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J Neurophysiol 89: 909-921, 2003; doi:10.1152/jn.00573.2002
0022-3077/03 $5.00
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J Neurophysiol (February 1, 2003). 10.1152/jn.00573.2002
Submitted on Submitted 18 July 2002; accepted in final form 29 October 2002

Fast Rhythmic Bursting Can Be Induced in Layer 2/3 Cortical Neurons by Enhancing Persistent Na+ Conductance or by Blocking BK Channels

Roger D. Traub,1 Eberhard H. Buhl,2 Tengis Gloveli,2 and Miles A. Whittington2

 1Departments of Physiology and Pharmacology and Neurology, State University of New York Health Science Center, Brooklyn, New York 11203; and  2Division of Biomedical Sciences, The Worsley Building, University of Leeds, Leeds LS2 9NQ, United Kingdom

Traub, Roger D., Eberhard H. Buhl, Tengis Gloveli, and Miles A. Whittington. Fast Rhythmic Bursting Can Be Induced in Layer 2/3 Cortical Neurons by Enhancing Persistent Na+ Conductance or by Blocking BK Channels. J. Neurophysiol. 89: 909-921, 2003. Fast rhythmic bursting (or "chattering") is a firing pattern exhibited by selected neocortical neurons in cats in vivo and in slices of adult ferret and cat brain. Fast rhythmic bursting (FRB) has been recorded in certain superficial and deep principal neurons and in aspiny presumed local circuit neurons; it can be evoked by depolarizing currents or by sensory stimulation and has been proposed to depend on a persistent gNa that causes spike depolarizing afterpotentials. We constructed a multicompartment 11-conductance model of a layer 2/3 pyramidal neuron, containing apical dendritic calcium-mediated electrogenesis; the model can switch between rhythmic spiking (RS) and FRB modes of firing, with various parameter changes. FRB in this model is favored by enhancing persistent gNa and also by measures that reduce [Ca2+]i or that reduce the conductance of gK(C) (a fast voltage- and Ca2+-dependent conductance). Axonal excitability plays a critical role in generating fast bursts in the model. In vitro experiments in rat layer 2/3 neurons confirmed (as shown previously by others) that RS firing could be switched to fast rhythmic bursting, either by buffering [Ca2+]i or by enhancing persistent gNa. In addition, our experiments confirmed the model prediction that reducing gKC (with iberiotoxin) would favor FRB. During the bursts, fast prepotentials (spikelets) could occur that did not originate in apical dendrites and that appear to derive from the axon. We suggest that modulator-induced regulation of [Ca2+] dynamics or of BK channel conductance, for example via protein kinase A, could play a role in determining the firing pattern of neocortical neurons; specifically, such modulation could play a role in regulating whether neurons respond to strong stimulation with fast rhythmic bursts.




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