Afferent‐specific properties of interneuron synapses underlie selective long‐term regulation of feedback inhibitory circuits in CA1 hippocampus

Croce, Ariane; Pelletier, Joe Guillaume; Tartas, Maylis; Lacaille, Jean‐Claude

doi:10.1113/jphysiol.2010.189316

Cited by 28 publications

(53 citation statements)

References 45 publications

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“…In OA-INs from sham-treated slices, EPSCs (evoked at 2ϫ threshold stimulation intensity) showed inward rectification (Fig. 8A), consistent with previous evidence that synaptic inputs to OA-INs are composed of Ca 2ϩ -permeable non-NMDA receptors (Croce et al, 2010). Moreover, at 24 h after repeated mGluR1 stimulation, EPSCs showed similar inward rectification and the rectification index was not different relative to sham treatment (Fig.…”

Section: Intact Rectification and Nmda/non-nmda Receptor Ratio Duringsupporting

confidence: 89%

CREB-Dependent Transcriptional Control and Quantal Changes in Persistent Long-Term Potentiation in Hippocampal Interneurons

Ran¹,

Laplante²,

Lacaille³

2012

J. Neurosci.

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Mounting evidence indicates an important role of long-term synaptic plasticity in hippocampal inhibitory interneurons in learning and memory. The cellular and molecular mechanisms that underlie such persistent changes in synaptic function in interneurons remain, however, largely undetermined. A transcription-and translation-dependent form of long-term potentiation was uncovered at excitatory synapses onto hippocampal interneurons in oriens-alveus (OA-INs) which is induced by activation of type 1 metabotropic glutamate receptors (cL-LTP mGluR1 ). Here, we use (1) a combination of pharmacological siRNA knock-down and overexpression approaches to reveal the molecular mechanisms of transcriptional control via cAMP response element-binding protein (CREB) during induction, and (2) quantal analysis to identify synaptic changes during maintenance of cL-LTP mGluR1 in rat hippocampus. Induction stimulated CREB phosphorylation in OA-INs via extracellular signal-regulated protein kinase (ERK) signaling. Also, CREB knockdown impaired cL-LTP mGluR1 , whereas CREB overexpression facilitated the induction, demonstrating a necessary and permissive role of CREB via ERK signaling in transcriptional control in cL-LTP mGluR1 . Quantal analysis of synaptic responses during cL-LTP mGluR1 maintenance revealed an increased number of quanta released, corresponding to enhanced transmitter release and a larger quantal size, indicating enhanced responsiveness to individual quanta. Fluctuation analysis of synaptic currents uncovered an increase in conductance and number of functional postsynaptic receptors contributing to single quanta. Our findings indicate that CREB-dependent transcription is a necessary permissive switch for eliciting persistent presynaptic and postsynaptic quantal changes at excitatory synapses in inhibitory local circuits, uncovering cell type-specific coupling of induction and expression mechanisms during persistent synaptic plasticity which may contribute to hippocampal long-term memory processes.

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Section: Intact Rectification and Nmda/non-nmda Receptor Ratio Duringsupporting

confidence: 89%

CREB-Dependent Transcriptional Control and Quantal Changes in Persistent Long-Term Potentiation in Hippocampal Interneurons

Ran¹,

Laplante²,

Lacaille³

2012

J. Neurosci.

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“…O/A INs are dendrite-projecting interneurons consisting mostly of oriens/lacunosum-moleculare (O-LM) cells, but also projection cells with additional subicular, retro-hippocampal or septal projections, as well as bistratified cells [2,6]. O/A INs receive excitatory glutamatergic inputs from CA1 pyramidal cells that express a Hebbian form of LTP [5,7,8]. This LTP depends on the activation of metabotropic glutamate receptor subtype 1a (mGluR1a) and postsynaptic calcium elevation [9,10].…”

Section: Introductionmentioning

confidence: 99%

TRPC1 mediates slow excitatory synaptic transmission in hippocampal oriens/alveus interneurons

et al. 2020

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Hippocampal GABAergic interneurons play key roles in regulating principal cell activity and plasticity. Interneurons located in stratum oriens/alveus (O/A INs) receive excitatory inputs from CA1 pyramidal cells and express a Hebbian form of long-term potentiation (LTP) at their excitatory input synapses. This LTP requires the activation of metabotropic glutamate receptors 1a (mGluR1a) and Ca 2+ entry via transient receptor potential (TRP) channels. However, the type of TRP channels involved in synaptic transmission at these synapses remains largely unknown. Using patch-clamp recordings, we show that slow excitatory postsynaptic currents (EPSCs) evoked in O/A INs are dependent on TRP channels but may be independent of phospholipase C. Using reverse transcription polymerase chain reaction (RT-PCR) we found that mRNA for TRPC 1, 3-7 was present in CA1 hippocampus. Using single-cell RT-PCR, we found expression of mRNA for TRPC 1, 4-7, but not TRPC3, in O/A INs. Using co-immunoprecipitation assays in HEK-293 cell expression system, we found that TRPC1 and TRPC4 interacted with mGluR1a. Coimmunoprecipitation in hippocampus showed that TRPC1 interacted with mGluR1a. Using immunofluorescence, we found that TRPC1 co-localized with mGluR1a in O/A IN dendrites, whereas TRPC4 localization appeared limited to O/A IN cell body. Down-regulation of TRPC1, but not TRPC4, expression in O/A INs using small interfering RNAs prevented slow EPSCs, suggesting that TRPC1 is an obligatory TRPC subunit for these EPSCs. Our findings uncover a functional role of TRPC1 in mGluR1a-mediated slow excitatory synaptic transmission onto O/A INs that could be involved in Hebbian LTP at these synapses.

