Hippocampal theta rhythm and its coupling with gamma oscillations require fast inhibition onto parvalbumin-positive interneurons
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Hippocampal theta (5-10 Hz) and gamma (35-85 Hz) oscillations depend on an inhibitory network of GABAergic interneurons. However, the lack of methods for direct and cell-type-specific interference with inhibition has prevented better insights that help link synaptic and cellular properties with network function. Here, we generated genetically modified mice (PV-Deltagamma(2)) in which synaptic inhibition was ablated in parvalbumin-positive (PV+) interneurons. Hippocampal local field potential and unit recordings in the CA1 area of freely behaving mice revealed that theta rhythm was strongly reduced in these mice. The characteristic coupling of theta and gamma oscillations was strongly altered in PV-Deltagamma(2) mice more than could be accounted for by the reduction in theta rhythm only. Surprisingly, gamma oscillations were not altered. These data indicate that synaptic inhibition onto PV+ interneurons is indispensable for theta- and its coupling to gamma oscillations but not for rhythmic gamma-activity in the hippocampus. Similar alterations in rhythmic activity were obtained in a computational hippocampal network model mimicking the genetic modification, suggesting that intrahippocampal networks might contribute to these effects.
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The involvement of PV+ interneurons in theta-gamma coupling has been previously established.
“While the involvement of PV+ interneurons in theta-gamma coupling has been previously established (23)”
From Perineuronal nets, inhibitory interneurons and anxiety-related ventral hippocampal neuronal oscillations are altered by early life adversity (2019) · cites this paper as [23]
Disconnecting PV cell activity from the fast spiking inhibitory network in the hippocampus reduces both theta power and theta-gamma coupling.
“In fact, disconnecting PV cell activity from the fast spiking inhibitory network in the hippocampus reduces both theta power and theta-gamma coupling (23)”
From Perineuronal nets, inhibitory interneurons and anxiety-related ventral hippocampal neuronal oscillations are altered by early life adversity (2019) · cites this paper as [23]
Selective knockout of γ2GABAARs in PV+ interneurons alters theta-gamma coupling.
“A selective knockout of y2GABAARs in PV+ interneurons led to a reduction in theta range oscillations in the hippocampus, altered theta-gamma coupling [87], neuronal population activity patterns that have been shown to be important for memory formation, and impaired spatial learning.”
From An emerging circuit pharmacology of GABAA receptors (2018) · cites this paper as [87]
Selective knockout of γ2GABAARs in PV+ interneurons leads to a reduction in theta range oscillations in the hippocampus.
“A selective knockout of y2GABAARs in PV+ interneurons led to a reduction in theta range oscillations in the hippocampus, altered theta-gamma coupling [87], neuronal population activity patterns that have been shown to be important for memory formation, and impaired spatial learning.”
From An emerging circuit pharmacology of GABAA receptors (2018) · cites this paper as [87]
Selective knockout of γ2GABAARs in PV+ interneurons impairs spatial learning.
“A selective knockout of y2GABAARs in PV+ interneurons led to a reduction in theta range oscillations in the hippocampus, altered theta-gamma coupling [87], neuronal population activity patterns that have been shown to be important for memory formation, and impaired spatial learning.”
From An emerging circuit pharmacology of GABAA receptors (2018) · cites this paper as [87]
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Booker, S. A., Gross, A., Althof, D., Shigemoto, R., Bettler, B., Frotscher, M., Hearing, M., Wickman, K., Watanabe, M., Kulik, Á., et al. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.1186-12.2013 · Cited by 58 · see citing works
Ferando, I., & Mody, I. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.09.010 · Cited by 49 · see citing works
Memory corticalization triggered by REM sleep: mechanisms of cellular and systems consolidation
Almeida-Filho, D. G., Queiroz, C. M., & Ribeiro, S. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2886-9 · Cited by 38 · see citing works
Yu, J., Proddutur, A., Swietek, B., Elgammal, F. S., & Santhakumar, V. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhv199 · Cited by 28 · see citing works
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Spontaneous Infraslow Fluctuations Modulate Hippocampal EPSP-PS Coupling
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- Authors
- Wulff, P., Ponomarenko, A. A., Bartos, M., Korotkova, T. M., Fuchs, E. C., Bähner, F., Both, M., Tort, A. B. L., Kopell, N. J., Wisden, W., & Monyer, H.
- Affiliations
- University of Aberdeen (GB)
- Heidelberg University (DE)
- Boston University (US)
- Department of Clinical Neurobiology, IZN, and
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2009-03-03
- Volume
- 106
- Issue
- 9
- Pages
- 3561-3566
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2637907
- OpenAlex
- W2057397555
- Cited by
- 400
- References
- 56
- Citations by year
- 2026: 10 · 2025: 15 · 2024: 13 · 2023: 16 · 2022: 24 · 2021: 23 · 2020: 24 · 2019: 23 · 2018: 24 · 2017: 24 · 2016: 28 · 2015: 32 · 2014: 23 · 2013: 27 · 2012: 20
- FWCI
- 15.22
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation
- Burroughs Wellcome Fund
- Royal Society
- Deutsche Forschungsgemeinschaft (SFB 505)
- Volkswagen Foundation
- National Institutes of Health
- Medical Research Council
- Leibniz-Gemeinschaft
- National Institute of Neurological Disorders and Stroke (R01 NS46058, R01NS046058)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- hippocampal theta rhythm, gamma oscillations, theta-gamma coupling, parvalbumin interneurons, synaptic inhibition, GABAergic interneurons, CA1, local field potentials
- MeSH terms
- Animals, Behavior, Animal, Electrophysiology, Hippocampus, Interneurons, Models, Neurological, Parvalbumins, Receptors, GABA-A, Synapses, Theta Rhythm, Time Factors, Patch-Clamp Techniques, Protein Subunits, Mice
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.
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