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Journal of Comparative Physiology A

, Volume 165, Issue 3, pp 293–314 | Cite as

Rhythmic electromyographic activities of trunk muscles characterize the sexual behavior in the Himé salmon (landlocked sockeye salmon,Oncorhynchus nerka)

  • Toshiya Matsushima
  • Kohtaro Takei
  • Shoji Kitamura
  • Makoto Kusunoki
  • Masahiko Satou
  • Naoto Okumoto
  • Kazuo Ueda
Article

Summary

In order to describe precisely the fixed action patterns of salmon sexual behavior, we recorded the electromyographic (EMG) activities of trunk and jaw muscles from freely behaving male and female Himé salmon (landlocked sockeye salmon,Oncorhynchus nerka). A series of action patterns (quivering and spawning act in males, digging, covering, prespawning act and spawning act in females, and the swimming and turning movements in both sexes) were characterized by rhythmic activities of the trunk muscles. Each of these activity patterns is quantitatively distinct from the others in such parameters as frequency, bout duration, duty value, intersegmental phase delay, and spatial distribution of rhythmic activities. However, all of these rhythms share a qualitatively homologous pattern with the forward swimming movement: rhythmic activities alternate on both sides of the body (bilateral coupling) and are posteriorly propagated (intersegmental coupling). In addition, a 3∶1 intersegmental phase coupling occurs in the most anterior trunk muscles during the spawning act in some males. Based on these observations, we discussed the biomechanics for these motor patterns (oviposition, ejaculation, body vibration, and mouth opening), and the neural mechanisms for the pattern generation. A possibility was pointed out that the locomotor pattern generator in the spinal cord may be modulated by descending supraspinal signals and recruited to generate such diverse forms of action patterns in sexual behavior.

Keywords

Sexual Behavior Action Pattern Rhythmic Activity Trunk Muscle Swimming Movement 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

CPG

central pattern generator

EMG

electromyography

AC

adductor mandibulae (cephalic portion)

AM

adductor mandibulae (mandibular portion)

DO

dilator operculi

GH

geniohyoideus

LAP

levator arcus palatitni

LPe

musculus lateralis profundus (epaxial portion)

LPh

musculus lateralis profundus (hypaxial portion)

