Non-centralized and functionally localized nervous system of ophiuroids: evidence from topical anesthetic experiments

Ophiuroids locomote along the seafloor by coordinated rhythmic movements of multi-segmented arms. The mechanisms by which such coordinated movements are achieved are a focus of interest from the standpoints of neurobiology and robotics, because ophiuroids appear to lack a central nervous system that...

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Main Authors: Yoshiya Matsuzaka, Eiki Sato, Takeshi Kano, Hitoshi Aonuma, Akio Ishiguro
Format: Article
Language:English
Published: The Company of Biologists 2017-04-01
Series:Biology Open
Subjects:
Online Access:http://bio.biologists.org/content/6/4/425
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spelling doaj-4867a209b4654f03974dc1f0928c1bf32021-06-02T09:26:58ZengThe Company of BiologistsBiology Open2046-63902017-04-016442543810.1242/bio.019836019836Non-centralized and functionally localized nervous system of ophiuroids: evidence from topical anesthetic experimentsYoshiya Matsuzaka0Eiki Sato1Takeshi Kano2Hitoshi Aonuma3Akio Ishiguro4 Department of Physiology, Graduate School of Medicine, Tohoku University, 2-1 Seiryo-cho, Aoba ward, Sendai 980-8575, Japan Research Institute of Electrical Communication, Tohoku University, 2-1-1 Katahira, Aoba ward, Sendai 980-8577, Japan Research Institute of Electrical Communication, Tohoku University, 2-1-1 Katahira, Aoba ward, Sendai 980-8577, Japan Research Institute for Electronic Science, Hokkaido University, Sapporo, Hokkaido 060-0812, Japan Research Institute of Electrical Communication, Tohoku University, 2-1-1 Katahira, Aoba ward, Sendai 980-8577, Japan Ophiuroids locomote along the seafloor by coordinated rhythmic movements of multi-segmented arms. The mechanisms by which such coordinated movements are achieved are a focus of interest from the standpoints of neurobiology and robotics, because ophiuroids appear to lack a central nervous system that could exert centralized control over five arms. To explore the underlying mechanism of arm coordination, we examined the effects of selective anesthesia to various parts of the body of ophiuroids on locomotion. We observed the following: (1) anesthesia of the circumoral nerve ring completely blocked the initiation of locomotion; however, initiation of single arm movement, such as occurs during the retrieval of food, was unaffected, indicating that the inability to initiate locomotion was not due to the spread of the anesthetic agent. (2) During locomotion, the midsegments of the arms periodically made contact with the floor to elevate the disc. In contrast, the distal segments of the arms were pointed aborally and did not make contact with the floor. (3) When the midsegments of all arms were anesthetized, arm movements were rendered completely uncoordinated. In contrast, even when only one arm was left intact, inter-arm coordination was preserved. (4) Locomotion was unaffected by anesthesia of the distal arms. (5) A radial nerve block to the proximal region of an arm abolished coordination among the segments of that arm, rendering it motionless. These findings indicate that the circumoral nerve ring and radial nerves play different roles in intra- and inter-arm coordination in ophiuroids.http://bio.biologists.org/content/6/4/425OphiuroidsLocomotionNon-centralized nervous systemAutonomous controlFunctional localization
collection DOAJ
language English
format Article
sources DOAJ
author Yoshiya Matsuzaka
Eiki Sato
Takeshi Kano
Hitoshi Aonuma
Akio Ishiguro
spellingShingle Yoshiya Matsuzaka
Eiki Sato
Takeshi Kano
Hitoshi Aonuma
Akio Ishiguro
Non-centralized and functionally localized nervous system of ophiuroids: evidence from topical anesthetic experiments
Biology Open
Ophiuroids
Locomotion
Non-centralized nervous system
Autonomous control
Functional localization
author_facet Yoshiya Matsuzaka
Eiki Sato
Takeshi Kano
Hitoshi Aonuma
Akio Ishiguro
author_sort Yoshiya Matsuzaka
title Non-centralized and functionally localized nervous system of ophiuroids: evidence from topical anesthetic experiments
title_short Non-centralized and functionally localized nervous system of ophiuroids: evidence from topical anesthetic experiments
title_full Non-centralized and functionally localized nervous system of ophiuroids: evidence from topical anesthetic experiments
title_fullStr Non-centralized and functionally localized nervous system of ophiuroids: evidence from topical anesthetic experiments
title_full_unstemmed Non-centralized and functionally localized nervous system of ophiuroids: evidence from topical anesthetic experiments
title_sort non-centralized and functionally localized nervous system of ophiuroids: evidence from topical anesthetic experiments
publisher The Company of Biologists
series Biology Open
issn 2046-6390
publishDate 2017-04-01
description Ophiuroids locomote along the seafloor by coordinated rhythmic movements of multi-segmented arms. The mechanisms by which such coordinated movements are achieved are a focus of interest from the standpoints of neurobiology and robotics, because ophiuroids appear to lack a central nervous system that could exert centralized control over five arms. To explore the underlying mechanism of arm coordination, we examined the effects of selective anesthesia to various parts of the body of ophiuroids on locomotion. We observed the following: (1) anesthesia of the circumoral nerve ring completely blocked the initiation of locomotion; however, initiation of single arm movement, such as occurs during the retrieval of food, was unaffected, indicating that the inability to initiate locomotion was not due to the spread of the anesthetic agent. (2) During locomotion, the midsegments of the arms periodically made contact with the floor to elevate the disc. In contrast, the distal segments of the arms were pointed aborally and did not make contact with the floor. (3) When the midsegments of all arms were anesthetized, arm movements were rendered completely uncoordinated. In contrast, even when only one arm was left intact, inter-arm coordination was preserved. (4) Locomotion was unaffected by anesthesia of the distal arms. (5) A radial nerve block to the proximal region of an arm abolished coordination among the segments of that arm, rendering it motionless. These findings indicate that the circumoral nerve ring and radial nerves play different roles in intra- and inter-arm coordination in ophiuroids.
topic Ophiuroids
Locomotion
Non-centralized nervous system
Autonomous control
Functional localization
url http://bio.biologists.org/content/6/4/425
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