Disinhibition in learning and memory circuits: New vistas for somatostatin interneurons and long-term synaptic plasticity

Artinian, Julien; Lacaille, Jean‐Claude

doi:10.1016/j.brainresbull.2017.11.012

Cited by 59 publications

(56 citation statements)

References 65 publications

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“…Given our evidence of the role of TRPC1 in excitatory synaptic transmission in inhibitory interneurons, it is interesting to speculate that some of these synaptic and behavioural effects may involve TRPCs in inhibitory neurons, possibly O/A interneurons. Hebbian mGluR1a-mediated LTP at excitatory synapses onto O/A INs, and more specifically onto interneurons that express somatostatin (SOM INs), was shown to upregulate persistently LTP magnitude at Schaffer collateral-CA1 pyramidal cell synapses via a disinhibition mechanism [5,11,75,76]. Moreover, impairing mGluR1a-mediated LTP by interfering with mTORC1 function specifically in somatostatin interneurons impairs hippocampal spatial and contextual fear memory consolidation [11,77,78].…”

Section: Functional Implicationsmentioning

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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Section: Functional Implicationsmentioning

confidence: 99%

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

et al. 2020

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“…The CCTinduced circuit modification includes increased MPP-supraDG synaptic efficacy, coincident with persistently increased PKMζ expression and local MMP-evoked disinhibition of the response that is coincident with increased PKMζ expression in SST+ interneurons (Figs. 3,4), known to mediate disinhibition 31 . These functional subcircuit changes are accompanied by upregulation of PKMζ persisting at least a week in SST+ cells, that may be HIPP cells that can mediate both widespread inhibition of granule cells and local excitation of granule cells via plastic disinhibition of inhibitory neurons such as MOPP (molecular layer perforant path projecting) cells, but this has not been investigated 24,25 .…”

Section: A Neocortical-hippocampal Subcircuit Tuned By Cognitive Traimentioning

confidence: 99%

Learning to learn persistently modifies an entorhinal-hippocampal excitatory-inhibitory subcircuit

Chung

Jou

Grau‐Perales

et al. 2019

Preprint

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SUMMARYThe neurobiology of psychological concepts like schema, and psychotherapeutic strategies of cognitive behavioral therapy (CBT) is poorly understood, partly because learning to process information confounds, and is rarely distinguished from acquiring content-specific memory. Learning to learn changes one’s overall information-processing ability, whereas neurobiological investigations typically focus on memory for content from particular experiences. We investigated entorhinal cortex-to-dentate gyrus neural circuit changes while mice learn to learn during cognitive control training (CCT) to judiciously use and ignore information. CCT changes synaptic circuit function by persistently modifying an excitatory-inhibitory interneuron subcircuit lasting weeks. CCT increases dentate gyrus expression of PKMζ that maintains long-term potentiation, particularly in somatostatin-expressing inhibitory interneurons that mediate both widespread inhibition, and through disinhibition, also local excitation of dentate gyrus. These findings that CCT modifies excitation-inhibition circuit coordination provide direct neurobiological evidence for a CBT-neuroplasticity hypothesis that, beyond particular item/event associations, learning to learn persistently changes neural circuit function.

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“…VIP INs, on the other hand, do not target principal cells, but rather selectively regulate the activity of other interneuron subpopulations, mostly SST INs (Pfeffer 2014). The observation that SST INs form more synapses with other interneurons than with PCs (Cottam et al 2013), suggests an important role of SST INs in the modulation of VIP INs and PV INs firing (Artinian and Lacaille 2018;Feldmeyer et al 2018;Karnani et al 2016a). However, SST neurons do not inhibit each other (Pfeffer et al 2013;Karnani et al 2016b).…”

Section: Introductionmentioning

confidence: 99%

Somatostatin receptors (SSTR1-5) on inhibitory interneurons in the barrel cortex

et al. 2019

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Inhibitory interneurons in the cerebral cortex contain specific proteins or peptides characteristic for a certain interneuron subtype. In mice, three biochemical markers constitute non-overlapping interneuron populations, which account for 80-90% of all inhibitory cells. These interneurons express parvalbumin (PV), somatostatin (SST), or vasoactive intestinal peptide (VIP). SST is not only a marker of a specific interneuron subtype, but also an important neuropeptide that participates in numerous biochemical and signalling pathways in the brain via somatostatin receptors (SSTR1-5). In the nervous system, SST acts as a neuromodulator and neurotransmitter affecting, among others, memory, learning, and mood. In the sensory cortex, the co-localisation of GABA and SST is found in approximately 30% of interneurons. Considering the importance of interactions between inhibitory interneurons in cortical plasticity and the possible GABA and SST co-release, it seems important to investigate the localisation of different SSTRs on cortical interneurons. Here, we examined the distribution of SSTR1-5 on barrel cortex interneurons containing PV, SST, or VIP. Immunofluorescent staining using specific antibodies was performed on brain sections from transgenic mice that expressed red fluorescence in one specific interneuron subtype (PV-Ai14, SST-Ai14, and VIP-Ai14 mice). SSTRs expression on PV, SST, and VIP interneurons varied among the cortical layers and we found two patterns of SSTRs distribution in L4 of barrel cortex. We also demonstrated that, in contrast to other interneurons, PV cells did not express SSTR2, but expressed other SSTRs. SST interneurons, which were not found to make chemical synapses among themselves, expressed all five SSTR subtypes.

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Disinhibition in learning and memory circuits: New vistas for somatostatin interneurons and long-term synaptic plasticity

Cited by 59 publications

References 65 publications

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

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

Learning to learn persistently modifies an entorhinal-hippocampal excitatory-inhibitory subcircuit

Somatostatin receptors (SSTR1-5) on inhibitory interneurons in the barrel cortex

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