Driving fast-spiking cells induces gamma rhythm and controls sensory responses
Open accessAbstract
Cortical gamma oscillations (20-80 Hz) predict increases in focused attention, and failure in gamma regulation is a hallmark of neurological and psychiatric disease. Current theory predicts that gamma oscillations are generated by synchronous activity of fast-spiking inhibitory interneurons, with the resulting rhythmic inhibition producing neural ensemble synchrony by generating a narrow window for effective excitation. We causally tested these hypotheses in barrel cortex in vivo by targeting optogenetic manipulation selectively to fast-spiking interneurons. Here we show that light-driven activation of fast-spiking interneurons at varied frequencies (8-200 Hz) selectively amplifies gamma oscillations. In contrast, pyramidal neuron activation amplifies only lower frequency oscillations, a cell-type-specific double dissociation. We found that the timing of a sensory input relative to a gamma cycle determined the amplitude and precision of evoked responses. Our data directly support the fast-spiking-gamma hypothesis and provide the first causal evidence that distinct network activity states can be induced in vivo by cell-type-specific activation.
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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 Cardin et al., 2009
The sections “FS activation generates gamma oscillations” and “Natural gamma oscillations require FS activity” support a role for PV-positive fast-spiking interneurons in cortical gamma rhythms. The paper does not establish this claim for basket cells specifically or for ripple oscillations; it reports that stimulating these cells at 8 Hz did not increase 8-Hz power, rather than showing theta generation. It also does not establish maintenance of all three rhythms. Page numbers are unavailable in our copy. (LLM, conf=0.90)
Experimental — accuracy not yet measuredGamma activity has a close link to neuronal spiking, which IIT considers a constituent property of the physical substrate of consciousness.
“Gamma activity was analysed because of its close link to neuronal spiking47, which IIT considers a constituent property of the physical substrate of consciousness5.”
From Adversarial testing of global neuronal workspace and integrated information theories of consciousness (2025) · cites this paper as [47]
Cortical PV cells contribute to synchronous oscillatory activity, particularly in the gamma range.
“Cortical PV cells contribute to synchronous oscillatory activity (Cardin et al., 2009; Sohal et al., 2009; Uhlhaas et al., 2009), particularly in the gamma range (∼30–100 Hz).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Cardin et al., 2009
FS-PV interneurons are at the origin of gamma oscillation in the cortex and contribute to cognitive functions.
“FS-PV interneurons are at the origin of gamma oscillation in the cortex and contribute to cognitive functions.29, 30”
From Cortical fast-spiking parvalbumin interneurons enwrapped in the perineuronal net express the metallopeptidases Adamts8, Adamts15 and Neprilysin (2015) · cites this paper as [29]
Optogenetically driving inhibitory interneurons specifically enhances slow gamma frequency oscillations throughout cortex, reducing circuit noise while amplifying circuit signal.
“Two foundational optogenetic studies demonstrated that optogenetically driving inhibitory interneurons specifically enhances slow gamma frequency oscillations throughout cortex, reducing circuit noise while amplifying circuit signal [201, 202].”
From Apolipoprotein E4, inhibitory network dysfunction, and Alzheimer’s disease (2019) · cites this paper as [201]
Parvalbumin interneurons are critical for high-frequency neuronal synchrony reflected in gamma band oscillations and can also modulate theta band activity and theta-gamma coupling.
“They are critical for high-frequency neuronal synchrony, reflected in gamma band oscillations (30–80 Hz) (Cardin et al., 2009; Fuchs et al., 2007; Gulyas et al., 2010; Massi et al., 2012; Sohal et al., 2009), but can also modulate neuronal activity in the theta band (4–8 Hz), as well as theta-gamma coupling (Korotkova et al., 2010; Wulff et al., 2009).”
From Redox dysregulation, neuroinflammation, and NMDA receptor hypofunction: A “central hub” in schizophrenia pathophysiology? (2016) · cites this paper as Cardin et al., 2009
Stimulating PV-INs increases gamma oscillation patterns, whereas inhibiting PV-INs or downregulating PV at cortical synapses reduces gamma oscillations.
“Stimulation of PV-INs leads to an increase in gamma oscillation patterns, while inhibition of PV-INs or downregulation of PV at cortical synapses reduces gamma oscillations [76][77][78].”
From Parvalbumin interneuron vulnerability and brain disorders (2021) · cites this paper as [76]
Increasing PV-interneuron-mediated feedback inhibition by boosting principal cell activity enhances gamma-band power.
“In contrast, increasing PV-interneuron-mediated feedback inhibition by boosting principal cell activity enhanced gamma-band power (Cardin et al., 2009”
From Neuronal Dynamics and Neuropsychiatric Disorders: Toward a Translational Paradigm for Dysfunctional Large-Scale Networks (2012) · cites this paper as Cardin et al., 2009
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- Authors
- Cardin, J. A., Carlén, M., Meletis, K., Knoblich, U., Zhang, F., Deisseroth, K., Tsai, L.-H., & Moore, C. I.
- Affiliations
- McGovern Institute for Brain Research (US)
- Broad Institute (US)
- Stanford University (US)
- Corresponding author
- Deisseroth, Karl
- Tsai, Li-Huei
- Moore, Christopher I.
- ORCID
- Venue
- Nature
- Published
- 2009-04-26
- Volume
- 459
- Issue
- 7247
- Pages
- 663-667
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC3655711
- OpenAlex
- W2149561999
- Cited by
- 2,603
- References
- 36
- Citations by year
- 2026: 110 · 2025: 145 · 2024: 160 · 2023: 121 · 2022: 172 · 2021: 171 · 2020: 183 · 2019: 154 · 2018: 161 · 2017: 147 · 2016: 151 · 2015: 178 · 2014: 158 · 2013: 157 · 2012: 137
- FWCI
- 70.01
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institute of Neurological Disorders and Stroke (R01NS045130)
- 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
- fast-spiking interneurons, parvalbumin interneurons, optogenetic stimulation, barrel cortex, sensory evoked potentials, pyramidal neurons, neuronal synchronization, attention, schizophrenia, signal-to-noise ratio
- MeSH terms
- Animals, Electrophysiology, Gene Expression Regulation, Interneurons, Photic Stimulation, Rhodopsin, Somatosensory Cortex, Chlamydomonas reinhardtii, Pyramidal Cells, Mice, Gene Knock-In Techniques
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