Functional differences in Na⁺ channel gating between fast-spiking interneurones and principal neurones of rat hippocampus

1. GABAergic interneurones differ from glutamatergic principal neurones in their ability to discharge high-frequency trains of action potentials without adaptation. To examine whether Na⁺ channel gating contributed to these differences, Na⁺ currents were recorded in nucleated patches from interneurones (dentate gyrus basket cells, BCs) and principal neurones (CA1 pyramidal cells, PCs) of rat hippocampal slices. 2. The voltage dependence of Na⁺ channel activation in BCs and PCs was similar. The slope factors of the activation curves, fitted with Boltzmann functions raised to the third power, were 11.5 and 11.8 mV, and the mid-point potentials were -25.1 and -23.9 mV, respectively. 3. Whereas the time course of Na⁺ channel activation (-30 to +40 mV) was similar, the deactivation kinetics (-100 to -40 mV) were faster in BCs than in PCs (tail current decay time constants, 0.13 and 0.20 ms, respectively, at -40 mV). 4. Na⁺ channels in BCs and PCs differed in the voltage dependence of inactivation. The slope factors of the steady-state inactivation curves fitted with Boltzmann functions were 6.7 and 10.7 mV, and the mid-point potentials were -58.3 and -62.9 mV, respectively. 5. The onset of Na⁺ channel inactivation at -55 mV was slower in BC's than in PCs; the inactivation time constants were 18.6 and 9.3 ms, respectively. At more positive potentials the differences in inactivation onset were smaller. 6. The time course of recovery of Na⁺ channels from inactivation induced by a 30 ms pulse was fast and mono-exponential (τ = 2.0 ms at -120 mV) in BCs, whereas it was slower and biexponential in PCs (τ₁ = 2.0 ms and τ₂ = 133 ms; amplitude contribution of the slow component, 15%). 7. We conclude that Na⁺ channels of BCs and PCs differ in gating properties that contribute to the characteristic action potential patterns of the two types of neurones.