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Key points

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    Parvalbumin-expressing interneurons represent a major source of inhibition of CA1 hippocampal principal cells and influence both spike timing precision and network oscillations.
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    These interneurons receive both feed-forward and feedback excitatory inputs which recruit them in the hippocampal network.
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    In this study, we compared the functional properties of these two inputs and how they may be modified by neuronal activity.
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    We show that calcium-permeable AMPA receptors and NMDA receptors are differentially distributed at feed-forward versus feedback inputs and act as coincidence detectors of opposing modalities.
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    Our results reveal that the two major excitatory inputs onto CA1 parvalbumin-expressing interneurons undergo long term plasticity with different frequency regimes of afferent activity, which is likely to influence their function under both normal and pathological conditions.

Abstract  Hippocampal parvalbumin-expressing interneurons (PV INs) provide fast and reliable GABAergic signalling to principal cells and orchestrate hippocampal ensemble activities. Precise coordination of principal cell activity by PV INs relies in part on the efficacy of excitatory afferents that recruit them in the hippocampal network. Feed-forward (FF) inputs in particular from Schaffer collaterals influence spike timing precision in CA1 principal cells whereas local feedback (FB) inputs may contribute to pacemaker activities. Although PV INs have been shown to undergo activity-dependent long term plasticity, how both inputs are modulated during principal cell firing is unknown. Here we show that FF and FB synapses onto PV INs are endowed with distinct postsynaptic glutamate receptors which set opposing long-term plasticity rules. Inward-rectifying AMPA receptors (AMPARs) expressed at both FF and FB inputs mediate a form of anti-Hebbian long term potentiation (LTP), relying on coincident membrane hyperpolarization and synaptic activation. In contrast, FF inputs are largely devoid of NMDA receptors (NMDARs) which are more abundant at FB afferents and confer on them an additional form of LTP with Hebbian properties. Both forms of LTP are expressed with no apparent change in presynaptic function. The specific endowment of FF and FB inputs with distinct coincidence detectors allow them to be differentially tuned upon high frequency afferent activity. Thus, high frequency (>20 Hz) stimulation specifically potentiates FB, but not FF afferents. We propose that these differential, input-specific learning rules may allow PV INs to adapt to changes in hippocampal activity while preserving their precisely timed, clockwork operation.