Reduced tonic inhibition in the dentate gyrus contributes to chronic stress-induced impairments in learning and memory
Open accessAbstract
It is well established that stress impacts the underlying processes of learning and memory. The effects of stress on memory are thought to involve, at least in part, effects on the hippocampus, which is particularly vulnerable to stress. Chronic stress induces hippocampal alterations, including but not limited to dendritic atrophy and decreased neurogenesis, which are thought to contribute to chronic stress-induced hippocampal dysfunction and deficits in learning and memory. Changes in synaptic transmission, including changes in GABAergic inhibition, have been documented following chronic stress. Recently, our laboratory demonstrated shifts in EGABA in CA1 pyramidal neurons following chronic stress, compromising GABAergic transmission and increasing excitability of these neurons. Interestingly, here we demonstrate that these alterations are unique to CA1 pyramidal neurons, since we do not observe shifts in EGABA following chronic stress in dentate gyrus granule cells. Following chronic stress, there is a decrease in the expression of the GABAA receptor (GABAA R) δ subunit and tonic GABAergic inhibition in dentate gyrus granule cells, whereas there is an increase in the phasic component of GABAergic inhibition, evident by an increase in the peak amplitude of spontaneous inhibitory postsynaptic currents (sIPSCs). Given the numerous changes observed in the hippocampus following stress, it is difficult to pinpoint the pertinent contributing pathophysiological factors. Here we directly assess the impact of a reduction in tonic GABAergic inhibition of dentate gyrus granule cells on learning and memory using a mouse model with a decrease in GABAA R δ subunit expression specifically in dentate gyrus granule cells (Gabrd/Pomc mice). Reduced GABAA R δ subunit expression and function in dentate gyrus granule cells is sufficient to induce deficits in learning and memory. Collectively, these findings suggest that the reduction in GABAA R δ subunit-mediated tonic inhibition in dentate gyrus granule cells contributes, at least in part, to deficits in learning and memory associated with chronic stress. These findings have significant implications regarding the pathophysiological mechanisms underlying impairments in learning and memory associated with stress and suggest a role for GABAA R δ subunit containing receptors in dentate gyrus granule cells. © 2016 Wiley Periodicals, Inc.
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DG-selective knockdown of δGABAARs failed to produce any anxiogenic effects.
“However, DG-selective knockdown of δGABAARs failed to produce any anxiogenic effects [49].”
From An emerging circuit pharmacology of GABAA receptors (2018) · cites this paper as [49]
DG granule cell-selective knockdown of δGABAARs impairs auditory and contextual fear conditioning.
“DG granule cell – selective knockdown δGABAARs has been shown to impair auditory and contextual fear conditioning [49], however, the knockdown mice were unfortunately not evaluated in tasks characterized by high memory interference.”
From An emerging circuit pharmacology of GABAA receptors (2018) · cites this paper as [49]
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- Authors
- Lee, V., MacKenzie, G., Hooper, A., & Maguire, J.
- Affiliations
- Tufts University (US)
- Corresponding author
- Maguire, Jamie
- Venue
- Hippocampus
- Publisher
- Wiley
- Published
- 2016-06-02
- Volume
- 26
- Issue
- 10
- Pages
- 1276-1290
- ISSN
- 1050-9631 (ISSN-L)
- 1098-1063
- PMC
- PMC5030140
- OpenAlex
- W2392810476
- Cited by
- 47
- References
- 55
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 7 · 2023: 3 · 2022: 2 · 2021: 9 · 2020: 3 · 2019: 5 · 2018: 7 · 2017: 3 · 2016: 2
- FWCI
- 3.19
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Hippocampus (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (NS073574)
- Center for Neuroscience Research (P30 NS047243)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- chronic stress, dentate gyrus granule cells, tonic inhibition, GABAergic inhibition, learning and memory impairment, spontaneous inhibitory postsynaptic currents, stress-induced memory impairment
- MeSH terms
- Animals, Chronic Disease, Female, gamma-Aminobutyric Acid, Learning, Learning Disabilities, Male, Memory, Memory Disorders, Mice, Inbred C57BL, Mice, Transgenic, Neural Inhibition, Receptors, GABA-A, Restraint, Physical, Stress, Psychological, Dentate Gyrus, Tissue Culture Techniques
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