Differences in inhibitory synaptic input between layer II-III and layer V neurons of the cat neocortex.
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1. The goal of this study was to compare the relative effectiveness of intrinsic inhibitory synaptic inputs in different layers of the cat motor cortex. Postsynaptic potentials (PSPs) were evoked in neurons located in the superficial (layer II-III) or deep layers (layer V) by local extracellular stimulation in vitro. Electrophysiological properties and intracellular filling indicated that the recorded neurons were pyramidal cells. 2. The shape and time course of the evoked PSPs differed. Layer II-III cells showed stereotyped triphasic PSPs consisting of a fast excitatory PSP (fEPSP) and a fast and slow inhibitory PSP (fIPSP and sIPSP, respectively). PSPs in layer V cells, in contrast, were much more variable, mainly depolarizing at resting membrane potential, and lacked a hyperpolarizing IPSP in 84% of neurons tested at rest. 3. Blockade of glutaminergic neurotransmission with 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) and D-2-amino-5-phosphonovaleric acid (AP5) revealed that fIPSPs could be evoked in all layer V cells by local stimulation of the superficial or deep layers, even in those that showed small or no IPSPs in control perfusate. Small (< 1 mV) isolated sIPSPs were evoked in only one-fifth of layer V cells when the deep layers were stimulated, and in about one-half of the layer V cells when the superficial layers were stimulated. In layer II-III cells, stimulation of the superficial layers always resulted in fIPSP-sIPSP combinations. No IPSPs could be evoked in layer II-III neurons by stimulating the deep layers after glutaminergic blockade. Selective blockade of gamma-aminobutyric acid-A (GABAA) or GABAB receptor-mediated neurotransmission showed that in both cell types fIPSPs were due to GABAA receptor stimulation, whereas sIPSPs were mediated by GABAB receptors. 4. Isolated fIPSPs were recorded in perfusate containing CNQX, AP5, and the GABAB antagonist CGP 35348. The rise and decay times of the fIPSPs in layer II-III cells were significantly longer than those in layer V cells. Rise and decay times normalized for differences in membrane time constant were not significantly different, however, suggesting that the intrinsic membrane properties of the postsynaptic membrane account for the difference in time course of the fIPSPs in these two cell types. 5. Selective blockade of the inward rectifier current Ih with extracellular Cs+ showed that this conductance functions to shorten and attenuate fIPSPs in layer V cells. In contrast, Ih is absent or small in layer II-III cells, and, consequently, Cs+ had little or no effect on the fIPSPs evoked in these cells.(ABSTRACT TRUNCATED AT 400 WORDS)