Journal of Comparative Physiology A

, Volume 172, Issue 5, pp 611–618 | Cite as

Activation of Mauthner neurons during prey capture

  • J. G. Canfield
  • G. J. Rose


The Mauthner (M-) cells, a bilateral pair of medullary neurons in fish, initiate the characteristic “C-start” predatory escape response of teleosts. Similar movements have been described during hatching, social interactions, and feeding. M-cell firing, however, has not been correlated directly with these other behaviors. The objective of this study was to determine whether the M-cell, in addition to escape, plays a role in feeding.
  1. 1.

    Goldfish were chronically implanted with electrodes positioned near the axon cap of one of the two M-cells. Subsequently, M-cell activity was monitored for up to 8 days while fish were surface feeding on live crickets.

  2. 2.

    The M-cell fires and the fish performs a C-shaped flexion in association with the terminal phase of prey capture. Thus, the M-cell is active in the context of at least two behaviors, predator escape and prey capture, and may be considered a part of behaviorally shared neural circuitry.

  3. 3.

    For the goldfish, Mauthner-initiated flexions during feeding rapidly remove the prey from the water's surface and minimizes the fish's own susceptibility to surface predation. Other species may possess a diverse repertoire of Mauthner-mediated feeding behaviors that depend on their adaptive specializations for predation. Moreover, group competition between predators and their prey may have facilitated a “neural arms race” for M-cell morphology and physiology.


Key words

Mauthner cell Prey capture Behavioral multifunction Escape neuron Shared circuitry Neu ral arms race 


