Journal Mobile Options
Table of Contents
Vol. 67, No. 2, 2006
Issue release date: January 2006
Add to my selection Citation Download
Brain Behav Evol 2006;67:111–122
(DOI:10.1159/000089185)
Original Paper

Spinal Nerve Innervation to the Sonic Muscle and Sonic Motor Nucleus in Red Piranha, Pygocentrus nattereri (Characiformes, Ostariophysi)

Onuki A.a · Ohmori Y.b · Somiya H.a
Laboratories of aFish Biology, and bAnimal Morphology and Function, Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Japan Brain Behav Evol 2006;67:111–122 (DOI:10.1159/000089185)

Abstract

The red piranha, Pygocentrus nattereri, produces sounds by rapid contractions of a pair of extrinsic sonic muscles. The detailed innervation pattern of the sonic muscle of the red piranha was investigated. The sonic muscle is innervated by branches (sonic branches) of the third (S3so), fourth (S4so), and fifth (S5so) spinal nerves. The average total number of nerve fibers contained in the right sonic branches (n = 5; standard length, SL, 71–85 mm) was 151.8 (standard deviation, SD, 28.3). The occipital nerve did not innervate the sonic muscle. The sonic motor nucleus (SMN) in the piranha was identified by tracer methods using wheat germ agglutinin-conjugated horseradish peroxidase; labeled sonic motor neurons were only observed on the side ipsilateral to the sonic muscle injected with the tracer. In the transverse sections, the labeled sonic motor neurons were located in the dorsal zone (mainly large and medium neurons) and in the ventral zone (mainly small neurons) of the ventral horn. In the horizontal sections, the labeled neurons formed a rostrocaudally elongated SMN from the level of the caudal part of the second spinal nerve root to the intermediate region between the fifth and sixth spinal nerve roots. The average number of the labeled neurons (n = 5; SL, 64–87 mm) was 152.6 (SD, 7.3). We conclude that the sonic muscles of the piranha are innervated by approximately 300 sonic motor neurons located only in the spinal cord.

References

  1. Bass AH, Baker R (1990) Sexual dimorphisms in the vocal control system of a teleost fish: morphology of physiologically identified neurons. J Neurobiol 21:1155–1168.
  2. Bass AH, Baker R (1991) Evolution of homologous vocal control traits. Brain Behav Evol 38:240–254.
  3. Bass AH, McKibben JR (2003) Neural mechanisms and behaviors for acoustic communication in teleost fish. Prog Neurobiol 69:1–26.
  4. Carlson BA, Bass AH (2000) Sonic/vocal motor pathways in squirrelfish (Teleostei, Holocentridae). Brain Behav Evol 56:14–28.
  5. Dufossé M (1874) Récherches sur les bruits et les sons éxpressifs que font entendre les poissons d’Europe. Ann des Sci Nat Zool 20:1–134.
  6. Fine ML, Mosca PJ (1989) Anatomical study of innervation pattern of the sonic muscle of the oyster toadfish. Brain Behav Evol 34:265–272.
  7. Fine ML, Winn HE, Olla BL (1977) Communication in fishes. In: How Animals Communicate (Sebeok TA, ed), pp 472–518. Bloomington, IN: Indiana University Press.
  8. Fink SV, Fink WL (1996) Interrelationships of ostariophysan fishes (Teleostei). In: Interrelationships of Fishes (Stiassny MLJ, Parenti LR, Johnson GD, eds), pp 209–249. San Diego, CA: Academic Press.
  9. Fürbriger M (1897) İber die spino-occipitalen Nerven der Selachier und Holocephalen und ihre vergleichende Morphologie. In: Festschrift zum siebenzigsten Geburtstage von Carl Gegenbaur 3, pp 349–788. Leipzig: Wilhelm Engelmann.
  10. Kastberger G (1981) Economy of sound production in piranhas (Serrasalminae, Characidae): II. Functional properties of sound emitter. Zool Jb Physiol 85:393–411.
  11. Ladich F (1991) Fische schweigen nicht. Naturwiss Rundsch 44:379–384.
  12. Ladich F, Bass AH (1998) Sonic/vocal motor pathways in catfishes: comparisons with other teleosts. Brain Behav Evol 51:315–330.
  13. Ladich F, Bass AH (2005) Sonic motor pathways in piranhas with a reassessment of phylogenetic patterns of sonic mechanisms among teleosts. Brain Behav Evol 66:167–176.
  14. Markl H (1971) Schallerzeugung bei Piranhas (Serrasalminae, Characidae). Z vergl Physiol 74:39–56.
  15. Meschkat A (1957) Von den Stimmen der Fische im Amazonas. Fischwirt 7:67–68.
  16. Mesulam MM (1982) Principles of horseradish peroxidase neurohistochemistry and their applications for tracing neural pathways: Axonal transport, enzyme histochemistry and light microscopic analysis. In: Tracing Neural Connections with Horseradish Peroxidase (Mesulam MM, ed), pp 1–151. New York: John Wiley and Sons.
  17. Ono RD, Poss SG (1982) Structure and innervation of the swim bladder musculature in the weakfish, Cynoscion regalis (Teleostei: Sciaenidae). Can J Zool 60:1955–1967.

