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Activation of Mauthner neurons during prey capture

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Abstract

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.

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References

  • Bastian J (1981a) Electrolocation. I. How the electroreceptors of Apteronotus albifrons code for moving objects and other electrical stimuli. J Comp Physiol 144:465–479

    Google Scholar 

  • 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 144:481–494

    Google Scholar 

  • Bellman KL, Krasne FB (1983) Adaptive complexity of interactions between feeding and escape in crayfish. Science 221:779–781

    Google Scholar 

  • Bennett MVL (1984) Escapism: some revelations. In: Eaton RC (ed) Neural mechanisms of startle behavior. Plenum Press, New York, 353–363

    Google Scholar 

  • Blaxter JHS, Grey JAB, Denton EJ (1981) Sound and startle responses in herring shoals. J Mar Biol Assoc UK 61:851–869

    Google Scholar 

  • 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, 1–13

    Google Scholar 

  • Canfield JG, Eaton RC (1990) Swimbladder acoustic pressure transduction initiates Mauthner-mediated escape. Nature 347:760–762

    Google Scholar 

  • Canfield JG, Rose GJ (1993) Electrosensory modulation of escape responses. J Comp Physiol A (in press)

  • Currie SN (1991) Vibration-evoked startle behavior in larval lampreys. Brain Behav Evol 37:260–271

    Google Scholar 

  • Dawkins R, Krebs JR (1979) Arms races between and within species. Proc R Soc Lond B 205:489–511

    Google Scholar 

  • 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, 265–346

    Google Scholar 

  • DiDomenico R, Nissanov J, Eaton RC (1988) Lateralization and adaptation of a continuously variable behavior following lesions of a reticulospinal command neuron. Brain Res 473:15–28

    Google Scholar 

  • Dill LM (1990) Distance-to-cover and the escape decisions of an African cichlid fish, Melanochromis chipokae. Environ Biol Fishes 27:147–152

    Google Scholar 

  • Dumont JPC, Robertson RM (1986) Neuronal circuits: an evolutionary perspective. Science 233:849–853

    Google Scholar 

  • 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, 221–244

    Google Scholar 

  • Eaton RC, DiDomenico (1986) Role of the teleost escape response during development. Trans Am Fish Soc 115:128–142

    Google Scholar 

  • Eaton RC, Emberley DS (1991) How stimulus direction determines the trajectory of the Mauthner-initiated escape response in a teleost fish. J Exp Biol 161:469–487

    Google Scholar 

  • 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, 213–266

    Google Scholar 

  • 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 12:265–279

    Google Scholar 

  • Eaton RC, Bombardieri RA, Meyer DL (1977) The Mauthner-initiated startle response in teleost fish. J Exp Biol 66:65–81

    Google Scholar 

  • Eaton RC, Lavender WA, Wieland CM (1981) Identification of Mauthner-initiated response patterns in goldfish: evidence from simultaneous cinematography and electrophysiology. J Comp Physiol 144:521–531

    Google Scholar 

  • 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 145:485–496

    Google Scholar 

  • 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 155:813–820

    Google Scholar 

  • Eaton RC, DiDomenico R, Nissanov J (1988) Flexible body dynamics of the goldfish C-start: implications for reticulospinal command mechanisms. J Neurosci 8:2758–2768

    Google Scholar 

  • Eaton RC, DiDomenico R, Nissanov J (1991) Role of the Mauthner cell in sensorimotor integration by the brainstem escape network. Brain Behav Evol 37:272–285

    Google Scholar 

  • 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, 47–131

    Google Scholar 

  • 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 563:11–33

    Google Scholar 

  • 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 37:286–297

    Google Scholar 

  • 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, 189–221

    Google Scholar 

  • 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, 3–42

    Google Scholar 

  • Fernald RD (1975) Fast body turns in a cichlid fish. Nature 258:228–229

    Google Scholar 

  • Fetcho JR (1991) Spinal network of the Mauthner cell. Brain Behav Evol 37:298–316

    Google Scholar 

  • Fetcho JR (1992) Excitation of motoneurons by the Mauthner axon in goldfish: complexities in a “simple” reticulospinal pathway. J Neurophysiol 67:1574–1586

    Google Scholar 

  • Fink SV, Fink WL (1981) Interrelationships of the ostariophysan fishes (Teleostei). Zool J Linn Soc 72:297–353

    Google Scholar 

  • Furshpan EJ (1964) Electrical transmission at an excitatory synapse in a vertebrate brain. Science 144:878–880

    Google Scholar 

  • Furshpan EJ, Furukawa T (1962) Intracellular and extracellular responses of the several regions of the Mauthner cell of the goldfish. J Neurophysiol 25:732–771

    Google Scholar 

  • Furukawa T, Furshpan EJ (1963) Two inhibitory mechanisms in the Mauthner neurons of goldfish. J Neurophysiol 26:140–176

