Inhibitory projections connecting the dentate gyri in the two hemispheres support spatial and contextual memory

Yen, Ting-Yun; Huang, Xu; MacLaren, Duncan A. A.; Schlesiger, Magdalene I.; Monyer, Hannah; Lien, Cheng Chang

doi:10.1016/j.celrep.2022.110831

Cited by 3 publications

(5 citation statements)

References 76 publications

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“…At the network level, the interaction between local and long-range excitation and inhibition in the cortex and hippocampus could be important for supporting context-dependent stability and flexibility of memory representations encoding familiar and novel experiences and generating adaptive learned behaviors. Furthermore, GABAergic circuits may substantially coordinate oscillations (Somogyi et al, 2014), such as gamma oscillations during learning (Wulff et al, 2009), theta oscillations during locomotion (Csicsvari et al, 1999;Buzsáki, 2002;Bezaire et al, 2016;Melzer and Monyer, 2020), and sharp wave ripples (SWR; Cutsuridis and Taxidis, 2013;Schlingloff et al, 2014;Stark et al, 2014;Evangelista et al, 2020;Noguchi et al, 2022) in quiet wakefulness, and sleep (Eichenbaum, 2000;Squire, 2004;Basu and Siegelbaum, 2015;Francavilla et al, 2018;Eyre and Bartos, 2019;Udakis et al, 2020;Malik et al, 2022;Yen et al, 2022).…”

Section: How Do Local and Long-range Gabaergic Circuits Interact To C...mentioning

confidence: 99%

“…In the hippocampus, disinhibitory gating can be local (LEC driven VIP INs) or long-range (direct GABAergic projections from EC). Curiously, most long-range GABAergic projection neurons synapse onto INs in their target region and are therefore primarily disinhibitory in nature (Fuchs et al, 2007;Melzer et al, 2012;Caputi et al, 2013;Tyan et al, 2014;Basu et al, 2016;Melzer and Monyer, 2020;Yen et al, 2022; Figure 1).…”

Section: Disinhibitionmentioning

confidence: 99%

“…While GABAergic inhibitory neurons are typically attributed to maintaining local excitation-inhibition balance and dynamically modulate activity at the microcircuit level, there is surmounting evidence that GABAergic neurons also send long-range inhibitory projections (LRIPs) between different brain areas (Jinno et al, 2007;Melzer et al, 2012;Caputi et al, 2013;Lee A. T. et al, 2014;Basu et al, 2016;Joshi et al, 2017;Melzer and Monyer, 2020;Sans-Dublanc et al, 2020;Szabo et al, 2022;Yen et al, 2022;Schroeder et al, 2023). It has been postulated that LRIPs exist to coordinate activity across longer distances within the brain and are important for generating interregional synchrony.…”

Section: Long-range Gabaergic Disinhibitory Circuitsmentioning

confidence: 99%

“…GABAergic INs modulate the activity of other neurons to maintain a homeostatic excitation-inhibition balance. This is a striking feature of the cortex where E/I ratios are tightly maintained within various layers (Pfeffer et al, 2013;Xue et al, 2014;Adesnik, 2018;Yen et al, 2022). Do GABAergic inputs just act to balance excitation, or do they have specific roles in organizing information flow?…”

Section: Introductionmentioning

confidence: 99%

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Local and long-range GABAergic circuits in hippocampal area CA1 and their link to Alzheimer’s disease

