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Synaptically Recruited Apical Currents Are Required to Initiate Axonal and Apical Spikes in Hippocampal Pyramidal Cells: Modulation by Inhibition

Experimental and Computational Neurophysiology Unit, Servicio Histología, Hospital Ramón y Cajal, Madrid, Spain

Submitted 6 July 2004; accepted in final form 26 September 2004

Dendritic voltage-dependent currents and inhibition modulate the information flow between synaptic and decision areas. Subthreshold and spike currents are sequentially recruited by synaptic potentials in the apical shaft of pyramidal cells, which may also decide cell output. We studied the global role of proximal apical recruited currents on cell output in vitro and in the anesthetized rat after local blockade of Na⁺ currents in the axon initial segment (AIS) or the proximal apical shaft and their modulation by inhibition. Microejection of TTX, field potentials, and intrasomatic and intradendritic recordings were employed. Dendritic population spikes (PSs) were much smaller in vitro, but the gross relations between synaptic and active currents are similar to in vivo. Activation of Schaffer collaterals triggered PSs and action potentials (APs) in the apical shaft that fully propagated to the axon. However, the specific blockade of proximal Na⁺ currents avoided cell firing, although antidromic PSs and APs readily invaded somata. The somatic depolarization of subthreshold excitatory postsynaptic potentials (EPSPs) also decreased to about 50%. These results were not due to decreased excitatory input by TTX. However, when GABA_A inhibition was locally removed, Schaffer synaptic currents skipped the proximal dendrite and fired somatic PSs, although initiated at the AIS. It is concluded that apical currents recruited en passant by Schaffer synaptic potentials in the apical shaft constitute a necessary amplifier for this input to cause output decision. Local inhibition decides when and where an AP will initiate, constituting an efficient mechanism to discriminate and weight different inputs.

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