Journal of comparative physiology

, Volume 143, Issue 4, pp 541–553 | Cite as

Electrophysiological and morphological characterization of the winter flounder mauthner cell

  • Steven J. Zottoli
Article

Summary

Flatfish (Pseudopleuronectes americanus) have Mauthner cells (M-cells) which are small as compared to certain other teleosts and behaviorally these fish display a suppression of a M-cell initiated startle response while on the substrate. They may depend on camouflage and, therefore, immobility in protection from predation. This ability to suppress the startle response could then be expressed in membrane properties of the M-cell, inhibition of the motoneurons innervated by M-axon collaterals or visual, tactile, auditory and vestibular inputs to the M-cell. Thus the present experiments were designed to study some electrophysiological and morphological properties of the winter flounder M-cell for comparison with that of the goldfish.

Morphologically the winter flounder M-cell is similar to that of the goldfish. Specifically it has two major dendrites, is located at the level of the VIIIth nerve, has an axon that decussates to the opposite side of the medulla and has an axon cap. The latter structure is similar in its organization to that of the goldfish, a finding which contradicts previous reports (Figs. 8–10).

Electrophysiological identification of the winter flounder M-cell was complicated by the similarity of its antidromic response latency to that of other adjacent neurons. In addition, the frequent failure of the antidromically activated spike to invade the M-cell initial segment-axon hillock region resulted in small field potentials recorded in the axon cap. Rather, the cell was localized utilizing orthodromic fields generated by stimulation of the VIIIth nerve or more commonly with an ‘extrinsic hyperpolarizing potential’ which is localized to the axon cap (Fig. 2). Intracellular records of membrane potential, inhibitory potentials (Fig. 4) and VIIIth nerve EPSPs (Fig. 5) were similar to those described in the goldfish. However, the saccular input, which in goldfish is auditory in nature, most likely is responsive to postural changes in the adult flatfish and would have little influence on M-cell excitability in response to an abrupt sound stimulus. This postulated reduction of excitatory input may be one factor contributing to the suppression of sound-evoked startle responses when the winter flounder is on a compatible background.