    Google Scholar 

  • Hackett JT, Faber DS (1983) Relay neurons mediate collateral inhibition of the goldfish Mauthner cell. Brain Res 264:302–306

    Google Scholar 

  • Hagedorn M (1986) The ecology, courtship, and mating of gymnotiform electric fish. In: Bullock TH, Heiligenberg W (eds) Electroreception. John Wiley & Sons, New York, 497–525

    Google Scholar 

  • Hagedorn M, Heiligenberg W (1985) Court and spark: electric signals in the courtship and mating of gymnotoid electric fish. Anim Behav 33:254–265

    Google Scholar 

  • Harper DG, Blake RW (1990) Fast-start performance of rainbow trout Salmo gairdneri and northern pike Esox lucius. J Exp Biol 150:321–342

    Google Scholar 

  • Harper DG, Blake RW (1991) Prey capture and the fast-start per- formance of northern pike Esox lucius. J Exp Biol 155:175–192

    Google Scholar 

  • Heiligenberg W (1973) Electrolocation of objects in the electric fish, Eigenmannia (Rhamphichthyidae, Gymnotoidei). J Comp Physiol 87:137–164

    Google Scholar 

  • Lauder GV (1983) Food capture. In: Webb PW, Weihs D (eds) Fish biomechanics. Praeger Publishers, New York, 280–311

    Google Scholar 

  • 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., 397–399

    Google Scholar 

  • Magurran AE (1990) The inheritance and development of minnow anti-predatory behaviour. Anim Behav 39:834–842

    Google Scholar 

  • Nissanov J, Eaton RC (1989) Reticulospinal control of rapid escape turning maneuvers in fishes. Am Zool 29:103–121

    Google Scholar 

  • Nissanov J, Eaton RC, DiDomenico R (1990) The motor output of the Mauthner cell, a reticulospinal command neuron. Brain Res 517:88–98

    Google Scholar 

  • Nolen TG, Hoy RR (1984) Initiation of behavior by single neurons: The role of behavioral context. Science 226:992–994

    Google Scholar 

  • Pitt R (1978) Warfare and hominid brain evolution. J Theor Biol 72:551–575

    Google Scholar 

  • 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, 125–178

    Google Scholar 

  • Ritzmann RE, Tobias ML, Fourtner CR (1980) Flight activity initiated via giant interneurons of the cockroach: Evidence for bifunctional trigger interneurons. Science 210:443–445

    Google Scholar 

  • 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 168:461–467

    Google Scholar 

  • 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 162:759–772

    Google Scholar 

  • Stefanelli A (1980) I neuroni di Mauthner degli ittiopside. Valutazioni comparative morfologiche e funzionali. Atti Accad Naz Lincei, Ser VIII, 16:1–45

    Google Scholar 

  • Van Home SM, Eaton RC, Fetcho JR, Nissanov J (1988) What difference does it make having a Mauthner axon? Soc Neurosci Abstr 14:312

    Google Scholar 

  • Wainwright PC (1986) Motor correlates of learning behavior: feeding on novel prey by pumpkinsed sunfish (Lepomis gibbosus). J Exp Biol 126:237–247

    Google Scholar 

  • 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 65:157–177

    Google Scholar 

  • Webb PW (1978) Fast-start performance and body form in seven species of teleost fish. J Exp Biol 74:211–226

    Google Scholar 

  • Webb PW (1982) Avoidance responses of fathead minnow to strikes by four teleost predators. J Comp Physiol 147:371–378

    Google Scholar 

  • Webb PW (1984) Body form, locomotion and foraging in aquatic vertebrates. Am Zool 24:107–120

    Google Scholar 

  • 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 43:763–771

    Google Scholar 

  • Webb PW (in press) Exercise performance of fish. In: Jones JH (ed) Comparative vertebrate exercise physiology. Academic Press, Orlando, Florida

  • Webb PW, Skadsen JM (1980) Strike tactics of Esox. Can J Zool 58:1462–1469

    Google Scholar 

  • 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 155:219–226

    Google Scholar 

  • Will U (1991) Amphibian Mauthner cells. Brain Behav Evol 37:317–332

    Google Scholar 

  • Zottoli SJ (1977) Correlation of the startle reflex and Mauthner cell auditory responses in unrestrained goldfish. J Exp Biol 66:243–254

    Google Scholar 

  • 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, 13–45

    Google Scholar 

  • Zottoli SJ, Hordes AR, Faber DS (1987) Localization of optic tectal input to the ventral dendrite of the goldfish Mauthner cell. Brain Res 401:113–121

    Google Scholar 

  • 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, Modena

    Google Scholar 

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Authors and Affiliations

  1. Department of Biology, University of Utah, 84112, Salt Lake City, Utah, USA

    J. G. Canfield & G. J. Rose

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  1. J. G. Canfield
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  2. G. J. Rose
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Canfield, J.G., Rose, G.J. Activation of Mauthner neurons during prey capture. J Comp Physiol A 172, 611–618 (1993). https://doi.org/10.1007/BF00213683

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