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

Vasuta, Cristina; Artinian, Julien; Laplante, Isabel; Hébert-Seropian, Sarah; Elayoubi, K.; Lacaille, Jean-Claude

doi:10.1523/eneuro.0051-15.2015

Cited by 35 publications

(73 citation statements)

References 63 publications

(93 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Because this excitation-inhibition coordination depends only on MPP activation, it provides a distinct mechanism of DG excitation-inhibition coordination, complementary to that provided by immature adult-born granule cells that mediate mGluRdependent inhibition in response to LPP activation and NMDAR-dependent excitation in response to MPP activation 34 . Similar disinhibitory plasticity has also been described at the Schaffer collateral and other cortical synapses [35][36][37] . These CCT-induced subcircuit changes have widespread effects because we detected them in field potential recordings, indicating they are not the sparse changes that mediate content-specific memory formation according to the synaptic plasticity and memory hypothesis 38 .…”

Section: A Neocortical-hippocampal Subcircuit Tuned By Cognitive Traisupporting

confidence: 67%

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

Chung

Jou

Grau‐Perales

et al. 2019

Preprint

View full text Add to dashboard Cite

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.

show abstract

Section: A Neocortical-hippocampal Subcircuit Tuned By Cognitive Traisupporting

confidence: 67%

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

Chung

Jou

Grau‐Perales

et al. 2019

Preprint

View full text Add to dashboard Cite

show abstract

“…The LTP gating by Sst-INs, however, is not a universal phenomenon throughout the brain. For example, in the hippocampus, the Sst-INs located in the oriens/alveus region of the area CA1 rather enhance LTP in the Schaffer collateral pathway by inhibiting GABAergic neurons in the stratum radiatum and thereby disinhibiting the CA1 principal cells (31). The PV-INs, in turn, appear to gate the hippocampal LTP, based on the finding of a stronger LTP in the model mice for the pre-symptomatic ASL and Altzheimer, in which a mutated NRG1 receptor Erb4 causes deficiencies of the PV-INs (32-34).…”

Section: Discussionmentioning

confidence: 99%

Disinhibition-assisted LTP in the prefrontal-amygdala pathway via suppression of somatostatin-expressing interneurons

Ito

Fisco

Morozov

2019

Preprint

View full text Add to dashboard Cite

Natural brain adaptations often involve changes in synaptic strength. The artificial manipulations can help 10 investigate the role of synaptic strength in a specific brain circuit not only in various physiological phenomena like 11 correlated neuronal firing and oscillations but also in behaviors. High and low-frequency stimulation at presynaptic 12 sites has been used widely to induce long-term potentiation (LTP) and depression (LTD), respectively. This approach 13 is effective in many brain areas, but not in the basolateral amygdala (BLA), because the robust local GABAergic tone 14 inside the BLA restricts synaptic plasticity. Here, we identified the subclass of GABAergic neurons that gate LTP in 15 the BLA afferents from the dorsomedial prefrontal cortex (dmPFC). Chemogenetic suppression of somatostatin-16 positive interneurons (Sst-INs) enabled the ex vivo LTP by high-frequency stimulation of the afferent, but the 17 suppression of parvalbumin-positive interneurons (PV-INs) did not. Moreover, optogenetic suppression of Sst-INs 18 with Arch also enabled LTP of the dmPFC-BLA synapses both ex vivo and in vivo. These findings reveal that Sst-INs 19 but not PV-INs gate LTP in the dmPFC-BLA pathway and provide a method for artificial synaptic facilitation in BLA. 20 21 24 25 26Circuit interrogation using the optogenetics and chemogenetics has become a standard approach 27 for testing the causal role of specific neuronal populations and synapses in brain activities and 28 animal behaviors. The techniques employ depolarizing or hyperpolarizing neuronal compartments, 29 like the soma, dendrites, and synaptic terminals, to trigger or suppress the action potentials and 30 release of neurotransmitter (1, 2). Meanwhile, the natural neuronal adaptations driven by 31 experience and learning, or observed during development or in disease, involve brain alterations, 32 not only in the neuronal activity but also in the synaptic efficacy. For example, the auditory fear 33 conditioning, a model of adaptive defensive behavior, strengthens the auditory inputs to the lateral 34 amygdala (3), whereas the fear extinction training depresses the prefrontal-amygdala synapses and 35 strengthens the reciprocal amygdala-prefrontal synapses (4, 5). Modeling and quantitative analyses 36 of such naturally occurring brain adaptations require methods for selective manipulation of the 37 synaptic strength both ex vivo and in vivo. 38 By applying high-or low-frequency presynaptic stimulation, synapses, in many cases, can 39 be potentiated or depressed, respectively (6). This simple technique has been employed in 40 optogenetics for manipulating synaptic strength ex vivo and in vivo and proved successful in 41 several cases. LTP was obtained in the recurrent synapses in hippocampal area CA3 by applying 42 20 Hz stimulation (7) and in the cortico-striatal synapses by applying the theta-burst stimulation 43 (8). LTD was obtained in the inputs to the nucleus accumbens from the infralimbic cortex and 44 basolateral amygdala by applying the low-freq...

show abstract

“…Interneuron functions are not static and inhibitory cells express short-and longterm plasticity of their synaptic inputs and outputs [3,4]. Long-lasting changes at interneurons synapses may serve to enhance hippocampal network computation and flexibility [3,5]. 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].…”

Section: Introductionmentioning

confidence: 99%

“…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%

See 1 more Smart Citation

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

et al. 2020

Self Cite

View full text Add to dashboard Cite

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.

show abstract

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

Cited by 35 publications

References 63 publications

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

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

Disinhibition-assisted LTP in the prefrontal-amygdala pathway via suppression of somatostatin-expressing interneurons

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

Contact Info

Product

Resources

About