The Mauthner cell (M-cell) is one of the few identifiable neurons in the vertebrate central nervous system. The ability to locate the M-cell, along with its inputs and outputs, has resulted in important findings in diverse areas of neurobiology including the molecular biology of neurons, synaptic and systems physiology, behavior, development, and neuroethology. The review provides a brief overview of the M-cell and then focuses on recent studies applying state-of-the-art techniques to address new issues and revisit old ones. One advantage of this preparation is the ability to conduct multidisciplinary studies from the subcellular to behavioral levels. For example, studies of activity-dependent changes in the strength of mixed electrotonic and chemical synapses on the M-cell's lateral dendrite in vivo have been correlated with changes in the probability of eliciting a fast startle response initiated by the M-cell and its associated circuits. Similarly, it is now possible to image the activity of the M-cell and its homologs while observing motor behavior in zebrafish larvae. These approaches will provide direct tests of the functional properties of complex neural networks. Moreover, molecular mechanisms that underlie neuronal development can be tested directly with this neuron and its segmental homologs, because these cells occur in singular pairs at defined locations. Finally, after spinal cord injury, the M-cell's axon regenerates, but does not follow its original course, and the startle response gradually recovers. The accessibility of the M-cell system offers the promise that strategies employed in restoring the function of a neural network will be revealed. Thus, we anticipate that the M-cell system will become a favored preparation for multidisciplinary studies on the neuronal basis of behavior and the recovery of behavior after injury. NEUROSCIENTIST 6:26-38, 2000
Platt JB.Ontogenetische Differenzirung des Ektoderms m Necturus. I. Studie. Arch Mikr Anat1894;43:911-66.
2.
Mauthner L.Untersuchungen über den Bau des Rückenmarks der Fische. Eine vorläufige Mittheilung. Sitzgsber Kaiserl Akad Wiss Wien Math-Naturw Classe1859;34:31-6.
3.
Stieda L.Studien über den Amphioxus lanceolatus. Mémoires de L'Academie Imp de Science St. Petersbourg, VIIe série, tome XIX1873;7:1-70.
4.
Seyfarth E-A, Zottoli SJ.Ludwig Mauthner (1840-1894): Neuroanatomist and noted ophthalmologist in fin-de-siécle Vienna. Brain Behav Evol1991;37:252-9.
5.
Faber DS, Korn H, editors. Neurobiology of the Mauthner cell. New York: Raven Press; 1978.
6.
Bullock TH.Identifiable and addressed neurons in the vertebrates. In: Faber DS, Korn H, editors. Neurobiology of the Mauthner cell. New York: Raven Press; 1978. p. 1-12.
Edström A, Sjöstrand J.Protein synthesis in the isolated Mauthner nerve fibre of goldfish. J Neurochem1969;16:67-81.
9.
Koemg E.Evaluation of local synthesis of axonal proteins in the goldfish Mauthner cell axon and axons of dorsal and ventral roots of the rat in vitro. Mol Cell Neurosci1991;2:384-394.
10.
Koemg E.Ribosomal RNA in Mauthner axon: implications for a protein synthesizing machinery in the myelinated axon. Brain Res1979;174:95-107.
11.
Koenig E, Martin R.Cortical plaque-like structures identify ribosome-containing domains in the Mauthner axon. J Neurosci1996;16:1400-11.
12.
Koenig E, Giuditta A.Protein-synthesizing machinery in the axon compartment. Neuroscience1999;89:5-15
13.
Furukawa T, Furshpan EJ.Two inhibitory mechanisms in the Mauthner neurons of goldfish. J Neurophysiol1963;26:140-76.
14.
Korn H, Axelrod H.Electrical inhibition of Purkinje cells in the cerebellum of the rat. Proc Natl Acad Sci U S A1980;77:6244-7.
15.
Furshpan EJ.Electrical transmission at an excitatory synapse in a vertebrate brain. Science1964;144:878-80.
16.
Robertson JD, Bodenheimer TS, Stage DE.The ultrastructure of Mauthner cell synapses and nodes m goldfish brains . J Cell Biol1963;19:159-99.
17.
Diamond J.The activation and distribution of GABA & L-glutamate receptors on goldfish Mauthner neurones: an analysis of dendritic remote inhibition. J Physiol (Lond)1968;194:669-723.
18.
Zottoli SJ.Correlation of the startle reflex and Mauthner cell auditory responses in unrestrained goldfish . J Exp Biol1977;66:243-54.
19.
