Slow inhibitory potentials in the teleost Mauthner cell

In vivo recordings from Mauthner cells in adult zebrafish (Danio rerio) and goldfish (Carassius auratus) preparations with potassium chloride filled e lectrodes revealed a new class of long-lasting synaptic events in these cel ls. Their decay time constant ranged from 20 to 80 ms, which is about 20 ti mes longer than that of previously identified fast glycinergic inhibitory p ostsynaptic potentials in this neuron. The average time to peak of these sl ow events ranged from 1 to 6 ms. We demonstrated that they are also inhibit ory since (i) they were resistant to antagonists of the excitatory glutamat ergic receptors; (ii) their amplitude was increased following chloride load ing of the Mauthner cell; (iii) their reversal potential was the same as th at of fast, glycinergic inhibitory postsynaptic potentials; and (iv) they p roduced an inhibitory shunt of the cell's membrane resistance. Furthermore, as with the fast inhibitory postsynaptic potentials, the decay time of the slow events is voltage dependent, increasing when the Mauthner cell is dep olarized. However, these inhibitory post synaptic potentials had a differen t pharmacological profile to the fast glycinergic ones. That is, they persi sted in the presence of strychnine at doses that abolished the fast ones an d they were more sensitive to bicuculline. These data are compatible with t he notion that these inhibitory postsynaptic potentials are mediated by act ivation of a different inhibitory receptor type, and may be GABAergic. In a ddition, the decay time constant of the fast inhibitory postsynaptic curren t was shorter than the first of the two components that contribute to the b i-exponential decay reported previously for miniature inhibitory postsynapt ic currents in Mauthner cells of larval zebrafish. This suggests developmen tal modifications and/or a switch in the assembly of glycine receptor subty pes. While amplitude distributions of the fast miniature inhibitory postsyn aptic potentials recorded in the presence of tetrodotoxin generally could f it with a single Gaussian function, the amplitude histograms of slow miniat ure events were skewed, often with multiple nearly equally spaced peaks, co nsistent with the synchronous release of several quantal units. These previ ously undescribed slow unitary inhibitory postsynaptic potentials contribut e to inhibitory synaptic noise recorded in the Mauthner cells. Specifically , autocorrelation analysis revealed gamma-like rhythms (30-80 Hz) in each o f two phases, characterized as ''noisy" and "quiet", and dominated by the f ast and slow inhibitory postsynaptic potentials, respectively. The major fr equencies of these two states were significantly different (i.e. around 90 and 40 Hz, respectively), suggesting that the fast and slow inhibitory post synaptic potentials are derived from different inhibitory networks. Chlorid e-filled Mauthner cells gradually hyperpolarized in the presence of tetrodo toxin, reflecting the effect of ongoing activity in the interneurons that p roduce the slow events. We conclude that this new class of inhibitory postsynaptic potentials contr ibutes to the tonic inhibition which controls the Mauthner cell's excitabil ity. In physiological conditions, this regulatory influence is expressed as a continuous shunt of this neuron's input resistance and responsiveness to sensory inputs. (C) 2001 IBRO. Published by Elsevier Science Ltd. All righ ts reserved.