Background synaptic activity in rat entorhinal cortex shows a progressively greater dominance of inhibition over excitation from deep to superficial layers

Jones, Roland Spencer Gwynne; Greenhill, Stuart David; Chamberlain, Sophie Elizabeth Lyn; Lench, Alex; Massey, Peter Vernon; Yuill, Kathryn Heather; Woodhall, Gavin Lawrence; Spencer, Roland; Dickson, Clayton T

Abstract

The entorhinal cortex (EC) controls hippocampal input and output, playing major roles in memory and spatial navigation. Different layers of the EC subserve different functions and a number of studies have compared properties of neurones across layers. We have studied synaptic inhibition and excitation in EC neurones, and we have previously compared spontaneous synaptic release of glutamate and GABA using patch clamp recordings of synaptic currents in principal neurones of layers II (L2) and V (L5). Here, we add comparative studies in layer III (L3). Such studies essentially look at neuronal activity from a presynaptic viewpoint. To correlate this with the postsynaptic consequences of spontaneous transmitter release, we have determined global postsynaptic conductances mediated by the two transmitters, using a method to estimate conductances from membrane potential fluctuations. We have previously presented some of this data for L3 and now extend to L2 and L5. Inhibition dominates excitation in all layers but the ratio follows a clear rank order (highest to lowest) of L2>L3>L5. The variance of the background conductances was markedly higher for excitation and inhibition in L2 compared to L3 or L5. We also show that induction of synchronized network epileptiform activity by blockade of GABA inhibition reveals a relative reluctance of L2 to participate in such activity. This was associated with maintenance of a dominant background inhibition in L2, whereas in L3 and L5 the absolute level of inhibition fell below that of excitation, coincident with the appearance of synchronized discharges. Further experiments identified potential roles for competition for bicuculline by ambient GABA at the GABAA receptor, and strychnine-sensitive glycine receptors in residual inhibition in L2. We discuss our results in terms of control of excitability in neuronal subpopulations of EC neurones and what these may suggest for their functional roles. © 2014 Greenhill et al.

Citation

Jones, R. S. G., Greenhill, S. D., Chamberlain, S. E. L., Lench, A., Massey, P. V., Yuill, K. H., …Dickson, C. T. (2014). Background synaptic activity in rat entorhinal cortex shows a progressively greater dominance of inhibition over excitation from deep to superficial layers. PLoS ONE, 9(1), Article e85125. https://doi.org/10.1371/journal.pone.0085125

• Journal Article Type: Article
• Acceptance Date: Nov 22, 2013
• Publication Date: Jan 15, 2014
• Deposit Date: Jul 1, 2019
• Publicly Available Date: Jul 1, 2019
• Journal: PLoS ONE
• Electronic ISSN: 1932-6203
• Publisher: Public Library of Science
• Peer Reviewed: Peer Reviewed
• Volume: 9
• Issue: 1
• Article Number: e85125
• DOI: https://doi.org/10.1371/journal.pone.0085125
• Public URL: https://uwe-repository.worktribe.com/output/1467156
• Publisher URL: https://doi.org/10.1371/journal.pone.0085125