Elsevier

Neuroscience

Volume 115, Issue 4, 16 December 2002, Pages 1127-1138
Neuroscience

The role of Ca2+-dependent cationic current in generating gamma frequency rhythmic bursts: modeling study

https://doi.org/10.1016/S0306-4522(02)00537-7Get rights and content

Abstract

Fast rhythmic bursting pyramidal neuron or chattering neuron is a promising candidate for the pacemaker of coherent gamma-band (25–70 Hz) cortical oscillation. It, however, still remains to be clarified how the neuron generates such high-frequency bursts. Here, we demonstrate in a single-compartment model neuron that the fast rhythmic bursts (FRBs) can be achieved through Ca2+-activated channels in the entire gamma frequency range.

In a previous in vitro study, a subset of rat cortical pyramidal cells displayed a long-lasting depolarizing afterpotential (DAP) following a plateau-type action potential when K+ conductances were suppressed with Cs+, and this DAP was found to be mediated by a Ca2+-dependent cationic current. This current appeared also suitable for producing a hump-like DAP, a characteristic of the chattering neurons, because of its reversal potential being approximately −40 mV. In the present theoretical study, we show that the enhancement of such a DAP leads to generation of doublet/triplet spikes seen during FRBs. The firing pattern during FRBs is primarily determined by a Ca2+-dependent cationic current and a small-conductance Ca2+-dependent potassium current, which are differentially activated by a biphasically decaying Ca2+ transient produced by fast buffering and a slow pump extrusion after each spike.

With varying intensities of injected current pulses, the interburst frequencies of the FRBs range over the entire gamma frequency band (25–70 Hz) in our model, while the intraburst frequencies remain higher than 300 Hz. Our model suggests that FRBs are essentially generated in the soma, unlike the model based on a persistent sodium current, and that the alteration of Ca2+ sensitivity of Ca2+-dependent cationic current plays an essential role in controlling the FRB pattern.

Section snippets

Experimental procedures

Our model of the FRB neuron has a single compartment, in which only ionic currents essential to generate FRBs are included. The membrane potential V obeys the current–balance equation CmdVdt=−INa−IK−ICa−Icat−ISK−Ileak+Iappwhere the membrane capacitance Cm=1 μF/cm2 and Iapp is an applied current. The leak current is given by Ileak=gleak(VEleak) with gleak=0.13 mS/cm2 and Eleak=−68.8 mV. The permeability ratio for the leak current is PK:PNa:PCl=1:0.04:0.45. The voltage-dependent currents INa, IK

Generation of hump-like DAPs and epileptiform bursts

In response to a short current pulse, the model neuron displays an action potential followed by a hump-like DAP (Fig. 2A). This DAP is similar to those seen in the previous electrophysiological studies (Kang and Kayano, 1994, Gray and McCormick, 1996, Brumberg et al., 2000, Kang, 1997, Haj-Dahmane and Andrade, 1997). The amplitude or the peak level of the DAP is determined independently by the following three parameters: the reversal potential for Icat (Ecat), the maximum conductance (gcat) and

INaP-based model vs. Icat-based model

A previous simulation study proposed that the gamma-band FRB was primarily generated, without Ca2+-activated channels, by a ‘ping-pong’ interplay between action potentials in the somatic compartment and INaP in the dendritic compartment (Wang, 1999). In such a two-compartment model neuron, the somatic action potential propagated backward into the dendrite to activate INaP, which in turn generated a DAP and led to the generation of bursts. The bursting pattern of the model neuron was determined

Acknowledgements

This work was supported by a Grant-in-Aid for Scientific Research on Priority Areas (A) and by CREST (Core Research for Evolutional Science and Technology) of Japan Science and Technology (JST).

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