    External Resources

  18. Onuki A, Somiya H (2004) Two types of sounds and additional spinal nerve innervation to the sonic muscle in John Dory, Zeus faber (Zeiformes, Teleostei). J Mar Biol Assoc UK 84:843–850.

    External Resources

  19. Parenti LR, Song J (1996) Phylogenetic significance of the pectoral-pelvic fin association in acanthomorph fishes: a reassessment using comparative neuroanatomy. In: Interrelationships of Fishes (Stiassny MLJ, Parenti LR, Johnson GD, eds), pp 427–444. San Diego, CA: Academic Press.
  20. Takayama M, Onuki A, Yoshino T, Yoshimoto M, Ito H, Kohbara J, Somiya H (2003) Sound and sound producing system of the silver sweeper, Pempheris schwenkii (Perciformes, Pempheridae). J Mar Biol Assoc UK 83:1317–1320.

    External Resources

  21. Tavolga WN (1971) Sound production and detection. In: Fish Physiology, vol 5, Sensory systems and electric organs (Hoar WS, Randall DJ, eds), pp 135–205. New York: Academic Press.
  22. Taylor WR (1967) An enzyme method of clearing and staining small vertebrates. Proc US Natl Mus 122:1–17.
  23. Vance TL, Hewson JM, Modla S, Connaughton MA (2002) Variability in sonic muscle size and innervation among three sciaenids: spot, Atlantic croaker, and weakfish. Copeia 2002:1137–1143.

    External Resources

  24. Winterbottom R (1974) A descriptive synonymy of the striated muscles of the teleostei. Proc Acad Nat Sci Philadelphia 125:225–317.
  25. Yoshimoto M, Kikuchi K, Yamamoto N, Somiya H, Ito H (1999) Sonic motor nucleus and its connections with octaval and lateral line nuclei of the medulla in a rockfish, Sebastiscus marmoratus. Brain Behav Evol 54:183–204.

 goto top of outline Author Contacts

Atsushi Onuki
Laboratory of Fish Biology, Graduate School of Bioagricultural Sciences
Nagoya University, Furo-cho, Chikusa-ku
Nagoya, Aichi 464-8601 (Japan)
Tel./Fax +81 52 789 4083, E-Mail onuki96@nuagr1.agr.nagoya-u.ac.jp


 goto top of outline Article Information

Received: March 29, 2005
Accepted after revision: June 27, 2005
Returned for revision: May 27, 2005
Published online: October 24, 2005
Number of Print Pages : 12
Number of Figures : 9, Number of Tables : 2, Number of References : 25


 goto top of outline Publication Details

Brain, Behavior and Evolution

Vol. 67, No. 2, Year 2006 (Cover Date: January 2006)

Journal Editor: Wilczynski, W. (Atlanta, Ga.)
ISSN: 0006–8977 (print), 1421–9743 (Online)

For additional information: http://www.karger.com/bbe


Copyright / Drug Dosage

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.