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“…Particularly interesting are interneurons from the CA1 region, which have their cell body located in the stratum oriens, provide a dendritic inhibition to their pyramidal and interneuron targets and express somatostatin (SOM; also called SST; Tricoire et al, 2011 ; for review, see Freund and Buzsáki, 1996 ; Klausberger and Somogyi, 2008 ; Müller and Remy, 2014 ). Notably, NMDA receptor (NMDAR)-independent LTP, which depends on the type 1a metabotropic glutamate receptor (mGluR1a; Perez et al, 2001 ; Lapointe et al, 2004 ; Le Duigou and Kullmann, 2011 ) and on a postsynaptic Ca 2+ rise from multiple sources ( Topolnik et al, 2006 ; Lamsa et al, 2007 ; Oren et al, 2009 ; Croce et al, 2010 ), has been described in interneurons from the CA1 oriens/alveus region (O/A-IN) and in SOM-expressing interneurons (SOM-INs) from the O/A region ( Szabo et al, 2012 ). Furthermore, LTP occurrence and rules appear to be highly cell-type-specific ( Perez et al, 2001 ; Lamsa et al, 2007 ; Nissen et al, 2010 ; Szabo et al, 2012 ), adding an important level of complexity in our understanding of interneuron diversity.…”

Section: Introductionmentioning

confidence: 99%

Metaplastic Regulation of CA1 Schaffer Collateral Pathway Plasticity by Hebbian MGluR1a-Mediated Plasticity at Excitatory Synapses onto Somatostatin-Expressing Interneurons

Vasuta

Artinian

Laplante

et al. 2015

eneuro

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Cortical GABAergic interneurons represent a highly diverse neuronal type that regulates neural network activity. In particular, interneurons in the hippocampal CA1 oriens/alveus (O/A-INs) area provide feedback dendritic inhibition to local pyramidal cells and express somatostatin (SOM). Under relevant afferent stimulation patterns, they undergo long-term potentiation (LTP) of their excitatory synaptic inputs through multiple induction and expression mechanisms. However, the cell-type specificity of these different forms of LTP and their specific contribution to the dynamic regulation of the CA1 network remain unclear. Here we recorded from SOM-expressing interneurons (SOM-INs) in the O/A region from SOM-Cre-Ai3 transgenic mice in whole-cell patch-clamp. Results indicate that, like in anatomically identified O/A-INs, theta-burst stimulation (TBS) induced a Hebbian form of LTP dependent on metabotropic glutamate receptor type 1a (mGluR1a) in SOM-INs, but not in parvalbumin-expressing interneurons, another mainly nonoverlapping interneuron subtype in CA1. In addition, we demonstrated using field recordings from transgenic mice expressing archaerhodopsin 3 selectively in SOM-INs, that a prior conditioning TBS in O/A, to induce mGluR1a-dependent LTP in SOM-INs, upregulated LTP in the Schaffer collateral pathway of pyramidal cells. This effect was prevented by light-induced hyperpolarization of SOM-INs during TBS, or by application of the mGluR1a antagonist LY367385, indicating a necessity for mGluR1a and SOM-INs activation. These results uncover that SOM-INs perform an activity-dependent metaplastic control on hippocampal CA1 microcircuits in a cell-specific fashion. Our findings provide new insights on the contribution of interneuron synaptic plasticity in the regulation of the hippocampal network activity and mnemonic processes.

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Afferent‐specific properties of interneuron synapses underlie selective long‐term regulation of feedback inhibitory circuits in CA1 hippocampus

Cited by 28 publications

References 45 publications

CREB-Dependent Transcriptional Control and Quantal Changes in Persistent Long-Term Potentiation in Hippocampal Interneurons

CREB-Dependent Transcriptional Control and Quantal Changes in Persistent Long-Term Potentiation in Hippocampal Interneurons

TRPC1 mediates slow excitatory synaptic transmission in hippocampal oriens/alveus interneurons

Metaplastic Regulation of CA1 Schaffer Collateral Pathway Plasticity by Hebbian MGluR1a-Mediated Plasticity at Excitatory Synapses onto Somatostatin-Expressing Interneurons

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