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Slow removal of Na⁺ channel inactivation underlies the temporal filtering property in the teleost thalamic neurons

Hidekazu Tsutsui and Yoshitaka Oka

It has been previously shown that the 'large cell' in the corpus glomerulosum (CG) of a teleost brain has a low-pass temporal filtering property. It fires a single spike only in response to temporally sparse synaptic inputs and thus extracts temporal aspects of afferent activities. To explore the ionic mechanisms underlying this property, we quantitatively studied voltage-gated Na⁺ channels of the large cell in the CG slice preparation of the marine filefish by means of whole-cell patch clamp recordings in the voltage-clamp mode. Recorded Na⁺ current was well described using the Hodgkin-Huxley 'm³h' model. It was revealed that the Na⁺ channels have a novel feature: remarkably slow recovery from inactivation. In other words, the time constant for the 'h' gate was extremely large (~100 ms at -80 to -50 mV). In order to test whether the analysed Na⁺ current serves as a mechanism for filtering, the behaviour of the membrane model incorporating the Na⁺ channel was simulated using a computer program called NEURON. In response to current injections, the membrane model displayed low-pass filtering and firing properties similar to those reported in real cells. The present results suggest that slow removal of Na⁺ channel inactivation serves as a crucial mechanism for the low-pass temporal filtering property of the large cell. The simulation study also suggested that velocity and/or amplitude of a spike propagating though an axon expressing Na⁺ channels of this type could potentially be modulated depending on the preceding activities of the cells.

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