Brief synaptic inhibition persistently interrupts firing of fast-spiking interneurons

Chamberland, Simon; Nebet, Erica R.; Valero, Manuel; Hanani, Monica; Egger, Robert; Larsen, Samantha B.; Eyring, Katherine W.; Buzsáki, György; Tsien, Richard W.

doi:10.1016/j.neuron.2023.01.017

Cited by 11 publications

(47 citation statements)

References 101 publications

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“…4B,C) to reliably trigger the persistent interruption of firing. Therefore, these results establish Sst;;Tac1-INs in the CA1 hippocampus as a novel subclass of disinhibitory interneurons, one imbued with a potent capability to relieve pyramidal neurons from inhibition (20).…”

Section: Sst;;tac1-ins Are Necessary and Sufficient To Interrupt Fs-inssupporting

confidence: 53%

“…5). In brief, the Sst;;Tac1 (20). Having intersectional mouse lines ready for optogenetic or pharmacogenetic manipulation will hasten future testing of such circuit predictions and their behavioral implications.…”

Section: Discussionmentioning

confidence: 99%

“…We and others have previously shown that the superfamily of Sst-INs targets both CA1-PYRs and FS-INs in the CA1 region (9,20). In our recent study (20) This normalization circumvented potential confounds including different transgenic animal models, number of presynaptic axons in the slice and optrode placement (Fig.…”

Section: Cell Type-specific Targeting By Subpopulations Of Sst-insmentioning

confidence: 90%

“…We now turn to the use of subgroup-specific mouse lines as experimental tools. We recently reported that FS-INs undergo a strikingly persistent interruption of firing upon brief synaptic inhibition, resulting in CA1-PYR disinhibition (20). The interruption of firing was induced by optogenetic stimulation of the general Sst-INs population, but whether this function is exclusive or shared amongst multiple Sst-INs subpopulation remains unclear.…”

Section: Sst;;tac1-ins Are Necessary and Sufficient To Interrupt Fs-insmentioning

confidence: 99%

“…While Sst-INs have been functionally studied as a single ensemble ((6, 9, 10) but see (11,12)), multiple studies provide clues to divisions in their neurochemical, anatomical and electrophysiological properties (13)(14)(15)(16)(17)(18)(19). For example, the overall population of Sst-INs can target both principal neurons and FS-INs, resulting respectively in inhibition and disinhibition, two mostly opposing network effects (9,(20)(21)(22)(23). Whether specific subtypes of Sst-INs account for these disparate circuit functions remains unknown.…”

Section: Introductionmentioning

confidence: 99%

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Functional specialization of hippocampal somatostatin-expressing interneurons

Chamberland

Grant

Machold

et al. 2023

Preprint

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Hippocampal somatostatin-expressing (Sst) GABAergic interneurons (INs) exhibit considerable anatomical and functional heterogeneity. Recent single cell transcriptome analyses have provided a comprehensive Sst-IN subtype census, a plausible molecular ground truth of neuronal identity whose links to specific functionality remain incomplete. Here, we designed an approach to identify and access subpopulations of Sst-INs based on transcriptomic features. Four mouse models based on single or combinatorial Cre- and Flp- expression differentiated functionally distinct subpopulations of CA1 hippocampal Sst-INs that largely tiled the morpho-functional parameter space of the Sst-INs superfamily. Notably, the Sst;;Tac1 intersection revealed a population of bistratified INs that preferentially synapsed onto fast-spiking interneurons (FS-INs) and were both necessary and sufficient to interrupt their firing. In contrast, the Ndnf;;Nkx2-1 intersection identified a population of oriens lacunosum-moleculare (OLM) INs that predominantly targeted CA1 pyramidal neurons, avoiding FS-INs. Overall, our results provide a framework to translate neuronal transcriptomic identity into discrete functional subtypes that capture the diverse specializations of hippocampal Sst-INs.

show abstract

Section: Sst;;tac1-ins Are Necessary and Sufficient To Interrupt Fs-inssupporting

confidence: 53%

Section: Discussionmentioning

confidence: 99%

Section: Cell Type-specific Targeting By Subpopulations Of Sst-insmentioning

confidence: 90%

Section: Sst;;tac1-ins Are Necessary and Sufficient To Interrupt Fs-insmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Functional specialization of hippocampal somatostatin-expressing interneurons

Chamberland

Grant

Machold

et al. 2023

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

Functional specialization of hippocampal somatostatin-expressing interneurons

Chamberland,

Grant,

Machold

et al. 2024

Proc. Natl. Acad. Sci. U.S.A.

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Hippocampal somatostatin-expressing ( Sst ) GABAergic interneurons (INs) exhibit considerable anatomical and functional heterogeneity. Recent single-cell transcriptome analyses have provided a comprehensive Sst -IN subpopulations census, a plausible molecular ground truth of neuronal identity whose links to specific functionality remain incomplete. Here, we designed an approach to identify and access subpopulations of Sst -INs based on transcriptomic features. Four mouse models based on single or combinatorial Cre- and Flp- expression differentiated functionally distinct subpopulations of CA1 hippocampal Sst- INs that largely tiled the morpho-functional parameter space of the Sst -INs superfamily. Notably, the Sst;;Tac1 intersection revealed a population of bistratified INs that preferentially synapsed onto fast-spiking interneurons (FS-INs) and were sufficient to interrupt their firing. In contrast, the Ndnf;;Nkx2-1 intersection identified a population of oriens lacunosum-moleculare INs that predominantly targeted CA1 pyramidal neurons, avoiding FS-INs. Overall, our results provide a framework to translate neuronal transcriptomic identity into discrete functional subtypes that capture the diverse specializations of hippocampal Sst -INs.

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Functional networks of inhibitory neurons orchestrate synchrony in the hippocampus

Bocchio,

Vorobyev,

Sadeh

et al. 2023

Preprint

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Inhibitory interneurons are a critical component of cortical circuits. Beyond providing inhibition, they have been proposed to coordinate the firing of excitatory neurons within cell assemblies. While many studies have dissected the function of specific interneuron subtypes, the relationship between interneurons and pyramidal cell synchrony in vivo remains unclear. We use an all-optical approach to simultaneously record hippocampal interneurons and pyramidal cells, and test the network influence of single interneurons. We show that CA1 interneurons form a functionally interconnected network that promotes synchrony through disinhibition during awake immobility without altering endogenous cell assemblies. A network model indicates that cell assemblies and dense but unspecific connectivity between interneurons are necessary ingredients to explain our experimental results. Thus, interneurons may not only operate via division of labor, but also through concerted activity. Our data challenge the idea of a purely decorrelating or segregating function of inhibition.

show abstract

Brief synaptic inhibition persistently interrupts firing of fast-spiking interneurons

Cited by 11 publications

References 101 publications

Functional specialization of hippocampal somatostatin-expressing interneurons

Functional specialization of hippocampal somatostatin-expressing interneurons

Functional specialization of hippocampal somatostatin-expressing interneurons

Functional networks of inhibitory neurons orchestrate synchrony in the hippocampus

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