Two Inhibitory Mechanisms in the Mauthner Neurons of Goldfish

Furukawa, Taro; Furshpan, E. J.

doi:10.1152/jn.1963.26.1.140

Cited by 292 publications

(186 citation statements)

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“…Standard surgical procedures were used, and intracellular recordings of the eighth nerve responses were obtained in vivo from the lateral dendrite about 200 to 250 ,um from the M cell soma, generally with a KCl (2.5 M)-containing microelectrode of 7-15 Mfl resistance. In addition, the M cell and its recurrent inhibitory network were activated antidromically through an electrode on the spinal cord (10). EPSPs evoked by stimulation of the contralateral optic tectum (11), which projects to the ventral dendrite of the M cell, were also recorded in some instances.…”

Section: Methodsmentioning

confidence: 99%

“…The eighth nerve test stimulus strength was such that the range of postsynaptic coupling potential amplitudes was about 15-25 mV and the chemical EPSPs were about 5 mV. With these recording conditions, Cl-loading of the M cell did not occur and inhibitory responses were not associated with significant membrane potential changes, since the Cl-equilibrium potential equals the resting membrane potential (10,12).…”

Section: Methodsmentioning

confidence: 99%

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Initial synaptic efficacy influences induction and expression of long-term changes in transmission.

Yang

Faber

1991

Proc. Natl. Acad. Sci. U.S.A.

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Long-term depression (LTD) of glutamatergic and electrotonic transmission can be induced at mixed synapses between eighth nerve fibers and the goldfish Mauth-ner (M) cell in vivo, by pairing weak presynaptic tetani with postsynaptic inhibition. This LTD can be reversed by stronger tetani that produce long-term potentiation (LTP). Moreover, the depression is more likely to occur and tends to last longer when the initial synaptic efficacy is high-that is, if the synaptic strength is first potentiated. In addition, when synaptic efficacy is initially elevated, a weak tetanization that usually results in a gradually developing potentiation instead produces no change in chemical transmission and even a depression of electrotonic coupling. Thus, the modifications in synaptic transmission caused by a certain tetanizing protocol depend upon the history of synaptic efficacy. This last concept provides an experimental basis for theoretical models concerned with pre-and postsynaptic contributions to the regulation of synaptic plasticity.Two opposing forms of activity-dependent modifications of synaptic transmission that are considered to be bases for neural plasticity are long-term potentiation (LTP) (1-4) and long-term depression (LTD) (5-8). One issue of concern has been the identification of conditions which, for the same synaptic connection, differentially favor the induction of one or the other of these alterations. Recently, it was shown that, in visual cortical slices, presynaptic tetani produce either homosynaptic LTD or LTP, depending upon the global level of disinhibition produced pharmacologically or upon the magnitude of postsynaptic depolarization by the tetanus (8). It was also suggested that there are depolarization thresholds for both phenomena, with that for homosynaptic LTD being closer to the resting potential than that for LTP. We provide evidence here for a concept not considered previouslynamely, that the thresholds for the two phenomena might vary with the initial level of synaptic efficacy of the involved connections. Specifically, while studying homosynaptic LTD of both electrotonic coupling and chemical transmission at mixed synapses onto an identified reticulospinal neuron, we found that the amplitude, duration, and sign of long-term changes in synaptic transmission produced by a certain tetanizing protocol depended upon the pretetanization level of efficacy. In addition, it is shown that postsynaptic inhibition is an important factor in induction of LTD in vivo. MATERIALS AND METHODSLTP and LTD have been studied at the monosynaptic connection between eighth nerve fibers and the Mauthner (M) cell in goldfish (Carassius auratus). As shown in Fig. 1A, single afferents have both gap junctions and chemical synapses on the M cell's lateral dendrite. Standard surgical procedures were used, and intracellular recordings of the eighth nerve responses were obtained in vivo from the lateral dendrite about 200 to 250 ,um from the M cell soma, generally with a KCl (2.5 M)-containing microelectrode of ...

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Initial synaptic efficacy influences induction and expression of long-term changes in transmission.

Yang

Faber

1991

Proc. Natl. Acad. Sci. U.S.A.