Eaton RC, Lavender WA, Wieland CM.Identification of Mauthner-mitiated response patterns in goldfish: evidence from simultaneous cinematography and electrophysiology. J Comp Physiol [A]1981;144:521-31.
20.
Korn H, Tnller A, Mallet A, Faber DS.Fluctuating responses at a central synapse: n of binomial fit predicts number of stained presynaptic boutons . Science1981;213:898-901.
21.
Korn H, Mallet A, Tnller A, Faber DS.Transmission at a central inhibitory synapse. II. Quantal description of release, with a physical correlate for the binomial n. J Neurophysiol1982;48:679-707.
22.
Korn H, Burnod Y, Faber DS.Spontaneous quantal currents in a central neuron match predictions from binomial analysis of evoked responses. Proc Natl Acad Sci U S A1987;84:5981-5.
23.
Korn H.Correlation of morphology and function: the one-vesicle hypothesis at Mauthner neuron inhibitory synapses . In: Faber DS, Korn H, Redman SJ, Thompson SM, Altman J, editors. Central synapses: quantal mechanisms and plasticity. Strasbourg: HFSP; 1998 . p. 37-46.
24.
Faber DS, Korn H.Synergism at central synapses due to lateral diffusion of transmitter. Proc Natl Acad Sci U S A1988 ;85: 8708-12.
25.
Lin J-W, Faber DS.Synaptic transmission mediated by single club endings on the goldfish Mauthner cell. I. Characteristics of electrotomc and chemical postsynaptic potentials. J Neurosci1988;8:1302-12
26.
Charpier S, Behrends JC, Triller A, Faber DS, Korn H."Latent" inhibitory connections become functional during activity-dependent plasticity. Proc Natl Acad Sci U S A1995;92:117-20.
27.
Faber DS, Korn H.Unitary conductance changes at teleost Mauthner cell glycinergic synapses: a voltage-clamp and pharmacological analysis. J Neurophysiol1988; 60:1982-99.
28.
Kruk PJ, Korn H, Faber DS.The effects of geometrical parameters on synaptic transmission: a Monte Carlo simulation study. Biophys J1997;73:2874-90.
29.
Legendre P, Korn H.Glycinergic inhibitory synaptic currents and related receptor channels in the zebrafish brain. European J Neurosci1994;6:1544-57.
30.
Fucile S, De Saint Jan, D, David-Watine B, Korn H, Bregestovski P.Comparison of glycme and GABA actions on the zebrafish homomeric glycme receptor. J Physiol (Lond)1999;517:369-83.
31.
Johnston JB.The nervous system of vertebrates. Philadelphia: P. Blakiston's Son & Co.; 1906.
32.
Korn H, Faber DS.Organizational and cellular mechanisms underlymg chemical inhibition of two vertebrate neurons. Prog Brain Res1983;58:165-73.
33.
Korn H, Faber DS, Tnller A.Convergence of morphological, physiological and immunocytochemical techniques for the study of single Mauthner cells. In: Björklund A, Hökfelt T, Wouterlood FG, van den Pol AN, editors. Handbook of chemical neuroanatomy : analysis of microcircuits and synaptic interactions. Amsterdam : Elsevier Science Publishers; 1990. p. 403-80.
34.
Lee RKK, Eaton RC, Zottoli SJ.Segmental arrangement of reticulospmal neurons in the goldfish hindbram. J Comp Neurol1993;329:539-56.
35.
Foreman MB, Eaton RC.The direction change concept for reticulospmal control of goldfish escape. J Neurosci1993 ;13:4101-13.
36.
Faber DS, Yang X-D, Wolszon LR.Plasticity of gap junctions at mixed synapses. In: Hall JE, Zampighi GA, Davis RM, editors. Progress in cell research . New York: Elsevier Science Publishers ; 1993. p. 135-9.
37.
Stefanelli A.I neurom di Mauthner degli Ittiopsidi. Valutaziom comparative morfologiche e funzionali . Lmcei Mem Sci Fis Eccol, Ser VIII, SEZ III, 1 Roma1980,XVI:1-45.
38.
Korn H, Faber DS.Regulation and significance of probabilistic release mechanisms at central synapses. In: Edelman GM, Gall WE, Cowan WM, editors. Synaptic function. New York: Wiley Press;1987. p. 57-108.
39.
Faber DS, Fetcho JR, Korn H.Neuronal networks underlying the escape response in goldfish: general implications for motor control. Ann NY Acad Sci1989;563:11-33.
