Apolipoprotein E4 Causes Age-Dependent Disruption of Slow Gamma Oscillations during Hippocampal Sharp-Wave Ripples
Open accessAbstract
Apolipoprotein (apo) E4 is the major genetic risk factor for Alzheimer's disease (AD), but the mechanism by which it causes cognitive decline is unclear. In knockin (KI) mice, human apoE4 causes age-dependent learning and memory impairments and degeneration of GABAergic interneurons in the hippocampal dentate gyrus. Here we report two functional apoE4-KI phenotypes involving sharp-wave ripples (SWRs), hippocampal network events critical for memory processes. Aged apoE4-KI mice had fewer SWRs than apoE3-KI mice and significantly reduced slow gamma activity during SWRs. Elimination of apoE4 in GABAergic interneurons, which prevents learning and memory impairments, rescued SWR-associated slow gamma activity but not SWR abundance in aged mice. SWR abundance was reduced similarly in young and aged apoE4-KI mice; however, the full SWR-associated slow gamma deficit emerged only in aged apoE4-KI mice. These results suggest that progressive decline of interneuron-enabled slow gamma activity during SWRs critically contributes to apoE4-mediated learning and memory impairments. VIDEO ABSTRACT.
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ApoE4-KI mice show reduced abundance of sharp-wave ripples.
“ApoE4-KI mice show reduced abundance of sharp-wave ripples, the local field potential of hippocampal replay events which are critical for consolidating spatial memory [182, 183].”
From Apolipoprotein E4, inhibitory network dysfunction, and Alzheimer’s disease (2019) · cites this paper as [182]
Sharp-wave ripples are critical for consolidating spatial memory.
“the local field potential of hippocampal replay events which are critical for consolidating spatial memory [182, 183]”
From Apolipoprotein E4, inhibitory network dysfunction, and Alzheimer’s disease (2019) · cites this paper as [182]
Removing apoE4 from inhibitory interneurons specifically rescues slow gamma power and learning and memory deficits.
“Notably, removing apoE4 from inhibitory interneurons specifically rescues slow gamma power and learning and memory deficits”
From Apolipoprotein E4, inhibitory network dysfunction, and Alzheimer’s disease (2019) · cites this paper as [182]
Younger mice recorded before the onset of significant interneuron loss do not show significant slow gamma power loss.
“Younger mice recorded before the onset of significant interneuron loss do not show significant slow gamma power loss”
From Apolipoprotein E4, inhibitory network dysfunction, and Alzheimer’s disease (2019) · cites this paper as [182]
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- Authors
- Gillespie, A. K., Jones, E. A., Lin, Y.-H., Karlsson, M. P., Kay, K., Yoon, S. Y., Tong, L. M., Nova, P., Carr, J. S., Frank, L. M., & Huang, Y.
- Affiliations
- Gladstone Institutes (US)
- University of California, San Francisco (US)
- Corresponding author
- Huang, Yadong
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2016-05
- Volume
- 90
- Issue
- 4
- Pages
- 740-751
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC5097044
- OpenAlex
- W2346016739
- Cited by
- 187
- References
- 57
- Citations by year
- 2026: 13 · 2025: 23 · 2024: 16 · 2023: 20 · 2022: 28 · 2021: 24 · 2020: 19 · 2019: 13 · 2018: 11 · 2017: 12 · 2016: 8
- FWCI
- 11.81
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- McKnight Foundation
- Achievement Rewards for College Scientists Foundation
- Hellman Foundation
- National Institutes of Health (1c06rr018928-01)
- National Institute on Aging (RF1AG047655, R01AG048017)
- National Institute of Mental Health (R01MH105174, R01MH090188)
- National Institute of General Medical Sciences (T32GM007618)
- National Center for Research Resources (C06-RR-018928)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (T32HD007470)
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- APOE ε4, Alzheimer's disease, sharp-wave ripples, hippocampus, GABAergic interneurons, dentate gyrus, aging, learning and memory impairment
- MeSH terms
- Aging, Alzheimer Disease, Animals, Cognition Disorders, Disease Models, Animal, Hippocampus, Interneurons, Memory Disorders, Mice, Transgenic, Maze Learning, Apolipoprotein E4, Gene Knock-In Techniques
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