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

Abstract

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.