Excitation-Inhibition Dynamics Regulate Activity Transmission Through the Perirhinal–Entorhinal Network

Abstract

The perirhinal (PER) – lateral entorhinal (LEC) network plays a pivotal role in the information transfer between the neocortex and the hippocampus. Anatomical studies have shown that the connectivity is organized bi-directionally: the superficial layers consist of projections running from the neocortex via the PER-LEC network to the hippocampus while the deep layers form the output pathway back to the neocortex. Although these pathways are characterized anatomically, the functional organization of the superficial and deep connections in the PER-LEC network remains to be revealed. We performed paired recordings of superficial and deep layer principal neurons and found that a larger population of superficial neurons responded with action potential firing in response to superficial cortical input, compared to the deep layer population. This suggested that the superficial network can carry information from the cortex towards the hippocampus. The relation between the excitatory and inhibitory input onto the deep and superficial principal neurons showed that the window of net excitability was larger in superficial principal neurons. We performed paired recordings in superficial layer principal neurons and parvalbumin (PV) expressing interneurons to address how this window of opportunity for spiking is affected in superficial principal neurons. The PV interneuron population initiated inhibition at a very consistent timing with increasing stimulus intensity, whereas the excitation temporally shifted to ensure action potential firing. These data indicate that superficial principal neurons can transmit cortical synaptic input through the PER-LEC network because these neurons have a favorable window of opportunity for spiking in contrast to deep neurons.