Connectivity and network state-dependent recruitment of long-range VIP-GABAergic neurons in the mouse hippocampus

Francavilla, Ruggiero; Villette, Vincent; Luo, Xiao; Chamberland, Simon; Muñoz-Pino, Einer; Camiré, Olivier; Wagner, Kristina; Kis, Viktor; Somogyi, Péter; Topolnik, Lisa

doi:10.1038/s41467-018-07162-5

Cited by 77 publications

(109 citation statements)

References 72 publications

Supporting

Mentioning

105

Contrasting

Order By: Relevance

“…Given that here the soma size of VIP+ cells recorded in vivo was used for pIS3 identification and that all CR+/VIP+ cells have a smaller soma size ( Figure 5), the subiculum-projecting fraction of this population could be sampled as pIS3 cells and contribute to variability in cellular activity patterns. Indeed, we reported that the subiculum-projecting VIP+ cells are the theta-off cells, as they strongly decrease their activity during theta-run episodes [32]. The latter was seen in a small number of pIS3 cells recorded in the current study (3/18 cells were decreasing activity during theta-run episodes), and may be due to specific modulatory inputs received by the two VIP+ cell types.…”

Section: Discussionsupporting

confidence: 45%

“…CA1 PCs or subcortical neuronal populations), or cellular diversity within the pIS3 cell population. Indeed, we recently identified a new type of VIP+ long-range projecting (VIP-LRP) cell in the CA1 hippocampus that, in addition to the CA1, innervates subiculum with a region-specific target preference [32]. Further diversity was revealed within the VIP-LRP population, with cells co-expressing the muscarinic receptor 2, CR or proenkephalin in addition to VIP, and having somata located within PYR, RAD or LM.…”

Section: Discussionmentioning

confidence: 99%

“…The Vip Cre mice were crossed with a reporter Ai9 line to achieve the tdTomato expression in VIP+ cells [30]. Both mouse lines (Vip-eGFP and Vip Cre ) have been previously characterized in details and validated for the expression of the reporter fluorescent proteins selectively in cells expressing VIP endogenously [18,31,32]. Consistent with previous findings on VIP expression in hippocampal interneurons [14,15], in both mouse lines, fluorescently-labeled cells were located throughout the CA1, with many of these having a vertical orientation that resembled the IS3 cell morphology ( Figure 1A) [17,18].…”

Section: Synaptic Properties Of Is3 Interneuronsmentioning

confidence: 99%

“…We expressed a genetically-encoded Ca 2+ indicator GCaMP6f [43] in VIP+ cells using a Cre-dependent viral vector AAV1.Syn.Flex.GCaMP6f.WPRE.SV40 injected into the CA1 area of Vip Cre mice (n = 3 mice). Two-photon somatic Ca 2+ -imaging was performed within the hippocampal CA1 PYR and RAD, the main location site of IS3 cell somata (Figures 1A; S1; 5C), in combination with local field potential (LFP) recordings from the contralateral CA1 PYR ( Figure 5D, top) considering that theta oscillations and SWRs are coherent between the two hemispheres [32,44,45]. In addition, recordings of the animal's speed were performed to track locomotion ( Figure 5A [42,46].…”

Section: Delayed Recruitment Of Is3 Cells During Theta-run Epochs In mentioning

confidence: 99%

See 3 more Smart Citations

Synaptic mechanisms underlying the network state-dependent recruitment of VIP-expressing interneuron-specific interneurons in the CA1 hippocampus

Luo

Guet-McCreight

Villette

et al. 2018

Preprint

Self Cite

View full text Add to dashboard Cite

In the hippocampus, a highly specialized population of vasoactive intestinal peptide (VIP)-expressing interneuron-specific (IS) inhibitory cells provides local circuit disinhibition via preferential innervation of different types of GABAergic interneurons.While disinhibition can be critical in modulating network activity and different forms of hippocampal learning, the synaptic and integrative properties of IS cells and their recruitment during network oscillations remain unknown. Using a combination of patchclamp recordings, photostimulation, computational modelling as well as recordings of network oscillations simultaneously with two-photon Ca 2+ -imaging in awake mice in vivo, we identified synaptic mechanisms that can control the firing of IS cells, and explored their impact on the cell recruitment during theta oscillations and sharp-waveassociated ripples. We found that IS cells fire spikes in response to both the Schaffer collateral and the temporoammonic pathway activation. Moreover, integrating their intrinsic and synaptic properties into computational models predicted recruitment of these cells during the rising to peak phases of theta oscillations and during ripples depending on inhibitory contributions. In vivo Ca 2+ -imaging in awake mice confirmed in part the theoretical predictions, revealing a significant speed modulation of IS cells and their preferential albeit delayed recruitment during theta-run epochs, with firing at the rising phase to peak of the theta cycle. However, it also uncovered that IS cells are not activated during ripples. Thus, given the preferential theta-modulated firing of IS cells in awake hippocampus, we postulate that these cells may be important for information gating during spatial navigation and memory encoding.3

show abstract

Section: Discussionsupporting

confidence: 45%

Section: Discussionmentioning

confidence: 99%

Section: Synaptic Properties Of Is3 Interneuronsmentioning

confidence: 99%

Section: Delayed Recruitment Of Is3 Cells During Theta-run Epochs In mentioning

confidence: 99%

See 2 more Smart Citations

Synaptic mechanisms underlying the network state-dependent recruitment of VIP-expressing interneuron-specific interneurons in the CA1 hippocampus