40.
Eaton RC.Neuroethology of the Mauthner system. Bram Behav Evol1991 ;37.
41.
Eaton RC, Hofve JC, Fetcho JR.Beating the competition: the reliability hypothesis for Mauthner axon size . Brain Behav Evol1995;45:183-194.
42.
Korn H, Faber DS.Escape behavior-brainstem and spinal cord circuitry and function. Curr Opin Neurobiol1996;6:826-32.
Fetcho JR, Cox KJA, O'Malley DM.Monitoring activity in neuronal populations with single-cell resolution in a behaving vertebrate. Histochem J1998;30:153-67.
45.
Ritzmann RE, Eaton RC.Neural substrates for initiation of startle responses. In: Stein PSG, Grillner S, Selverston AI, Stuart DG , editors. Neurons, networks, and motor behavior. Cambridge: MIT Press; 1997. p. 33-44.
46.
Eaton RC, Lee RKK, Foreman MB.The Mauthner cell and other identified neurons of the bramstem escape network of fish. In: Leonard JL, editor. Identified neurons in model systems: twenty-five years of progress . Cambridge: Harvard University Press; 1999, in press.
47.
Zottoli SJ.Comparative morphology of the Mauthner cell in fish and amphibians. In: Faber DS, Korn H, editors. Neurobiology of the Mauthner cell. New York: Raven Press; 1978. p. 13-45.
48.
Hackett JT, Faber DS.Relay neurons mediate collateral inhibition of the goldfish Mauthner cell. Brain Res1983 ;264:302-6.
49.
Fetcho JR.Spinal network of the Mauthner cell. Brain Behav Evol1991 ;37:298-316.
50.
Fursphan EJ, Furukawa T.Intracellular and extracellular responses of the several regions of the Mauthner cell of the goldfish. J Neurophysiol1962;25:732-71.
51.
Zottoli SJ, Bentley AP, Prendergast BJ, Rieff HI.Comparative studies on the Mauthner cell of teleost fish in relation to sensory input. Brain Behav Evol1995;46:151-64.
Korn H, Faber DS.An electrically mediated inhibition in the goldfish medulla. J Neurophysiol38; 1975:452-71.
54.
Faber DS, Korn H, Lin J-W.Role of medullary networks and postsynaptic membrane properties in regulating Mauthner cell responsiveness to sensory excitation. Brain Behav Evol1991;37:286-97.
55.
Eaton RC, DiDomenico R, Nissanov J.Role of the Mauthner cell in sensorimotor integration by the bramstem escape network. Brain Behav Evol1991;37:272-85.
56.
Canfield JG, Rose GJ.Activation of Mauthner neurons during prey capture . J Comp Physiol [A]1993;172:611-18.
57.
Bliss TVP, Lomo T.Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol (Lond)1973;232:331-56
58.
Yang X-D, Korn H, Faber DS. Long-term potentiation of electrotonic coupling at mixed synapses. Nature1990;348:542-5.
59.
Pereda AE, Bell TD, Chang BH, Czernik AJ, Nairn AC, Solderling TR, Faber DS.Ca2+/calmodulin-dependent kinase II mediates simultaneous enhancement of gap-junctional conductance and glutamatergic transmission . Proc Natl Acad Sci U S A1998;95:13272-7.
60.
Yang X-D, Faber DS.Initial synaptic efficacy influences induction and expression of long-term changes in transmission. Proc Natl Acad Sci U S A1991;88:4299-303.
61.
Korn H, Oda Y, Faber DS.Long-term potentiation of inhibitory circuits and synapses in the central nervous system . Proc Natl Acad Sci U S A1992;89:440-3.
62.
Oda Y, Charpier S, Murayama Y, Suma C, Korn H.Long-term potentiation of glycinergic inhibitory synaptic transmission . J Neurophysiol1995;74:1056-74.
63.
Oda Y, Kawasaki K, Monta M, Korn H, Matsui H.Inhibitory long-term potentiation underlies auditory conditioning of goldfish escape behaviour. Nature1998;394:182-5.
64.
Pereda A, Tnller A, Kom H, Faber DS.Dopamine enhances both electrotonic coupling and chemical excitatory postsynaptic potentials at mixed synapses . Proc Natl Acad Sci U S A1992;89:12088-92.
65.
Pereda AE, Nairn AC, Wolszon LR, Faber DS.Postsynaptic modulation of synaptic efficacy at mixed synapses on the Mauthner cell. J Neurosci1994;14:3704-12.
