Inhibition-induced theta resonance in cortical circuits
Open accessAbstract
Both circuit and single-cell properties contribute to network rhythms. In vitro, pyramidal cells exhibit theta-band membrane potential (subthreshold) resonance, but whether and how subthreshold resonance translates into spiking resonance in freely behaving animals is unknown. Here, we used optogenetic activation to trigger spiking in pyramidal cells or parvalbumin immunoreactive interneurons (PV) in the hippocampus and neocortex of freely behaving rodents. Individual directly activated pyramidal cells exhibited narrow-band spiking centered on a wide range of frequencies. In contrast, PV photoactivation indirectly induced theta-band-limited, excess postinhibitory spiking in pyramidal cells (resonance). PV-inhibited pyramidal cells and interneurons spiked at PV-inhibition troughs, similar to CA1 cells during spontaneous theta oscillations. Pharmacological blockade of hyperpolarization-activated (I(h)) currents abolished theta resonance. Inhibition-induced theta-band spiking was replicated in a pyramidal cell-interneuron model that included I(h). Thus, PV interneurons mediate pyramidal cell spiking resonance in intact cortical networks, favoring transmission at theta frequency.
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PV-expressing basket cells have critical roles in generating and maintaining gamma, theta and ripple oscillations.
“strong evidence supporting the view that PV-expressing basket cells have critical roles in the generation and maintenance of gamma, theta and ripple oscillations”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as Stark et al., 2013
The Results report that PV-cell activation induced theta-band spiking in pyramidal cells, and the Discussion says this mechanism may amplify theta-range spiking in local circuits. The paper does not establish a critical role in generating or maintaining gamma or ripple oscillations. It also reports that focal PV-cell stimulation did not change the frequency or phase of the global theta rhythm. (LLM, conf=0.87)
Experimental — accuracy not yet measuredSingle isolated units were classified into putative pyramidal neurons and FS interneurons using a 2-D Gaussian mixture model based on spike waveform features, and only units with posterior probability greater than 0.95 were included.
“Single isolated units were further classified into putative pyramidal neurons and FS interneurons using a 2-D Gaussian mixture model (GMM) based on spike waveform features (spike half-width and trough-to-peak time). Only units belonging to a cluster with a posterior probability greater than 0.95 were included in the analysis126.”
From Place and behavioral modulation of hippocampal neurons during immobility (2026) · cites this paper as [126]
The Experimental Procedures say that well-isolated units were classified as putative pyramidal cells or interneurons, with a waveform-based Gaussian-mixture classifier used as one of several methods. They do not specify a two-dimensional model, the claimed waveform features, or a posterior-probability threshold of 0.95; the reported p<0.05 classification criterion is not that threshold. The paper also describes the classified group as interneurons, not exclusively fast-spiking interneurons. (LLM, conf=0.88)
Experimental — accuracy not yet measuredPV+ interneurons appear to be the main generators of intrinsic theta oscillations in the hippocampus.
“PV+ interneurons appear to be the main generators of intrinsic theta oscillations in the hippocampus (24).”
From Perineuronal nets, inhibitory interneurons and anxiety-related ventral hippocampal neuronal oscillations are altered by early life adversity (2019) · cites this paper as [24]
GABAergic interneurons, especially the PV+ subtype, play an important role in the regulation of neuronal oscillations in the brain.
“GABAergic interneurons, especially the PV+ subtype, play an important role in the regulation of neuronal oscillations in the brain (24–27) and have also been implicated in neuropsychiatric disease (66; 67).”
From Perineuronal nets, inhibitory interneurons and anxiety-related ventral hippocampal neuronal oscillations are altered by early life adversity (2019) · cites this paper as [24]
PV+ basket cells have been implicated in theta generation in vivo.
“we focused on PV+ basket cells, which have been implicated in theta generation in vivo (Soltesz and Deschênes, 1993; Buzsáki, 2002; Stark et al., 2013; Hu et al., 2014)”
From Interneuronal mechanisms of hippocampal theta oscillations in a full-scale model of the rodent CA1 circuit (2016) · cites this paper as Stark et al., 2013
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- Authors
- Stark, E., Eichler, R., Roux, L., Fujisawa, S., Rotstein, H. G., & Buzsáki, G.
- Affiliations
- New York University (US)
- New Jersey Institute of Technology (US)
- Corresponding author
- Stark, Eran
- Buzsáki, György
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2013-12
- Volume
- 80
- Issue
- 5
- Pages
- 1263-1276
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC3857586
- OpenAlex
- W2088358935
- Cited by
- 326
- References
- 66
- Citations by year
- 2026: 9 · 2025: 37 · 2024: 18 · 2023: 23 · 2022: 26 · 2021: 27 · 2020: 26 · 2019: 24 · 2018: 20 · 2017: 32 · 2016: 35 · 2015: 25 · 2014: 23 · 2013: 1
- FWCI
- 15.30
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- HAL (submittedVersion, other-oa)
- Radboud Repository (Radboud University) (submittedVersion)
- Funders
- National Institute of Mental Health (R01MH054671, MH54671)
- National Institute of Neurological Disorders and Stroke (NS074015, R01NS034994, NS034994, R01NS074015)
- 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
- parvalbumin interneurons, pyramidal neurons, hyperpolarization-activated current, hippocampus, neocortex, optogenetic stimulation, theta oscillations, cortical circuits
- MeSH terms
- Channelrhodopsins, Action Potentials, Animals, Biophysics, Cerebral Cortex, Electric Stimulation, Hippocampus, Interneurons, Mice, Inbred C57BL, Mice, Transgenic, Nerve Net, Neural Inhibition, Parvalbumins, Theta Rhythm, Patch-Clamp Techniques, Green Fluorescent Proteins, Mice, Calcium-Calmodulin-Dependent Protein Kinase Type 2, Optogenetics, 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.
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