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  1. Bastian J (1981a) Electrolocation. I. How the electroreceptors of Apteronotus albifrons code for moving objects and other electrical stimuli. J Comp Physiol 144:465–479Google Scholar
  2. Bastian J (1981b) Electrolocation. II. The effects of moving objects and other electrical stimuli on the activities of two categories of posterior lateral line lobe cells in Apteronotus albifrons. J Comp Physiol 144:481–494Google Scholar
  3. Bellman KL, Krasne FB (1983) Adaptive complexity of interactions between feeding and escape in crayfish. Science 221:779–781Google Scholar
  4. Bennett MVL (1984) Escapism: some revelations. In: Eaton RC (ed) Neural mechanisms of startle behavior. Plenum Press, New York, 353–363Google Scholar
  5. Blaxter JHS, Grey JAB, Denton EJ (1981) Sound and startle responses in herring shoals. J Mar Biol Assoc UK 61:851–869Google Scholar
  6. Bullock TH (1984) Comparative neuroethology of startle, rapid escape, and giant fiber-mediated responses. In: Eaton RC (ed) Neural mechanisms of startle behavior. Plenum Press, New York, 1–13Google Scholar
  7. Canfield JG, Eaton RC (1990) Swimbladder acoustic pressure transduction initiates Mauthner-mediated escape. Nature 347:760–762Google Scholar
  8. Canfield JG, Rose GJ (1993) Electrosensory modulation of escape responses. J Comp Physiol A (in press)Google Scholar
  9. Currie SN (1991) Vibration-evoked startle behavior in larval lampreys. Brain Behav Evol 37:260–271Google Scholar
  10. Dawkins R, Krebs JR (1979) Arms races between and within species. Proc R Soc Lond B 205:489–511Google Scholar
  11. Diamond J (1971) The Mauthner cell. In: Hoar WS, Randall DJ (eds) Fish physiology, sensory systems and electric organs, vol. 5. Academic Press, New York, 265–346Google Scholar
  12. DiDomenico R, Nissanov J, Eaton RC (1988) Lateralization and adaptation of a continuously variable behavior following lesions of a reticulospinal command neuron. Brain Res 473:15–28Google Scholar
  13. Dill LM (1990) Distance-to-cover and the escape decisions of an African cichlid fish, Melanochromis chipokae. Environ Biol Fishes 27:147–152Google Scholar
  14. Dumont JPC, Robertson RM (1986) Neuronal circuits: an evolutionary perspective. Science 233:849–853Google Scholar
  15. Eaton RC, Bombardieri RA (1978) Behavioral functions of the Mauthner neuron. In: Faber D, Korn H (eds) Neurobiology of the Mauthner cell. Raven Press, New York, 221–244Google Scholar
  16. Eaton RC, DiDomenico (1986) Role of the teleost escape response during development. Trans Am Fish Soc 115:128–142Google Scholar
  17. Eaton RC, Emberley DS (1991) How stimulus direction determines the trajectory of the Mauthner-initiated escape response in a teleost fish. J Exp Biol 161:469–487Google Scholar
  18. Eaton RC, Hackett JT (1984) The role of the Mauthner cell in fast-starts involving escape in teleost fishes. In: Eaton RC (ed) Neural mechanisms of startle behavior. Plenum Press, New York, 213–266Google Scholar
  19. Eaton RC, Nissanov J (1985) A review of Mauthner-initiated escape behavior and its possible role in hatching in the immature zebrafish, Branchydanio rerio. Environ Biol Fishes 12:265–279Google Scholar
  20. Eaton RC, Bombardieri RA, Meyer DL (1977) The Mauthner-initiated startle response in teleost fish. J Exp Biol 66:65–81Google Scholar
  21. Eaton RC, Lavender WA, Wieland CM (1981) Identification of Mauthner-initiated response patterns in goldfish: evidence from simultaneous cinematography and electrophysiology. J Comp Physiol 144:521–531Google Scholar
  22. Eaton RC, Lavender WA, Wieland CM (1982) Alternative neural pathways initiate fast-start responses following lesions of the Mauthner neuron in goldfish. J Comp Physiol 145:485–496Google Scholar
  23. Eaton RC, Nissanov J, Wieland CM (1984) Differential activation of Mauthner and non-Mauthner startle circuits in the zebrafish: implications for functional substitution. J Comp Physiol A 155:813–820Google Scholar
  24. Eaton RC, DiDomenico R, Nissanov J (1988) Flexible body dynamics of the goldfish C-start: implications for reticulospinal command mechanisms. J Neurosci 8:2758–2768Google Scholar
  25. Eaton RC, DiDomenico R, Nissanov J (1991) Role of the Mauthner cell in sensorimotor integration by the brainstem escape network. Brain Behav Evol 37:272–285Google Scholar
  26. Faber DS, Korn H (1978) Electrophysiology in 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, 47–131Google Scholar
  27. Faber DS, Fetcho JR, Korn H (1989) Neuronal networks underly- ing the escape response in goldfish: general implications for motor control. Ann NY Acad Sci 563:11–33Google Scholar
  28. Faber DS, Korn H, Lin J-W (1991) Role of medullary networks and postsynaptic membrane properties in regulating Mauthner cell responsiveness to sensory excitation. Brain Behav Evol 37:286–297Google Scholar
  29. Fay RR (1981) Coding of acoustic information in the eighth nerve. In: Tavolga WN, Popper AN, Fay RR (eds) Hearing and sound communication in fishes. Springer, New York, 189–221Google Scholar
  30. Fay RR, Popper AN (1980) Structure and function in teleost auditory systems. In: Popper AN, Fay RR (eds) Comparative studies of hearing in vertebrates. Springer, Berlin Heidelberg New York, 3–42Google Scholar
  31. Fernald RD (1975) Fast body turns in a cichlid fish. Nature 258:228–229Google Scholar
  32. Fetcho JR (1991) Spinal network of the Mauthner cell. Brain Behav Evol 37:298–316Google Scholar
  33. Fetcho JR (1992) Excitation of motoneurons by the Mauthner axon in goldfish: complexities in a “simple” reticulospinal pathway. J Neurophysiol 67:1574–1586Google Scholar
  34. Fink SV, Fink WL (1981) Interrelationships of the ostariophysan fishes (Teleostei). Zool J Linn Soc 72:297–353Google Scholar
  35. Furshpan EJ (1964) Electrical transmission at an excitatory synapse in a vertebrate brain. Science 144:878–880Google Scholar