66.
Silva A, Kumar S, Pereda A, Faber DS.Regulation of synaptic strength at mixed synapses: effects of dopamine receptor blockade and protein kinase C activation. Neuropharmacology1995, 34:1559-65.
67.
Kumar S, Faber, DS.Plasticity of first-order sensory synapses: interactions between homosynaptic long-term potentiation and heterosynaptically evoked dopaminergic potentiation. J Neurosci1999;19:1620-35.
68.
O'Malley DM, Fetcho JR.Calcium signals in the zebrafish Mauthner cell: large size and potentiation with repetitive sensory stimulation. Soc Neurosci Abstr1996;22:795.
69.
Kimmel CB.Mauthner axons in living fish larvae. Dev Biol1972;27:272-5.
70.
Eisen JS, Meyers PZ, Westerfield M.Pathway selection by growth cones of identified motoneurones in live zebrafish embryos. Nature1986;320:269-71.
71.
Eaton RC, Bombardieri RA.Behavioral functions of the Mauthner neuron . In: Faber DS, Korn H, editors. Neurobiology of the Mauthner cell. New York: Raven Press; 1978. p. 221-44
72.
Fetcho JR, O'Malley DM.Visualization of active neural circuitry in the spmal cord of mtact zebrafish. J Neurophysiol1995;73:399-406.
73.
Cox KJA, Fetcho JR.Labeling blastomeres with a calcium m-dicator : a non-invasive method of visualizing neuronal activity in zebrafish. J Neurosci Methods1996;68:185-91.
74.
O'Malley DM, Kao Y-H, Fetcho JR.Imaging the functional orgamzation of zebrafish hindbrain segments during escape behaviors . Neuron1996;17:1145-55.
75.
Ritter D, Fetcho JR.Confocal calcium imaging of spinal inter-neurons during swimming in larval zebrafish. Soc Neurosci Abstr1998;24:1667.
76.
Liu KS, Fetcho JR.Photoablations of serially homologous reticulospinal neurons support their differential contributions to escape behavior in larval zebrafish. Soc Neurosci Abstr1998;24-1667.
77.
Sobierajski LM, Avila RS, O'Malley DM, Wang S, Kaufman AE.Visualization of calcium activity in nerve cells. IEEE Computer Graphics Applications1995;15:55-60.
78.
Mendelson B.Development of reticulospinal neurons of the zebrafish. I. Time of origin. J Comp Neurol1986;251:160-71
79.
Metcalfe WK, Mendelson B, Kimmel CB.Segmental homologies among reticulospinal neurons in the hindbrain of the zebrafish larva. J Comp Neurol1986;251:147-59
80.
Haddon C, Smithers L, Schneider-Maunoury S, Coche T, Dommgos H, Lewis J.Multiple delta genes and lateral inhibition in zebrafish primary neurogenesis. Development1998;125.359-70.
81.
Jiang Y-J, Brand M, Heisenberg C-P, Beuchle D, Furutani-Seiki M, Kelsh RN, et al. Mutations affecting neurogenesis and brain morphology in the zebrafish, Damo rerio. Development1996; 123:205-16.
82.
Schier AF, Neuhauss SCF, Harvey M, Malicki J, Solmca-Krezel L, Stainier DYR, et al. Mutations affecting the development of the embryonic zebrafish brain . Development1996;123:165-78.
83.
Bernstein JJ.Relation of spinal cord regeneration to age in adult goldfish. Exp Neurol1964;9:161-74.
84.
Zottoli SJ, Bentley AP, Femer DG, Hering JR, Prendergast BJ , Rieff HI.Spinal cord regeneration in adult goldfish: implications for functional recovery in vertebrates . In: Seil FJ, editor. Progress in brain research. New York: Elsevier Science Publishers;1994. p. 219-28.
85.
McClellan AD.Spinal cord injury: lessons from locomotor recovery and axonal regeneration in lower vertebrates . THE NEUROSCIENTIST1998;4.250-63.
86.
Zottoh SJ, Freemer MM.Behavioral recovery of the goldfish startle response after spmal cord crush. Soc Neurosci Abstr1991;17:942.
87.
Zottoli SJ, Agostini MA, Danielson PD, Lee EJ, Laidley TL, Mark-stem EA, Scalise TL.Pathway selection by regenerating Mauthner axons of the adult goldfish. Soc Neurosci Abstr1988 ;14.54.
88.