Abbreviations

M-cell

Mauthner cell

PHP

passive hyperpolarizing potential

EHP

extrinsic hyperpolarizing potential

LCI

late collateral inhibition

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aljure E, Day JW, Bennett MVL (1980) Postsynaptic depression of Mauthner cell-mediated startle reflex, a possible contributor to habituation. Brain Res 188:261–268Google Scholar
  2. Auerbach AA, Bennett MVL (1969) Chemically mediated transmission at a giant fiber synapse in the central nervous system of a vertebrate. J Gen Physiol 53:183–210Google Scholar
  3. Bartelmez GW (1915) Mauthner's cell and the nucleus motorius tegmenti. J Comp Neurol 25:87–128Google Scholar
  4. Bennett MVL, Crain SM, Grundfest H (1959) Electrophysiology of supramedullary neurons. J Gen Physiol 43:159–250Google Scholar
  5. Bodian D (1937) The structure of the vertebrate synapse. A study of the axon endings on Mauthner's cell and neighboring centers in the goldfish. J Comp Neurol 68:117–159Google Scholar
  6. Diamond J (1971) The Mauthner cell. In: Hoar WS, Randall DJ (eds) Fish physiology, vol V. Academic Press, New York, pp 265–346Google Scholar
  7. Eaton RC, Bombardieri RA (1978) Behavioral functions of the Mauthner neuron. In: Faber DS, Korn H (eds) Neurobiology of the Mauthner cell. Raven Press, New York, pp 221–244Google Scholar
  8. Eaton RC, Bombardieri RA, Meyer DL (1977a) The Mauthner- iniin newly hatched larvae of the zebra fish. J Neurophysiol 38:502–512Google Scholar
  9. Eaton RC, Bombardieri RA, Meyer DL (1977a) The Mauthner initiated startle response in teleost fish. J Exp Biol 66:65–81Google Scholar
  10. Eaton RC, Farley RD, Kimmel CB, Schabtach E (1977b) Functional development in the Mauthner cell system of embryos and larvae of the zebra fish. J Neurobiol 8:151–172Google Scholar
  11. Enger PS (1963) Single unit activity in the peripheral auditory system of the teleost fish. Acta Physiol Scand Suppl 59:210Google Scholar
  12. Faber DS, Funch PG (1980) Differential properties of orthodromic and antidromic impulse propagation across the Mauthner cell initial segment. Brain Res 190:255–260Google Scholar
  13. Faber DS, Korn H (1973) A neuronal inhibition mediated electrically. Science 179:577–578Google Scholar
  14. Faber DS, Korn H (1978) Electrophysiology of the Mauthner cell: basic properties, synaptic mechanisms, and associated networks. In: Faber DS, Korn H (eds) Neurobiology of the Mauthner cell. Raven Press, New York, pp 47–131Google Scholar
  15. Frisch K von (1936) Über den Gehörsinn der Fische. Biol Rev 11:210–246Google Scholar
  16. Frisch K von (1938) Über die Bedeutung des Sacculus und der Lagena für den Gehörsinn der Fische. Z Vergl Physiol 25:703–747Google Scholar
  17. Furshpan EJ (1964) ‘Electrical transmission’ at an excitatory synapse in a vertebrate brain. Science 144:878–880Google Scholar
  18. Furshpan EJ, Furukawa T (1962) Intracellular and extracellular responses of the several regions of the Mauthner cell of the goldfish. J Neurophysiol 25:732–771Google Scholar
  19. Furukawa T, Furshpan EJ (1963) Two inhibitory mechanisms in the Mauthner neurons of goldfish. J Neurophysiol 26:140–176Google Scholar
  20. Jacob W (1928) Über das Labyrinth der Pleuronectiden. Zool Allg Zool 44:523–574Google Scholar
  21. Johnson PC (1976) A rapidly setting glue for resectioning and remounting epoxy embedded tissue. Stain Technol 51:275–276Google Scholar
  22. Kohno K (1970) Symmetrical axo-axonic synapses in the axon cap of the goldfish Mauthner cell. Brain Res 23:255–258Google Scholar
  23. Korn H, Bennett MVL (1975) Vestibular nystagmus and teleost oculomotor neurons: functions of electrotonic coupling and dendritic impulse initiation. J Neurophysiol 38:430–451Google Scholar
  24. Korn H, Faber DS (1975) An electrically mediated inhibition in goldfish medulla. J Neurophysiol 38:452–471Google Scholar
  25. Korn H, Faber DS (1976) Vertebrate central nervous system: same neurons mediate both electrical and chemical inhibitions. Science 194:1166–1169Google Scholar
  26. Korn H, Triller A, Faber DS (1978) Structural correlates of recurrent collateral interneurons producing both electrical and chemical inhibitions of the Mauthner cell. Proc R Soc Lond [Biol] 202:533–539Google Scholar
  27. Lowenstein O (1957) The acousticolateralis system. In: Brown ME (ed) The physiology of fishes, vol 2. Academic Press, New York, pp 155–186Google Scholar
  28. Lowenstein O (1971) The labyrinth. In: Hoar WS, Randall DJ (eds) Fish physiology, vol V. Academic Press, New York, pp 207–240Google Scholar
  29. Manning FB (1924) Hearing in the goldfish in relation to the structure of its ear. J Exp Zool 41:5–20Google Scholar
  30. Nakajima Y (1974) Fine structure of the synaptic endings on the Mauthner cell of the goldfish. J Comp Neurol 156:375–402Google Scholar
  31. Nakajima Y, Kohno K (1978) Fine structure of the Mauthner cell: synaptic topography and comparative study. In: Faber DS, Korn H (eds) Neurobiology of the Mauthner cell. Raven Press, New York, pp 133–166Google Scholar
  32. Otsuka N (1964) Weitere Vergleichend-anatomische Untersuchungen an Mauthnerschen Zellen von Fischen. Z Zellforsch 62:61–71Google Scholar
  33. Platt C (1973) Central control of postural orientation in flatfish. I. Postural change dependence on central neural changes. J Exp Biol 59:491–521Google Scholar
  34. Retzius G (1881) Das Gehörorgan der Wirbelthiere: morphologisch-histologische Studien. I. Das Gehörorgan der Fische und Amphibien. Samson and Wallin, StockholmGoogle Scholar
  35. Rovainen CM (1967) Physiological and anatomical studies on large neurons of central nervous system of the sea lamprey (Petromyzon marinus). I. Müller and Mauthner cells. J Neurophysiol 30:1000–1023Google Scholar
  36. Rovainen CM (1978) Müller cells, “Mauthner” cells, and other identified reticulospinal neurons in the lamprey. In: Faber DS, Korn H (eds) Neurobiology of the Mauthner cell. Raven Press, New York, pp 245–269Google Scholar
  37. Schöne H (1964) Über die Arbeitsweise der Statolithenapparate bei Plattfischen. Biol Jahresh 4:135–156Google Scholar
  38. Triller A, Korn H (1978) Mise en évidence électrophysiologique et anatomique de neurones vestibulaires inhibiteurs commissuraux chez la tenche (Tinca tinca). CR Acad Sci (D) (Paris) 286:89–92Google Scholar
  39. Triller A, Korn H (1980) Glio-axonic junctional like complexes at the Mauthner cell's axon cap of teleosts: a possible morphological basis for field effect inhibition. Neurosci Lett 18:275–281Google Scholar
  40. Tyrer NM, Bell EM (1974) The intensification of cobalt-filled neurone profiles using a modification of Timm's sulfide-silver method. Brain Res 73:151–155Google Scholar
  41. Zottoli SJ (1976) A comparison of Mauthner cell size in teleosts and cell function in escape tail-flips of unrestrained goldfish in response to sound. PhD Dissertation, University of Massachusetts, Amherst, MAGoogle Scholar
  42. Zottoli SJ (1977) Correlation of startle reflex and Mauthner cell auditory responses in unrestrained goldfish. J Exp Biol 66:243–254Google Scholar
  43. Zottoli SJ (1978a) Comparison of Mauthner cell size in teleosts. J Comp Neurol 178:741–758Google Scholar
  44. Zottoli SJ (1978b) Comparative morphology of the Mauthner cell in fish and amphibians. In: Faber DS, Korn H (eds) Neurobiology of the Mauthner cell. Raven Press, New York, pp 13–15Google Scholar
  45. Zottoli SJ, Faber DS (1979) Properties and distribution of anterior VIIIth nerve excitatory inputs to the goldfish Mauthner cell. Brain Res 174:319–323Google Scholar
  46. Zottoli SJ, Faber DS (1980) An identifiable class of statoacoustic interneurons with bilateral projections in the goldfish medulla. Neurosci 5:1287–1302sGoogle Scholar

Copyright information

© Springer-Verlag 1981

Authors and Affiliations

  • Steven J. Zottoli
    • 1
    • 2
    • 3
  1. 1.Marine Biological LaboratoryWoods HoleUSA
  2. 2.Division of NeurobiologyState University of New York at BuffaloBuffaloUSA
  3. 3.Research Institute on AlcoholismBuffaloUSA
  4. 4.Department of BiologyWilliams CollegeWilliamstownUSA

Personalised recommendations