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Immunohistochemical and biochemical evidence for the presence of serotonin-containing neurons and nerve fibers in the octopus arm

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Abstract

The octopus arm contains a tridimensional array of muscles with a massive sensory-motor system. We herein provide the first evidence for the existence of serotonin (5-HT) in the octopus arm nervous system and investigated its distribution using immunohistochemistry. 5-HT-like immunoreactive (5-HT-lir) nerve cell bodies were exclusively localized in the cellular layer of the axial nerve cord. Those cell bodies emitted 5-HT-lir nerve fibers in the direction of the sucker, the intramuscular nerves cords, the ganglion of the sucker, and the intrinsic musculature. Others 5-HT-lir nerve fibers were observed in various tissues, including the cerebrobrachial tract, the skin, and the blood vessels. 5-HT was detected by high-performance liquid chromatography in various regions of the octopus arm at levels matching the density of 5-HT-lir staining. The absence of 5-HT-lir interconnections between the cerebrobrachial tract and the other components of the axial nerve cord suggests that two types of 5-HT-lir innervation exist in the arm. One type, which originates from the brain, may innervate the periphery through the cerebrobrachial tract. Another type, which originates in the cellular layer of the axial nerve cord, may form an intrinsic network in the arm. In addition, 5-HT-lir fibers likely emitted from the neuropil of the axial nerve cord were found to project into cells showing staining for peripheral choline acetyltransferase, a marker of sensory cells of the sucker. Taken together, these observations suggest that intrinsic 5-HT-lir innervation may participate in the sensory transmission in the octopus arm.

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Abbreviations

5-HT:

5-Hydroxytryptamine (serotonin)

5-HT-lir:

5-Hydroxytryptamine-like immunoreactive

abm :

Acetabulo-brachial muscles

ANC:

Axial nerve cord

AR:

Roof of the acetabulum

AT:

Anastomotic tract

AW:

Wall of the acetabulum

BA:

Brachial artery

BN:

Brachial nerve

CBT:

Cerebrobrachial tract

CB:

Central brain (brain)

CL:

Cellular layer of axial nerve cord

ECD-HPLC:

High-performance liquid chromatography coupled with electrochemical detection

Epi:

Epithelium

GS:

Ganglion of sucker

IC:

Interbrachial commissure

im :

Intrinsic musculature

IN:

Infundibulum

INC:

Intramuscular nerve cord

LM:

Longitudinal muscle

LR:

Lateral root

NP:

Neuropil of the axial nerve cord

OM:

Oblique muscle

PBST:

Phosphate-buffered saline with Triton X-100

pChAT:

Peripheral choline acetyltransferase

S:

Sucker

SM:

Sucker muscle

SR:

Sucker rim

TM:

Transverse muscle

VR:

Ventral root

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Acknowledgements

We thank Ms. Koyama and Mrs. Mori, Nakase, Okamoto, Urushiyama, and Yamamoto from the Central Research Laboratory of Shiga University of Medical Science for their excellent technical help.

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Authors and Affiliations

  1. Molecular Neuroscience Research Center, Shiga University of Medical Science, Otsu, Shiga, 520-2192, Japan

    Jean-Pierre Bellier, Ikuo Tooyama & Hiroshi Kimura

  2. Life Science Research Center, Beihua University, Jilin, 132013, China

    Yu Xie

  3. Department of Cytology and Histology, Faculty of Veterinary Medicine, Suez Canal University, Ismailia, 41522, Egypt

    Sameh Mohamed Farouk

  4. Department of Pediatrics, Shiga University of Medical Science, Otsu, Shiga, 520-2192, Japan

    Yuko Sakaue

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  1. Jean-Pierre Bellier
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  2. Yu Xie
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Correspondence to Jean-Pierre Bellier.

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This work was supported by JSPS KAKENHI Grant Number 15K1055600.

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Bellier, JP., Xie, Y., Farouk, S.M. et al. Immunohistochemical and biochemical evidence for the presence of serotonin-containing neurons and nerve fibers in the octopus arm. Brain Struct Funct 222, 3043–3061 (2017). https://doi.org/10.1007/s00429-017-1385-3

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