LS

musculus lateralis superficialis

PD

protractor dorsalis

PI

protractor ischii

RD

retractor dorsalis

RI

retractor ischii

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References

  1. Aihara K (1984) Periodic and non-periodic responses of a periodically forced Hodgkin-Huxley oscillator. J Theor Biol 109:249–269Google Scholar
  2. Ayers J, Carpenter GA, Currie S, Kinch J (1983) Which behavior does the lamprey central motor program mediate? Science 221:1312–1314Google Scholar
  3. Camhi JM (1984) Neuroethology; Nerve cells and the natural behavior of animals. Sinauer Associates Inc Publishers, Sunderland, Mass, pp 289–329Google Scholar
  4. Cohen AH (1988) Evolution of the vertebrate central pattern generator for locomotion. In: Cohen AH, Rossingnol S, Grillner S (eds) Neural control of rhythmic movements in vertebrates. Wiley, New York Chichester Brisbane, pp 129–166Google Scholar
  5. Cohen AH, Wallén P (1980) The neural correlates of locomotion in fish: ‘fictive swimming’ induced in an in vitro preparation of the lamprey spinal cord. Exp Brain Res 41:11–18Google Scholar
  6. Cohen AH, Holmes PJ, Rand RH (1982) The nature of the coupling between segmental oscillators of the lamprey spinal generator for locomotion: a mathematical model. J Math Biol 13:345–369Google Scholar
  7. Fabricius E (1953) Aquarium observations on the spawning behavior of the char,Salmo alpinus. Rept Inst Freshwater Res Drottningholm 34:14–48Google Scholar
  8. Gelfand IM, Orlovsky GN, Shik ML (1988) Locomotion and scratching in tetrapods. In: Cohen AH, Rossingnol S, Grillner S (eds) Neural control of rhythmic movements in vertebrates. Wiley, New York Chichester Brisbane, pp 167–199Google Scholar
  9. Greene CW, Greene CH (1914) The skeletal musculature of the king salmon. Bull US Bur Fish 33:21–59Google Scholar
  10. Grillner S, Kashin S (1976) On the generation and performance of swimming in fish. In: Herman RM, Grillner S, Stein PSG, Stuart DG (eds) Neural control of locomotion, vol 18. Plenum Press, New York, pp 181–202Google Scholar
  11. Grillner S, Wallén P (1984) How does the lamprey central nervous system make the lamprey swim? J Exp Biol 112:337–357Google Scholar
  12. Grillner S, McClellan A, Perret C (1981) Entrainment of the spinal pattern generator for swimming by mechanosensitive elements in the lamprey spinal cord in vitro. Brain Res 217:380–386Google Scholar
  13. Grillner S, Wallén P, Dale N, Brodin L, Buchanan JT, Hill R (1987) Transmitters, membrane properties and network circuitry in the control of locomotion in lamprey. Trends Neurosci 10:34–41Google Scholar
  14. Grillner S, Buchanan JT, Wallén P, Brodin L (1988) Neural control of locomotion in lower vertebrates: from behavior to ionic mechanisms. In: Cohen AH, Rossingnol S, Grillner S (eds) Neural control of rhythmic movements in vertebrates. Wiley, New York Chichester Brisbane, pp 1–40Google Scholar
  15. Hanyu I, Tsukamoto K, Yamamori K, Ngan PV, Furukawa K, Hibiya T (1979) Simultaneous recording of physiological information from swimming fish. Bull Jpn Soc Sci Fish 45:1261–1265Google Scholar
  16. Harris-Warrick RM (1988) Chemical modulation of central pattern generators. In: Cohen AH, Rossingnol S, Grillner S (eds) Neural control of rhythmic movements in vertebrates. Wiley, New York Chichester Brisbane, pp 285–331Google Scholar
  17. Harris-Warrick RM, Cohen AH (1985) Serotonin modulates the central pattern generator for locomotion in the isolated lamprey spinal cord. J Exp Biol 116:27–46Google Scholar
  18. Johnston IA (1982) Biochemistry of myosins and contractile properties of fish skeletal muscles. Molec Physiol 2:15–29Google Scholar
  19. Jones JM, Ball JN (1954) The spawning behavior of brown trout and salmon. Brit J Anim Behav 2:103–114Google Scholar
  20. Jones JW, King GM (1949) Experimental observations on the spawning behavior of the Atlantic salmon (Salmo salar Linn.). Proc Zool Soc London 119:33–48Google Scholar
  21. Keith WL, Rand RH (1984) 1∶1 and 2∶1 phase entrainment in a system of two coupled limit cycle oscillators. J Math Biol 20:133–152Google Scholar
  22. Matsumoto G, Aihara K, Ichikawa M, Tasaki A (1984) Periodic and nonperiodic responses of membrane potentials in squid giant axons during sinusoidal current stimulation. J Theor Neurobiol 3:1–14Google Scholar
  23. Matsushima T, Kitamura S, Takei K, Okumoto N, Satou M, Ueda K (1985) An electromyographic study of sexual behavior in Himé salmon (landlocked sockeye salmon,Oncorhynchus nerka). Zool Sci 3:563–567Google Scholar
