Synapse-specific mGluR1-dependent long-term potentiation in interneurones regulates mouse hippocampal inhibition

Hippocampal CA1 inhibitory interneurones control the excitability and synchronization of pyramidal cells, and participate in hippocampal synaptic plasticity. Pairing theta-burst stimulation (TBS) with postsynaptic depolarization, we induced long-term potentiation (LTP) of putative single-fibre excitatory postsynaptic currents (EPSCs) in stratum oriens/alveus (O/A) interneurones of mouse hippocampal slices. UP induction was absent in metabotropic glutamate receptor I (mGluR1) knockout mice, was correlated with the postsynaptic presence of mGluR1 a, and required a postsynaptic Ca2+ rise. Changes in paired-pulse facilitation and coefficient of variation indicated that UP expression involved presynaptic mechanisms. UP was synapse specific, occurring selectively at synapses modulated by presynaptic group 11, but not group 111, mGluRs. Furthermore, the TBS protocol applied in O/A induced a long-term increase of polysynaptic inhibitory responses in CA1 pyramidal cells, that was absent in mGluR1 knockout mice. These results uncover the mechanisms of a novel form of interneurone synaptic plasticity that can adaptively regulate inhibition of hippocampal pyramidal cells.