Hernández-Frausto,

Bilash,

Masurkar

et al. 2023

Front. Neural Circuits

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GABAergic inhibitory neurons are the principal source of inhibition in the brain. Traditionally, their role in maintaining the balance of excitation-inhibition has been emphasized. Beyond homeostatic functions, recent circuit mapping and functional manipulation studies have revealed a wide range of specific roles that GABAergic circuits play in dynamically tilting excitation-inhibition coupling across spatio-temporal scales. These span from gating of compartment- and input-specific signaling, gain modulation, shaping input–output functions and synaptic plasticity, to generating signal-to-noise contrast, defining temporal windows for integration and rate codes, as well as organizing neural assemblies, and coordinating inter-regional synchrony. GABAergic circuits are thus instrumental in controlling single-neuron computations and behaviorally-linked network activity. The activity dependent modulation of sensory and mnemonic information processing by GABAergic circuits is pivotal for the formation and maintenance of episodic memories in the hippocampus. Here, we present an overview of the local and long-range GABAergic circuits that modulate the dynamics of excitation-inhibition and disinhibition in the main output area of the hippocampus CA1, which is crucial for episodic memory. Specifically, we link recent findings pertaining to GABAergic neuron molecular markers, electrophysiological properties, and synaptic wiring with their function at the circuit level. Lastly, given that area CA1 is particularly impaired during early stages of Alzheimer’s disease, we emphasize how these GABAergic circuits may contribute to and be involved in the pathophysiology.

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Section: How Do Local and Long-range Gabaergic Circuits Interact To C...mentioning

confidence: 99%

Section: Disinhibitionmentioning

confidence: 99%

Section: Long-range Gabaergic Disinhibitory Circuitsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Local and long-range GABAergic circuits in hippocampal area CA1 and their link to Alzheimer’s disease

Hernández-Frausto,

Bilash,

Masurkar

et al. 2023

Front. Neural Circuits

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“…Indeed, silencing of either the general LECGABA hippocampal projections 36 or the LECGLU&GABA to CA3 input impair novel object recognition, which might reflect a default in encoding novelty such that familiar objects are not registered. Further roles for long-range GABAergic transmission in learning and memory include encoding of object location 46,93 , spatial learning 97 , and contextual memory [97][98][99] .…”

Section: Contrasting Sub-region-specific Microcircuitry and Related I...mentioning

confidence: 99%

Entorhinal cortex glutamatergic and GABAergic projections bidirectionally control discrimination and generalization of hippocampal representations

Robert,

O’Neil,

Rashid

et al. 2023

Preprint

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Discrimination and generalization are crucial brain-wide functions for memory and object recognition that utilize pattern separation and completion computations. Circuit mechanisms supporting these operations remain enigmatic. We show lateral entorhinal cortex glutamatergic (LECGLU) and GABAergic (LECGABA) projections are essential for object recognition memory. Silencing LECGLUduringin vivotwo-photon imaging increased the population of active CA3 pyramidal cells but decreased activity rates, suggesting a sparse coding function through local inhibition. Silencing LECGLUalso decreased place cell remapping between different environments validating this circuit drives pattern separation and context discrimination. Optogenetic circuit mapping confirmed that LECGLUdrives dominant feedforward inhibition to prevent CA3 somatic and dendritic spikes. However, conjunctively active LECGABAsuppresses this local inhibition to disinhibit CA3 pyramidal neuron soma and selectively boost integrative output of LEC and CA3 recurrent network. LECGABAthus promotes pattern completion and context generalization. Indeed, without this disinhibitory input, CA3 place maps show decreased similarity between contexts. Our findings provide circuit mechanisms whereby long-range glutamatergic and GABAergic cortico-hippocampal inputs bidirectionally modulate pattern separation and completion, providing neuronal representations with a dynamic range for context discrimination and generalization.

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A theory of hippocampal function: New developments

Rolls,

Treves

2024

Progress in Neurobiology

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Inhibitory projections connecting the dentate gyri in the two hemispheres support spatial and contextual memory

Cited by 3 publications

References 76 publications

Local and long-range GABAergic circuits in hippocampal area CA1 and their link to Alzheimer’s disease

Local and long-range GABAergic circuits in hippocampal area CA1 and their link to Alzheimer’s disease

Entorhinal cortex glutamatergic and GABAergic projections bidirectionally control discrimination and generalization of hippocampal representations

A theory of hippocampal function: New developments

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