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. LTP induction was absent in metabotropic glutamate receptor 1 (mGluR1) knockout mice, was correlated with the postsynaptic presence of mGluR1a, and required a postsynaptic Ca2+ rise. Changes in paired‐pulse facilitation and coefficient of variation indicated that LTP expression involved presynaptic mechanisms. LTP was synapse specific, occurring selectively at synapses modulated by presynaptic group II, but not group III, 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.

[1]  K. Tóth,et al.  Differential Mechanisms of Transmission at Three Types of Mossy Fiber Synapse , 2000, The Journal of Neuroscience.

[2]  K. Reymann,et al.  Interaction between paired-pulse facilitation and long-term potentiation of minimal excitatory postsynaptic potentials in rat hippocampal slices: A patch-clamp study , 1998, Neuroscience.

[3]  Morten Raastad,et al.  Extracellular Activation of Unitary Excitatory Synapses Between Hippocampal CA3 and CA1 Pyramidal Cells , 1995, The European journal of neuroscience.

[4]  R. Nicoll,et al.  Contrasting properties of two forms of long-term potentiation in the hippocampus , 1995, Nature.

[5]  C. Stevens,et al.  Changes in reliability of synaptic function as a mechanism for plasticity , 1994, Nature.

[6]  D. Winder,et al.  Differential involvement of group II and group III mGluRs as autoreceptors at lateral and medial perforant path synapses. , 1996, Journal of neurophysiology.

[7]  G. Buzsáki,et al.  Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks , 1995, Current Opinion in Neurobiology.

[8]  K. Tóth,et al.  Afferent-specific innervation of two distinct AMPA receptor subtypes on single hippocampal interneurons , 1998, Nature Neuroscience.

[9]  G. Buzsáki,et al.  Interneurons of the hippocampus , 1998, Hippocampus.

[10]  R. Nicoll,et al.  Modulation of synaptic transmission and long-term potentiation: effects on paired pulse facilitation and EPSC variance in the CA1 region of the hippocampus. , 1993, Journal of neurophysiology.

[11]  R. S. Jones,et al.  Differential actions of PKA and PKC in the regulation of glutamate release by group III mGluRs in the entorhinal cortex. , 2001, Journal of neurophysiology.

[12]  H. Shinozaki,et al.  Activation of metabotropic glutamate receptor type 2/3 suppresses transmission at rat hippocampal mossy fibre synapses. , 1996, The Journal of physiology.

[13]  M. Hasselmo,et al.  NMDA-dependent modulation of CA1 local circuit inhibition , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  Ayae Kinoshita,et al.  Differential Presynaptic Localization of Metabotropic Glutamate Receptor Subtypes in the Rat Hippocampus , 1997, The Journal of Neuroscience.

[15]  R. Tsien,et al.  Chapter 18: Long-term potentiation: postsynaptic activation of Ca2+-dependent protein kinases with subsequent presynaptic enhancement , 1991 .

[16]  J. Lacaille,et al.  Membrane potential and intracellular Ca2+ oscillations activated by mGluRs in hippocampal stratum oriens/alveus interneurons. , 1999, Journal of neurophysiology.

[17]  R. Dingledine,et al.  Long-term depression in hippocampal interneurons: joint requirement for pre- and postsynaptic events. , 1999, Science.

[18]  J. Lacaille,et al.  Local circuit interactions between oriens/alveus interneurons and CA1 pyramidal cells in hippocampal slices: electrophysiology and morphology , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  P. Jonas,et al.  PTP and LTP at a hippocampal mossy fiber-interneuron synapse , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[20]  R. Nicoll,et al.  Long-term potentiation--a decade of progress? , 1999, Science.

[21]  T. Freund,et al.  Synaptic Input of Horizontal Interneurons in Stratum Oriens of the Hippocampal CA1 Subfield: Structural Basis of Feed‐back Activation , 1995, The European journal of neuroscience.

[22]  Roger D. Traub,et al.  Self-Organized Synaptic Plasticity Contributes to the Shaping of γ and β Oscillations In Vitro , 2001, The Journal of Neuroscience.

[23]  R. Traub,et al.  Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation , 1995, Nature.

[24]  K. Tóth,et al.  Target‐specific expression of pre‐ and postsynaptic mechanisms , 2000, The Journal of physiology.

[25]  A. Thomson,et al.  Facilitating pyramid to horizontal oriens‐alveus interneurone inputs: dual intracellular recordings in slices of rat hippocampus , 1998, The Journal of physiology.

[26]  R. Nicoll,et al.  Pharmacology of metabotropic glutamate receptors at the mossy fiber synapses of the guinea pig hippocampus , 1995, Neuropharmacology.

[27]  G. Buzsáki,et al.  Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  P. Somogyi,et al.  The metabotropic glutamate receptor (mGluRlα) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction , 1993, Neuron.

[29]  R. Petralia,et al.  The metabotropic glutamate receptors, MGLUR2 and MGLUR3, show unique postsynaptic, presynaptic and glial localizations , 1996, Neuroscience.

[30]  I. Soltesz,et al.  Long-term plasticity in interneurons of the dentate gyrus , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[31]  S. Redman,et al.  Long-term plasticity at excitatory synapses on aspinous interneurons in area CA1 lacks synaptic specificity. , 1998, Journal of neurophysiology.

[32]  J. Lacaille,et al.  Mechanisms of selective long-term potentiation of excitatory synapses in stratum oriens/alveus interneurons of rat hippocampal slices. , 1995, Journal of neurophysiology.

[33]  T. Bliss,et al.  A synaptic model of memory: long-term potentiation in the hippocampus , 1993, Nature.

[34]  J. Lacaille,et al.  A hebbian form of long-term potentiation dependent on mGluR1a in hippocampal inhibitory interneurons , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Chris J. McBain,et al.  Glutamatergic synapses onto hippocampal interneurons: precision timing without lasting plasticity , 1999, Trends in Neurosciences.

[36]  R. Malinow,et al.  Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice , 1995, Nature.

[37]  G. Collingridge,et al.  Motor deficit and impairment of synaptic plasticity in mice lacking mGluR1 , 1994, Nature.

[38]  J. Isaac,et al.  Evidence for silent synapses: Implications for the expression of LTP , 1995, Neuron.

[39]  J. Kauer,et al.  Hippocampal Interneurons Express a Novel Form of Synaptic Plasticity , 1997, Neuron.

[40]  R Lujan,et al.  Perisynaptic Location of Metabotropic Glutamate Receptors mGluR1 and mGluR5 on Dendrites and Dendritic Spines in the Rat Hippocampus , 1996, The European journal of neuroscience.

[41]  J. Lacaille,et al.  Synaptically activated calcium responses in dendrites of hippocampal oriens-alveus interneurons. , 2001, Journal of neurophysiology.