Luo

Guet-McCreight

Villette

et al. 2018

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…Accumulating evidence suggests that disinhibitory circuits play a crucial role in various cognitive tasks such as fear conditioning (Letzkus et al, 2011;Pi et al, 2013) and sensory discrimination (Hangya et al, 2015;Pinto et al, 2013). The dominant interneuron types of the disinhibitory circuits are VIP, SOM and PV inhibitory neurons (Donato, Rompani, & Caroni, 2013;Francavilla et al, 2018;Kamigaki & Dan, 2017;S. Zhang et al, 2014).…”

Section: Dynamic Processing Across Multiple Areasmentioning

confidence: 99%

Oscillation-driven memory encoding, maintenance and recall in an entorhinal-hippocampal circuit model

Kurikawa

Mizuseki

Fukai

2019

Preprint

View full text Add to dashboard Cite

Coherent neuronal activity phase-locked to theta and gamma oscillations is thought to be crucial for information processing across multiple brain regions. However, the network mechanisms underlying the oscillation-driven multi-area computation remains largely unclear. To explore such mechanisms, we constructed a hippocampal-entorhinal neural network model involving parvalbumin-positive, somatostatin-positive and vasoactive intestinal polypeptide interneurons in the hippocampal area CA1 and the superficial and deep layers of the entorhinal cortex. We examined the model behavior by using neural activity data recorded during delayed nonmatching to place tasks. Our model shows that experimentally observed relative phases of theta oscillation ensure working memory performance. Moreover, the model predicts that acetylcoline concentrations in these areas modulate the balance between intra-area and inter-area information processing according to cognitive demands emergent at encoding, maintenance and recall epochs of a working memory task. Our model suggests the active role of theta-phase-locked firing and cholinergic modulations for multi-area memory processing.

show abstract

Morpho‐physiological properties and connectivity of vasoactive intestinal polypeptide‐expressing interneurons in the mouse hippocampal dentate gyrus

Wei¹,

Wu²,

Yeh³

et al. 2021

J Comp Neurol

View full text Add to dashboard Cite

The hippocampus is a key brain structure for cognitive and emotional functions. Among the hippocampal subregions, the dentate gyrus (DG) is the first station that receives multimodal sensory information from the cortex. Local‐circuit inhibitory GABAergic interneurons (INs) regulate the excitation–inhibition balance in the DG principal neurons (PNs) and therefore are critical for information processing. Similar to PNs, GABAergic INs also receive distinct inhibitory inputs. Among various classes of INs, vasoactive intestinal polypeptide‐expressing (VIP+) INs preferentially target other INs in several brain regions and thereby directly modulate the GABAergic system. However, the morpho‐physiological characteristics and postsynaptic targets of VIP+ INs in the DG are poorly understood. Here, we report that VIP+ INs in the mouse DG are highly heterogeneous based on their morpho‐physiological characteristics. In approximately two‐thirds of morphologically reconstructed cells, their axons ramify in the hilus. The remaining cells project their axons exclusively to the molecular layer (15%), to both the molecular layer and hilus (10%), or throughout the entire DG layers (8%). Generally, VIP+ INs display variable intrinsic properties and discharge patterns without clear correlation with their morphologies. Finally, VIP+ INs are recruited with a long latency in response to theta‐band cortical inputs and preferentially innervate GABAergic INs over glutamatergic PNs. In summary, VIP+ INs in the DG are composed of highly diverse subpopulations and control the DG output via disinhibition.

show abstract

Connectivity and network state-dependent recruitment of long-range VIP-GABAergic neurons in the mouse hippocampus

Cited by 77 publications

References 72 publications

Synaptic mechanisms underlying the network state-dependent recruitment of VIP-expressing interneuron-specific interneurons in the CA1 hippocampus

Synaptic mechanisms underlying the network state-dependent recruitment of VIP-expressing interneuron-specific interneurons in the CA1 hippocampus

Oscillation-driven memory encoding, maintenance and recall in an entorhinal-hippocampal circuit model

Morpho‐physiological properties and connectivity of vasoactive intestinal polypeptide‐expressing interneurons in the mouse hippocampal dentate gyrus

Contact Info

Product

Resources

About