Characterization of cholinergic and noradrenergic slow excitatory postsynaptic potentials from rat cerebral cortical neurons

Abstract

Intracellular recordings from layer V pyramidal neurons in rat somatosensory neocortical slices were used to investigate the effects of electrically stimulating slices known to contain cholinergic and noradrenergic fibers. Repetitive electrical stimulation ventral to the recording site elicited a series of fast excitatory postsynaptic potentials followed by an inhibitory postsynaptic potential. These potentials were followed by a slow excitatory postsynaptic potential that lasted up to tens of seconds. The slow excitatory postsynaptic potential was more prominent when neurons were depolarized to 5-10 mV below firing threshold and was associated with increased input resistance and generated action potentials. The slow excitatory postsynaptic potential increased the amplitude of membrane potential oscillations and blocked the slow afterhyperpolarization which followed trains of action potentials. The amplitude of the slow excitatory postsynaptic potential was sensitive to extracellular potassium concentration. Blockade of postsynaptic action potentials by QX-314 did not block slow excitatory postsynaptic potentials. Exposure of slices to tetrodotoxin did block slow excitatory postsynaptic potentials, indicating they were dependent on propagated action potentials. Application of antagonists of glutamate and fast GABA responses failed to block slow excitatory postsynaptic potentials. Exposure to atropine or either propranolol or atenolol partially antagonized slow excitatory postsynaptic potentials, but only when atropine was added in combination with one of the other agents was the slow excitatory postsynaptic potential completely blocked. Exposure of slices to eserine, imipramine, or cocaine enhanced slow excitatory postsynaptic potentials. It is concluded that the slow excitatory postsynaptic potential triggered in neocortical slices is a composite of a cholinergic and a noradrenergic slow excitatory postsynaptic potential, and these potentials are capable of altering the firing properties of neurons for tens of seconds.