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Long-term potentiation of the nucleus reuniens and entorhinal cortex to CA1 distal dendritic synapses in mice

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Abstract

The present study investigated the short-term and long-term synaptic plasticity of excitatory synapses formed by the nucleus reuniens (RE) and entorhinal cortex (EC) on the distal apical dendrites of CA1 pyramidal cells. RE-CA1 synapses are implicated in memory involving the hippocampus and medial prefrontal cortex. Current source density (CSD) analysis was used to identify excitatory and inhibitory currents following stimulation of RE or medial perforant path (MPP) in urethane-anesthetized mice in vivo. At the distal apical dendrites, RE evoked an initial excitatory sink followed by inhibitory sources at short (~ 30 ms) and long (150–200 ms) latencies, and often showing gamma (25–40 Hz) oscillations. Both RE-evoked and spontaneous gamma-frequency local field potentials displayed the same CSD depth profile. Paired-pulse facilitation (PPF) of the distal excitatory sink at 20–200 ms interpulse intervals was observed following RE stimulation, generally higher than that following MPP stimulation. Theta-frequency burst stimulation (TBS) of RE induced input-specific long-term potentiation (LTP) at the distal dendritic CA1 synapses, accompanied by reduction of PPF. After TBS of the MPP, the MPP-CA1 distal dendritic synapse could manifest LTP or long-term depression, but the non-tetanized RE-CA1 synapse was typically potentiated. Heterosynaptic potentiation of the RE to CA1 distal synapses may occur after repeated activity of EC afferents, or spread of MPP stimulus currents to coursing RE afferents. The results indicate a propensity of RE-CA1 distal excitatory synapses to show PPF, LTP and gamma oscillations, all of which may participate in memory processing by RE and EC.

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Fig. 1

source density (CSD) time transients following stimulation of the nucleus reuniens (RE) or medial perforant path (MPP). a Thionin-stained sections showing location of stimulating electrode (after lesion) at the RE (leftmost) and medial part of the angular bundle (AB, rightmost) to activate the MPP; recording probe was inserted into CA1a near the subiculum (sub). b Schematic CA1 pyramidal cell and dentate gyrus granule cell (left), showing AEPs (n = 24 sweeps) and CSDs folliwng stimulation of RE at 300 µA, at 1.5 × threshold intensity (columns 1 and 2), or MPP stimulation at 60 µA, at 2 × threshold intensity (columns 3 and 4). Excitation of the distal apical dendrites was characterized by negative potentials (and current sinks) at stratum lacunosum-moleculare (SLM) and positive potentials (and current sources) at stratum radiatum (RAD). Other layers are: OR stratum oriens, PYR stratum pyramidale, MML middle molecular layer, GCL granule cell layer. Filled circle indicates stimulus artifact

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source appeared together with large MML sinks. b MPP evoked average CSD profiles in 30-min time blocks, at 10.4 ms latency. There was little potentiation of the MPP-evoked CSDs in CA1, but potentiation in the DG, maximal sinks at MML, was observed. c Time course of E1 slope and E1 peak measures of the MPP to CA1 SLM sink, and E1 peak measure of the MPP to DG MML sink

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Acknowledgements

We thank the laboratory of Vania and Marco Prado for the supply of mice, and L. Chiu for technical support.

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Funded by operating Grants from the Canadian Natural Sciences and Engineering Research Council (1037-2013) and Canadian Institutes of Health Research (CIHR) MOP-15685 (to LSL).

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  1. Graduate Program in Neuroscience, The University of Western Ontario, London, ON, N6A5C1, Canada

    Thyna Vu, Radu Gugustea & L. Stan Leung

  2. Department of Physiology and Pharmacology, The University of Western Ontario, London, ON, N6A5C1, Canada

    Thyna Vu, Radu Gugustea & L. Stan Leung

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Vu, T., Gugustea, R. & Leung, L.S. Long-term potentiation of the nucleus reuniens and entorhinal cortex to CA1 distal dendritic synapses in mice. Brain Struct Funct 225, 1817–1838 (2020). https://doi.org/10.1007/s00429-020-02095-6

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