  24. McClellan AD, Grillner S (1984) Activation of ‘fictive swimming’ by electrical microstimulation of brainstem locomotor regions in an in vitro preparation of the lamprey spinal cord. Brain Res 300:357–361Google Scholar
  25. Oka Y, Satou M, Ueda K (1986a) Descending pathways to the spinal cord in the Himé salmon (landlocked red salmon,Oncorhynchus nerka). J Comp Neurol 254:91–103Google Scholar
  26. Oka Y, Satou M, Ueda K (1986b) Ascending pathways from the spinal cord in the Himé salmon (landlocked red salmon,Oncorhynchus nerka). J Comp Neurol 254:104–112Google Scholar
  27. Rand RH, Cohen AH, Holmes PJ (1988) Systems of coupled oscillators as models of central pattern generators. In: Cohen AH, Rossingnol S, Grillner S (eds) Neural control of rhythmic movements in vertebrates. Wiley, New York Chichester Brisbane, pp 333–367Google Scholar
  28. Roberts BL, Williamson RM (1983) Motor pattern formation in the dogfish spinal cord. In: Roberts A, Roberts BL (eds) Neural origin of rhythmic movements. Cambridge University Press, Cambridge, pp 331–350Google Scholar
  29. Roberts A, Kahn JA, Soffe SR, Clarke JDW (1981) Neural control of swimming in a vertebrate. Science 213:1032–1034Google Scholar
  30. Roberts A, Soffe SR, Clarke JDW, Dale N (1983) Initiation and control of swimming in amphibian embryos. In: Roberts A, Roberts BL (eds) Neural origins of rhythmic movements. Cambridge University Press, Cambridge, pp 261–284Google Scholar
  31. Satou M, Ueda K (1982) Brain mechanisms of salmon sexual behavior. In: Ohnishi E, Hidaka T (eds) Mechanisms of sexual behavior. Sangyo-Tosho, Tokyo, pp 5–19Google Scholar
  32. Satou M, Ueda K (1984) Fish. In: Sugi H, Hiramoto Y (eds) Experimental biology, vol 10. Maruzen, Tokyo, pp 299–312Google Scholar
  33. Satou M, Oka Y, Kusunoki M, Matsushima T, Kato M, Fujita I, Ueda K (1984) Telencephalic and preoptic areas integrate sexual behavior in Himé salmon (landlocked red salon,Oncorhynchus nerka): results of electrical brain stimulation experiments. Physiol Behav 33:441–447Google Scholar
  34. Satou M, Takeuchi H, Takei K, Hasegawa T, Okumoto N, Ueda K (1987) Involvement of vibrational and visual cues in eliciting spawning behavior in male Himé salmon (landlocked red salmon,Oncorhynchus nerka). Anim Behav 35:1556–1558Google Scholar
  35. Schultz LP and students (1935) The breeding activities of the little redfish, a landlocked form of the sockeye salmon,Oncorhynchus nerka. Mid-Pacific Magazine, Jan–March: 67–77Google Scholar
  36. Sherman E, Novotny M, Camhi JM (1977) A modified walking rhythm employed during righting behavior in the cockroachGromphadorhina portentosa. J Comp Physiol 113:303–316Google Scholar
  37. Shiga T, Oka T, Satou M, Okumoto N, Ueda K (1985 a) An HRP study of afferent connections of the supracommissural ventral telencephalon and the medial preoptic area in Himé salmon (landlocked red salmon,Oncorhynchus nerka). Brain Res 361:162–177Google Scholar
  38. Shiga T, Oka T, Satou M, Ueda K (1985b) Efferents from the supracommissural ventral telencephalon in the Himé salmon (landlocked red salmon,Oncorhynchus nerka): an anterograde degeneration study. Brain Res Bull 14:55–61Google Scholar
  39. Takeuchi H, Takei K, Satou M, Matsushima T, Okumoto N, Ueda K (1987) Visual cues as key stimuli for courtship behavior in male Himé salmon (landlocked red salmon,Oncorhynchus nerka). Anim Behav 35:936–939Google Scholar
  40. Tauz AF, Groot C (1975) Spawning behavior of chum salmon (Oncorhynchus keta) and rainbow trout (Salmo gairdneri). J Fresh Res Bd Can 32:633–642Google Scholar
  41. Uematsu K, Yamamori K (1982) Body vibration as a timing cue for spawning in chum salmon. Comp Biochem Physiol 72A: 591–594Google Scholar
  42. Uematsu K, Hanyu I, Hibiya T, Yamamori K (1979) EMG recording from the spawning salmon. Bull Jpn Soc Sci Fish 45:409Google Scholar
  43. Uematsu K, Yamamori K, Hanyu I, Hibiya T (1980) Role of the trunk musculatures in oviposition of chum salmon,Oncorhynchus keta. Bull Jpn Soc Sci Fish 46:395–400Google Scholar

Copyright information

© Springer-Verlag 1989

Authors and Affiliations

  • Toshiya Matsushima
    • 1
  • Kohtaro Takei
    • 1
  • Shoji Kitamura
    • 2
  • Makoto Kusunoki
    • 1
  • Masahiko Satou
    • 1
  • Naoto Okumoto
    • 3
  • Kazuo Ueda
    • 1
  1. 1.Zoological Institute, Faculty of ScienceUniversity of TokyoTokyoJapan
  2. 2.Inland StationNational Research Institute of AquacultureMieJapan
  3. 3.Nikko BranchNational Research Institute of AquacultureTochigiJapan

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