  36. 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
  37. Furukawa T, Furshpan EJ (1963) Two inhibitory mechanisms in the Mauthner neurons of goldfish. J Neurophysiol 26:140–176Google Scholar
  38. Hackett JT, Faber DS (1983) Relay neurons mediate collateral inhibition of the goldfish Mauthner cell. Brain Res 264:302–306Google Scholar
  39. Hagedorn M (1986) The ecology, courtship, and mating of gymnotiform electric fish. In: Bullock TH, Heiligenberg W (eds) Electroreception. John Wiley & Sons, New York, 497–525Google Scholar
  40. Hagedorn M, Heiligenberg W (1985) Court and spark: electric signals in the courtship and mating of gymnotoid electric fish. Anim Behav 33:254–265Google Scholar
  41. Harper DG, Blake RW (1990) Fast-start performance of rainbow trout Salmo gairdneri and northern pike Esox lucius. J Exp Biol 150:321–342Google Scholar
  42. Harper DG, Blake RW (1991) Prey capture and the fast-start per- formance of northern pike Esox lucius. J Exp Biol 155:175–192Google Scholar
  43. Heiligenberg W (1973) Electrolocation of objects in the electric fish, Eigenmannia (Rhamphichthyidae, Gymnotoidei). J Comp Physiol 87:137–164Google Scholar
  44. Lauder GV (1983) Food capture. In: Webb PW, Weihs D (eds) Fish biomechanics. Praeger Publishers, New York, 280–311Google Scholar
  45. Lauder GV (1985) Aquatic feeding in lower vertebrates. In: Hildebrand M, Bramble DM, Liem KF, Wake DB (eds) Functional vertebrate morphology. Belknap Press, Cambridge, Mass., 397–399Google Scholar
  46. Magurran AE (1990) The inheritance and development of minnow anti-predatory behaviour. Anim Behav 39:834–842Google Scholar
  47. Nissanov J, Eaton RC (1989) Reticulospinal control of rapid escape turning maneuvers in fishes. Am Zool 29:103–121Google Scholar
  48. Nissanov J, Eaton RC, DiDomenico R (1990) The motor output of the Mauthner cell, a reticulospinal command neuron. Brain Res 517:88–98Google Scholar
  49. Nolen TG, Hoy RR (1984) Initiation of behavior by single neurons: The role of behavioral context. Science 226:992–994Google Scholar
  50. Pitt R (1978) Warfare and hominid brain evolution. J Theor Biol 72:551–575Google Scholar
  51. Popper AN (1983) Organization of the inner ear and auditory processing. In: Northcutt RG, Davis RE (eds) Fish neurobiology, vol. 1. Michigan University Press, Ann Arbor, 125–178Google Scholar
  52. Ritzmann RE, Tobias ML, Fourtner CR (1980) Flight activity initiated via giant interneurons of the cockroach: Evidence for bifunctional trigger interneurons. Science 210:443–445Google Scholar
  53. Rose GJ, Canfield JG (1991) Discrimination of the sign of frequency differences by Sternopygus, an electric fish without a jamming avoidance response. J Comp Physiol A 168:461–467Google Scholar
  54. Rose GJ, Keller C, Heiligenberg W (1987) ‘Ancestral’ neural mechanisms of electrolocation suggest a substrate for the evolution of the jamming avoidance response. J Comp Physiol A 162:759–772Google Scholar
  55. Stefanelli A (1980) I neuroni di Mauthner degli ittiopside. Valutazioni comparative morfologiche e funzionali. Atti Accad Naz Lincei, Ser VIII, 16:1–45Google Scholar
  56. Van Home SM, Eaton RC, Fetcho JR, Nissanov J (1988) What difference does it make having a Mauthner axon? Soc Neurosci Abstr 14:312Google Scholar
  57. Wainwright PC (1986) Motor correlates of learning behavior: feeding on novel prey by pumpkinsed sunfish (Lepomis gibbosus). J Exp Biol 126:237–247Google Scholar
  58. Webb PW (1976) The effect of size on the fast-start performance of rainbow trout Salmo gairdneri, and a consideration of piscivorous predator-prey interactions. J Exp Biol 65:157–177Google Scholar
  59. Webb PW (1978) Fast-start performance and body form in seven species of teleost fish. J Exp Biol 74:211–226Google Scholar
  60. Webb PW (1982) Avoidance responses of fathead minnow to strikes by four teleost predators. J Comp Physiol 147:371–378Google Scholar
  61. Webb PW (1984) Body form, locomotion and foraging in aquatic vertebrates. Am Zool 24:107–120Google Scholar
  62. Webb PW (1986) Effect of body form and response threshold on the vulnerability of four species of teleost prey attacked by largemouth bass (Micropterus salmoides). Can J Fish Aquat Sci 43:763–771Google Scholar
  63. Webb PW (in press) Exercise performance of fish. In: Jones JH (ed) Comparative vertebrate exercise physiology. Academic Press, Orlando, FloridaGoogle Scholar
  64. Webb PW, Skadsen JM (1980) Strike tactics of Esox. Can J Zool 58:1462–1469Google Scholar
  65. Webb PW, Sims D, Schultz WW (1991) The effect of an air/water surface on the fast-start performance of rainbow trout (Oncorhynchus mykiss). J Exp Biol 155:219–226Google Scholar
  66. Will U (1991) Amphibian Mauthner cells. Brain Behav Evol 37:317–332Google Scholar
  67. Zottoli SJ (1977) Correlation of the startle reflex and Mauthner cell auditory responses in unrestrained goldfish. J Exp Biol 66:243–254Google Scholar
  68. Zottoli SJ (1978) Comparative morphology of the Mauthner cell in fish and amphibians. In: Faber D, Korn H (eds) Neurobiology of the Mauthner cell. Raven Press, New York, 13–45Google Scholar
  69. Zottoli SJ, Hordes AR, Faber DS (1987) Localization of optic tectal input to the ventral dendrite of the goldfish Mauthner cell. Brain Res 401:113–121Google Scholar
  70. Zottoli SJ, Davis GW, Northen SC (1992) Comparative studies of the Mauthner cell in teleosts. In: Benedetii I, Bertolini B, Capanna E (eds) Neurology today. Selected symposia and monographs. Unione Zoologica Italiana, Mucchi Editore, ModenaGoogle Scholar

Copyright information

© Springer-Verlag 1993

Authors and Affiliations

  • J. G. Canfield
    • 1
  • G. J. Rose
    • 1
  1. 1.Department of BiologyUniversity of UtahSalt Lake CityUSA

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