The Journal of Neurophysiology Vol. 78 No. 5 November 1997, pp. 2531-2545
Copyright ©1997 The American Physiological Society

GABA_A-Mediated IPSCs in Piriform Cortex Have Fast and Slow Components With Different Properties and Locations on Pyramidal Cells

A. Kapur¹, R. A. Pearce^{1, 2}, W. W. Lytton^{1, 3}, and L. B. Haberly^{1, 4}

¹ Neuroscience Program, ² Department of Anesthesiology, ³ Department of Neurology, and ⁴ Department of Anatomy, University of Wisconsin, Madison, Wisconsin 53706

Kapur, A., R. A. Pearce, W. W. Lytton, and L. B. Haberly.GABA_A-mediated IPSCs in piriform cortex have fast and slow components with different properties and locations on pyramidal cells. J. Neurophysiol. 78: 2531-2545, 1997. A recent study in piriform (olfactory) cortex provided evidence that, as in hippocampus and neocortex, -aminobutyric acid-A (GABA_A)-mediated inhibition is generated in dendrites of pyramidal cells, not just in the somatic region as previously believed. This study examines selected properties of GABA_A inhibitory postsynaptic currents (IPSCs) in dendritic and somatic regions that could provide insight into their functional roles. Pharmacologically isolated GABA_A-mediated IPSCs were studied by whole cell patch recording in slices. To compare properties of IPSCs in distal dendritic and somatic regions, local stimulation was carried out with tungsten microelectrodes, and spatially restricted blockade of GABA_A-mediated inhibition was achieved by pressure-ejection of bicuculline from micropipettes. The results revealed that largely independent circuits generate GABA_A inhibition in distal apical dendritic and somatic regions. With such independence, a selective decrease in dendritic-region inhibition could enhance integrative or plastic processes in dendrites while allowing feedback inhibition in the somatic region to restrain system excitability. This could allow modulatory fiber systems from the basal forebrain or brain stem, for example, to change the functional state of the cortex by altering the excitability of interneurons that mediate dendritic inhibition without increasing the propensity for regenerative bursting in this highly epileptogenic system. As in hippocampus, GABA_A-mediated IPSCs were found to have fast and slow components with time constants of decay on the order of 10 and 40 ms, respectively, at 29°C. Modeling analysis supported physiological evidence that the slow time constant represents a true IPSC component rather than an artifactual slowing of the fast component from voltage clamp of a dendritic current. The results indicated that, whereas both dendritic and somatic-region IPSCs have both fast and slow GABA_A components, there is a greater proportion of the slow component in dendrites. In a companion paper, the hypothesis is explored that the resulting slower time course of the dendritic IPSC increases its capacity to regulate the N-methyl-D-aspartate component of EPSPs. Finally, evidence is presented that the slow GABA_A-mediated IPSC component is regulated by presynaptic GABA_B inhibition whereas the fast is not. Based on the requirement for presynaptic GABA_B-mediated block of inhibition for expression of long-term potentiation, this finding is consistent with participation of the slow GABA_A component in regulation of synaptic plasticity. The lack of susceptibility of the fast GABA_A component to the long-lasting, activity-induced suppression mediated by presynaptic GABA_B receptors is consistent with a protective role for this process in preventing seizure activity.

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