquired by an eye located on the superior tentacles, by which the slugs avoid light. Recent studies, however, suggested that the brain also plays a role as a photosensor in their negative phototaxis behavior. In the present study, we investigated how the photosensory information acquired by the eye and brain is integrated. The visual pathway in the brain was traced by incorporating tracer molecules from the cut end of an optic nerve, and commissural interactions were found in optic neuropiles located in the lateral regions of the cerebral ganglia. A cluster of neuronal cell bodies located near the dorsal surface of the cerebral ganglion had connections with the contralateral optic neuropile via gap junctions. Some of these neuronal cell bodies were Opn5A-immunoreactive, and contained numerous photic vesicle-like structures. Light-induced spikes were recorded extracellularly from the dorsal surface of these neuronal clusters, and they were synchronous with the spikes recorded from the cut end of the cerebral commissure. This study suggests that both the light information from the eye and the contralateral cerebral ganglion are integrated in the optic neuropile.

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Abbreviations

BSA:

Bovine serum albumin

CC:

Cerebral commissure

CCD:

Charge-coupled device

CG:

Cerebral ganglia

DAB:

3,3′-Diaminobenzidine

DAPI:

4′6-Diamidino-2-phenylidole

HEPES:

2-[4-(2-Hydroxyethyl)-1-piperazineyl]ethanesulfonic acid

HRP:

Horseradish peroxidase

NB:

Neurobiotin

PBS:

Phosphate-buffered saline

PC:

Procerebrum

RT-PCR:

Reverse transcription-polymerase chain reaction

PV:

Photic vesicle

SE:

Standard error

ST:

Superior tentacle

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Acknowledgements

We thank Tomoaki Kozaki for his help in the measurement of the light irradiance. We minimized the number of slugs used, and deep anesthesia to reduce the pain when they were sacrificed. This study was supported by Grants-in-Aid for KAKENHI from the Japan Society for the Promotion of Science (no. 19K06772 to RM) and a Grant of Ohsumi Frontier Science Foundation (3-G0017 to RM).

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Authors and Affiliations

  1. Laboratory of Neurobiology, International College of Arts and Sciences, Fukuoka Women’s University, 1-1-1 Kasumigaoka, Higashi-ku, Fukuoka, 813-8529, Japan

    Yuko Matsuo, Haruka Nishiyama & Ryota Matsuo

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  1. Yuko Matsuo
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  2. Haruka Nishiyama
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  3. Ryota Matsuo
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All authors had full access to all the data in the study and take responsibility for the integrity of the data and accuracy of the data analysis. YM, HN, and RM performed experiments and analyzed the data. RM was a major contributor in writing the manuscript. All authors read and approved the final manuscript.

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Correspondence to Ryota Matsuo.

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Matsuo, Y., Nishiyama, H. & Matsuo, R. Integration of ocular and non-ocular photosensory information in the brain of the terrestrial slug Limax. J Comp Physiol A 206, 907–919 (2020). https://doi.org/10.1007/s00359-020-01447-1

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  • DOI: https://doi.org/10.1007/s00359-020-01447-1

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