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

Stuart D. Greenhill, Sophie E.L. Chamberlain, Alex Lench, Peter V. Massey, Kathryn H. Yuill, Gavin L. Woodhall, Roland S.G. Jones

Research output: Contribution to journalArticle

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.

Original languageEnglish
Article numbere85125
Number of pages16
JournalPLoS ONE
Volume9
Issue number1
DOIs
Publication statusPublished - 15 Jan 2014

Fingerprint

Entorhinal Cortex
Neurons
Rats
cortex
neurons
gamma-Aminobutyric Acid
rats
Transmitters
strychnine
Glycine Receptors
Strychnine
Bicuculline
Clamping devices
GABA-A Receptors
membrane potential
glutamates
Glutamic Acid
Navigation
Membranes
Data storage equipment

Bibliographical note

© 2014 Greenhill et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding: NC3Rs (Grant Number G1000059; http://www.nc3rs.org.uk/); MRC, University of Bath and BBSRC for three studentships.

Cite this

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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. {\circledC} 2014 Greenhill et al.",
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Background synaptic activity in rat entorhinal cortex shows a progressively greater dominance of inhibition over excitation from deep to superficial layers. / Greenhill, Stuart D.; Chamberlain, Sophie E.L.; Lench, Alex; Massey, Peter V.; Yuill, Kathryn H.; Woodhall, Gavin L.; Jones, Roland S.G.

In: PLoS ONE, Vol. 9, No. 1, e85125, 15.01.2014.

Research output: Contribution to journalArticle

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T1 - Background synaptic activity in rat entorhinal cortex shows a progressively greater dominance of inhibition over excitation from deep to superficial layers

AU - Greenhill, Stuart D.

AU - Chamberlain, Sophie E.L.

AU - Lench, Alex

AU - Massey, Peter V.

AU - Yuill, Kathryn H.

AU - Woodhall, Gavin L.

AU - Jones, Roland S.G.

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