Zottoli SJ, Northern SC, Scalise TL.Regeneration of the goldfish Mauthner cell does not underlie behavioral recovery of the startle response. Soc Neurosci Abstr1989;15:333.
89.
Zottoli SJ, Feiner DG, Hering JR, Faber DS.Behavioral recovery of fast startle responses after spmal cord crush in goldfish can occur in the absence of Mauthner cells. Soc Neurosci Abstr1998;24:309.
90.
Eaton RC, Lavender WA, Wieland CM.Alternative neural pathways initiate fast-start responses following lesions of the Mauthner neuron in goldfish. J Comp Physiol [A]1982;145:485-96.
91.
Zottoli SJ, Newman BC, Rieff HI, Winters DC.Decrease in occurrence of fast startle responses after selective Mauthner cell ablation in goldfish (Carassius auratus. J Comp Physiol [A]1999;184:207-18.
92.
Bentley AP, Zottoli SJ.Central nervous system lesion triggers inappropriate pathway choice in adult vertebrate system. Brain Res1993;630:333-6.
93.
Mayr E.The growth of biological thought diversity, evolution, and inheritance. Cambridge (MA): Belknap Press; 1982.
94.
Meyers JR, Copanas EH, Zottoli SJComparison of fast startle responses between two elongate bony fish with an anguilliform type of locomotion and the implications for the underlying neuronal basis of escape behavior. Brain Behav Evol1998;52:7-22.
95.
Currie SNVibration-evoked startle behavior in larval lampreys. Brain Res1991;37:260-71.
96.
Canfield JG, Rose GJ.Hierarchical sensory guidance of Mauthner-mediated escape responses in goldfish (Carassius auratus) and cichlids (Haplochromis burtoni. Bram Behav Evol1996;48:137-56.
97.
Tnller A, Rostamg P, Korn H, Legendre P.Morphofunctional evidence for mature synaptic contacts on the Mauthner cell of 52-hour-old zebrafish larvae . Neurosci1997;80:133-45.
98.
Hatta K, Korn H.Physiological properties of the Mauthner system in the adult zebrafish. J Comp Neurol1998 ;395:493-509.
99.
David-Watine B, Goblet C, De Saint Jan D , Fucile S, Devignot V, Bregestovski P, Korn H.Cloning, expression and electrophysiological characterization of glycine receptor alpha subunit from zebrafish. Neuroscience1999;90:303-17.
100.
Eaton RC, Farley RD.Development of the Mauthner neurons in embryos and larvae of the zebrafish, Brachydanio rerio Copeia1973 ;4 673-82
101.
Pemado A, Yuste R, Katz L.Extensive dye coupling between rat neocortical neurons during the period of circuit formation. Neuron1993,10:103-14.
102.
Goodman CS, Shatz CJ.Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell1993 ;72:427-37
103.
Kandler K, Katz LR.Neuronal coupling and uncoupling in the developmg nervous systemCurr Opm Neurobiol1995;5:98-105
104.
Dudek FE, Snow RW, Taylor C.Role of electrical interactions in synchronization of epileptiform bursts. Adv Neurol1986;44: 593-617.
105.
Meldrum BS.The role of glutamate in epilepsy and other CNS disorders. Neurology1994;44:S14-S23.
106.
Moshkov DA, Mukhtasimova NF, Pavlik LL, Tiras NR, Pakhotma ID.In vitro long-term potentiation of electrotomc responses of goldfish Mauthner cells is accompanied by ultrastructural changes at afferent mixed synapses . Neuroscience1998; 87:591-605.
107.
Eaton RC, Guzik AL, Casagrand JL.Mauthner system discrimmation of stimulus direction from the acceleration and pressure components at sound onset. Biol Bull1997;192:146-9.
108.
Faber DS, Young WS, Legendre P, Korn H.Intrinsic quantal variability due to stochastic properties of receptor-transmitter m-teractions. Science1992;258:1494-8.
109.
Faure P, Korn H.A nonrandom dynamic component in the synaptic noise of a central neuron. Proc Natl Acad Sci U S A1997; 94:6506-11.
110.
Scott JW, Zottoli SJ, Beatty NP, Korn H.Origin and function of spiral fibers projecting to the goldfish Mauthner cell. J Comp Neurol1994;339:76-90.
111.
Faber DS, Pereda A.Regulation of primary eighth nerve synapses on the Mauthner cell. In: Mendell L, Romo R, Rudomin P, editors Presynaptic inhibition and neural control mechanisms. Oxford University Press, Inc.; 1998. p. 207-27.