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“…In the goldfish axon cap FURUKAWA and FURSHPAN (1963) found 'extrinsic hyperpolarizing potentials' following the activation of either one of the pair of M-cells, which inhibited the activation of the M-cell by its hyperpolarizing field effect. They suggest that this potential is partly formed by the tight sealing with the glial cap cell wall and the high electrical resistivity in the axon cap, and that at least a part of the inhibitory potential is mediated by the spiral fibers.…”

Section: Discussionmentioning

confidence: 99%

“…The significance of this structural organization in the inhibitory control of the Mauthner cell activation was discussed. FURUKAWA and FURSHPAN (1963) found a special inhibitory potential formed in the axon cap of the goldfish Mauthner cell (M-cell) immediately after the excitation of this or the other M-cell and proposed that this self and reciprocal inhibition is essential to the function of the teleost M-cell.The axon cap is a special mound-shaped neuropil surrounding the first unmyelinated portion of the axon, the initial segment, of teleostean M-cells. …”

mentioning

confidence: 99%

“…Electron microscopic observations have further elucidated intricate and well organized synaptic distributions in the axon cap (ROBERTSON, BODENHEIMER and STAGE, 1963;KOHNO, 1970;NAKAJIMA, 1974;NAKAJIMA and KOHNO, 1978). Considering the special property of the axonal initial segments as the site of spike initiation in most neurons (ECCLES, 1964;WAXMAN and QUICK, 1978), the unique differentiation of the axon cap neuropil is assumed to be developed for the strong and sure inhibitory control of the teleost M-cell (FURUKAWA and FURSHPAN, 1963;.…”

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Fine structure of the axon initial segment and the axon cap of the mauthner cell in the bullfrog tadpole.

Ito

1980

Arch. Histol. Jap., Arch. Histol. Jpn

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Summary. The axonal initial segment of the Mauthner cell of tadpoles of Rana catesbeiana and its surrounding neuropil, the axon cap, were examined by electron microscopy.The initial segment is almost completely covered by numerous synaptic terminals with profuse clear spherical synaptic vesicles. These synaptic terminals are of one uniform type and are found to be extensions of preterminal swellings, which are filled with accumulated mitochondria and glycogen granules in addition to the synaptic vesicles. Some swellings were shown to have two or more terminals. The synaptic terminals as well as the preterminal swelling are occasionally linked by small synaptic junctions. The significance of this structural organization in the inhibitory control of the Mauthner cell activation was discussed. FURUKAWA and FURSHPAN (1963) found a special inhibitory potential formed in the axon cap of the goldfish Mauthner cell (M-cell) immediately after the excitation of this or the other M-cell and proposed that this self and reciprocal inhibition is essential to the function of the teleost M-cell.The axon cap is a special mound-shaped neuropil surrounding the first unmyelinated portion of the axon, the initial segment, of teleostean M-cells.

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Physiological properties of the mauthner system in the adult zebrafish

Hatta¹,

Korn²

1998

J. Comp. Neurol.

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We investigated the morphological and electrophysiological properties of the Mauthner (M-) cell and its networks in the adult zebrafish (Danio rerio) in comparison with those in the goldfish (Carassius auratus). The zebrafish M-cell has an axon cap, a high resistivity structure which surrounds the initial segment of the M-axon, and accounts for an unusual amplification of the fields generated within and around it. Second, extra- and intracellular recordings were performed with microelectrodes. The resting potential was approximately -80 mV with an input resistance of approximately 0.42 M omega. The M-cell extracellular field was large (10-20 mV), close to the axon hillock, and the latency of antidromic spikes short (approximately 0.4 milliseconds), confirming a high conduction velocity in the M-axon. The extrinsic hyperpolarizing potential (EHP), which signals firing of presynaptic cells and collateral inhibition, was markedly lower at frequencies of spinal stimulation > approximately 5/second, suggesting an organization of the recurrent collateral network similar to that in the goldfish. Inhibitory postsynaptic potentials (IPSPs) were highly voltage-dependent; their decay time constant was increased by depolarizations. The presynaptic neurons which are numerous could be identified by their passive hyperpolarizing potential (PHP) produced by the M-spike current. Auditory responses, mediated via mixed synapses (electrical and chemical), had short delays and hence are well suited to trigger the escape reaction. The similarities of their properties indicate that the wealth of information generated over decades in the goldfish can be extrapolated to the zebrafish.

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Two Inhibitory Mechanisms in the Mauthner Neurons of Goldfish

Cited by 292 publications

References 0 publications

Initial synaptic efficacy influences induction and expression of long-term changes in transmission.

Initial synaptic efficacy influences induction and expression of long-term changes in transmission.

Fine structure of the axon initial segment and the axon cap of the mauthner cell in the bullfrog tadpole.

Physiological properties of the mauthner system in the adult zebrafish

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