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Interaction of nucleus reuniens and entorhinal cortex projections in hippocampal field CA1 of the rat

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Abstract

The nucleus reuniens (RE) and entorhinal cortex (EC) provide monosynaptic excitatory inputs to the apical dendrites of pyramidal cells and to interneurons with dendrites in stratum lacunosum moleculare (LM) of hippocampal field CA1. However, whether the RE and EC inputs interact at the cellular level is unknown. In this electrophysiological in vivo study, low-frequency stimulation was used to selectively activate each projection at its origin; field excitatory postsynaptic potentials (fEPSPs) were recorded in CA1. We applied (1) paired pulses to RE or EC, (2) combined paired pulses to RE and EC, and (3) simultaneously paired pulses to RE/EC. The main findings are that: (a) stimulation of either RE- or EC-evoked subthreshold fEPSPs, displaying paired pulse facilitation (PPF), (b) subthreshold fEPSPs evoked by combined stimulation did not display heterosynaptic PPF, and (c) simultaneous stimulation of RE/EC resulted in enhanced subthreshold fEPSPs in proximal LM displaying a nonlinear interaction. CSD analyses of RE/EC-evoked depth profiles revealed a nonlinear enlargement of the ‘LM sink-radiatum source’ configuration and the appearance of an additional small sink–source pair close to stratum pyramidale, likely reflecting (peri)somatic inhibition. The nonlinear interaction between both inputs indicates that RE and EC axons form synapses, at least partly, onto the same dendritic compartments of CA1 pyramidal cells. We propose that low-frequency activation of the RE-CA1 input facilitates the entorhinal-hippocampal dialogue, and may synchronize the neocortical-hippocampal slow oscillation which is relevant for hippocampal-dependent memory consolidation.

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Acknowledgements

This work was supported by NWA Grant 90-20 from the Graduate School for Neurosciences Amsterdam. We thank A.J.A. Juta for helping with the calculation of the CSDs.

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Authors and Affiliations

  1. Department of Anatomy and Neurosciences, VU University Medical Center, 1081 BT, Amsterdam, The Netherlands

    M. J. Dolleman-van der Weel

  2. Center for Neuroscience, Swammerdam Institute for Life Sciences, University of Amsterdam, 1098 XH, Amsterdam, The Netherlands

    M. J. Dolleman-van der Weel & F. H. Lopes da Silva

  3. Department of Bioengineering, Instituto Superior Técnico, Lisbon Technical University, 1049-001, Lisbon, Portugal

    F. H. Lopes da Silva

  4. Kavli Institute for Systems Neuroscience and Centre for Neural Computation, MTFS, Norwegian University of Science and Technology (NTNU), Postboks 8905, 7491, Trondheim, Norway

    M. P. Witter

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  1. M. J. Dolleman-van der Weel
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  2. F. H. Lopes da Silva
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  3. M. P. Witter
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Correspondence to M. P. Witter.

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Dolleman-van der Weel, M.J., Lopes da Silva, F.H. & Witter, M.P. Interaction of nucleus reuniens and entorhinal cortex projections in hippocampal field CA1 of the rat. Brain Struct Funct 222, 2421–2438 (2017). https://doi.org/10.1007/s00429-016-1350-6

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  • DOI: https://doi.org/10.1007/s00429-016-1350-6

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