Tonic Inhibitory Control of Dentate Gyrus Granule Cells by α5-Containing GABAAReceptors Reduces Memory Interference
Open accessAbstract
Interference between similar or overlapping memories formed at different times poses an important challenge on the hippocampal declarative memory system. Difficulties in managing interference are at the core of disabling cognitive deficits in neuropsychiatric disorders. Computational models have suggested that, in the normal brain, the sparse activation of the dentate gyrus granule cells maintained by tonic inhibitory control enables pattern separation, an orthogonalization process that allows distinct representations of memories despite interference. To test this mechanistic hypothesis, we generated mice with significantly reduced expression of the α5-containing GABAA (α5-GABAARs) receptors selectively in the granule cells of the dentate gyrus (α5DGKO mice). α5DGKO mice had reduced tonic inhibition of the granule cells without any change in fast phasic inhibition and showed increased activation in the dentate gyrus when presented with novel stimuli. α5DGKO mice showed impairments in cognitive tasks characterized by high interference, without any deficiencies in low-interference tasks, suggesting specific impairment of pattern separation. Reduction of fast phasic inhibition in the dentate gyrus through granule cell-selective knock-out of α2-GABAARs or the knock-out of the α5-GABAARs in the downstream CA3 area did not detract from pattern separation abilities, which confirms the anatomical and molecular specificity of the findings. In addition to lending empirical support to computational hypotheses, our findings have implications for the treatment of interference-related cognitive symptoms in neuropsychiatric disorders, particularly considering the availability of pharmacological agents selectively targeting α5-GABAARs. SIGNIFICANCE STATEMENT: Interference between similar memories poses a significant limitation on the hippocampal declarative memory system, and impaired interference management is a cognitive symptom in many disorders. Thus, understanding mechanisms of successful interference management or processes that can lead to interference-related memory problems has high theoretical and translational importance. This study provides empirical evidence that tonic inhibition in the dentate gyrus (DG), which maintains sparseness of neuronal activation in the DG, is essential for management of interference. The specificity of findings to tonic, but not faster, more transient types of neuronal inhibition and to the DG, but not the neighboring brain areas, is presented through control experiments. Thus, the findings link interference management to a specific mechanism, proposed previously by computational models.
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DG-selective knockdown of α5GABAARs did not produce any changes in anxiety-related behaviors.
“Similarly, DG-selective knockdown of α5GABAARs did not produce any changes in anxiety-related behaviors, casting doubt on the involvement of extrasynaptic GABAARs in the DG in anxiety regulation [50].”
From An emerging circuit pharmacology of GABAA receptors (2018) · cites this paper as [50]
Selective knockdown of α5GABAARs in CA3 or DG spanning the dorsal-ventral axis improves contextual memory in a fear-conditioning task.
“In studies focusing on hippocampal subregions rather than the anatomical division along the septo-temporal axis of the hippocampus, selective knockdown of α5GABAARs in CA3 or DG spanning the dorsal-ventral axis was shown to improve contextual memory in a fear-conditioning task [50].”
From An emerging circuit pharmacology of GABAA receptors (2018) · cites this paper as [50]
Knockdown of synaptic α2GABAARs in DG granule cells and the resulting reduction in fast phasic inhibition had no effect in high interference tasks.
“Importantly, knockdown of synaptic α2GABAARs in the DG granule cells and the resulting reduction in fast phasic inhibition had no effect in high interference tasks [50].”
From An emerging circuit pharmacology of GABAA receptors (2018) · cites this paper as [50]
Knockdown of α5GABAARs specifically in DG granule cells causes consistent impairments in behavioral tasks characterized by high memory interference, such as context discrimination with highly similar contexts, reversal learning in Morris water maze, and extinction of conditioned fear.
“Supporting this view, knockdown of α5GABAARs specifically in DG granule cells caused consistent impairments in behavioral tasks characterized by high memory interference, such as a context discrimination task with highly similar contexts, reversal learning in a Morris water maze spatial memory task, and extinction of conditioned fear responses (Fig. 3B) [50].”
From An emerging circuit pharmacology of GABAA receptors (2018) · cites this paper as [50]
Reduction of α2GABAAR activity selectively in the DG improves spatial memory.
“Selective knockdown of α2GABAARs in CA1 pyramidal neurons improves contextual fear conditioning [43], whereas reduction of α2GABAAR activity selectively in the DG improves both object recognition [84] and spatial [50, 43] memory.”
From An emerging circuit pharmacology of GABAA receptors (2018) · cites this paper as [50]
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An emerging circuit pharmacology of GABAA receptors
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- Authors
- Engin, E., Zarnowska, E. D., Benke, D., Tsvetkov, E., Sigal, M., Keist, R., Bolshakov, V. Y., Pearce, R. A., & Rudolph, U.
- Affiliations
- Harvard University (US)
- University of Zurich (CH)
- University of Wisconsin–Madison (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2015-10-07
- Volume
- 35
- Issue
- 40
- Pages
- 13698-13712
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC4595621
- OpenAlex
- W2207460105
- Cited by
- 79
- References
- 80
- Citations by year
- 2026: 7 · 2025: 3 · 2024: 9 · 2023: 12 · 2022: 3 · 2021: 7 · 2020: 7 · 2019: 7 · 2018: 9 · 2017: 6 · 2016: 9
- FWCI
- 4.81
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, other-oa)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion, other-oa)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- McLean Hospital
- National Alliance for Research on Schizophrenia and Depression
- Universität Zürich
- National Institutes of Health (1s10od010737-01a1)
- National Institute of Mental Health (R01MH080006)
- National Institute of General Medical Sciences (R01GM086448)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- alpha5 GABA-A receptor, dentate gyrus granule cells, tonic inhibition, pattern separation, memory interference, CA3, neuropsychiatric disorders
- MeSH terms
- Animals, Discrimination, Psychological, Exploratory Behavior, Gene Expression Regulation, Imidazoles, Memory, Mice, Inbred C57BL, Neural Inhibition, Neurons, Receptors, GABA-A, Swimming, Proto-Oncogene Proteins c-fos, Mice, Knockout, GABA Agonists, Maze Learning, Dentate Gyrus, Recognition, Psychology, Mice, Inhibitory Postsynaptic Potentials, In Vitro Techniques
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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