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Parvalbumin neurons and gamma rhythms enhance cortical circuit performance
Open accessAbstract
Synchronized oscillations and inhibitory interneurons have important and interconnected roles within cortical microcircuits. In particular, interneurons defined by the fast-spiking phenotype and expression of the calcium-binding protein parvalbumin have been suggested to be involved in gamma (30-80 Hz) oscillations, which are hypothesized to enhance information processing. However, because parvalbumin interneurons cannot be selectively controlled, definitive tests of their functional significance in gamma oscillations, and quantitative assessment of the impact of parvalbumin interneurons and gamma oscillations on cortical circuits, have been lacking despite potentially enormous significance (for example, abnormalities in parvalbumin interneurons may underlie altered gamma-frequency synchronization and cognition in schizophrenia and autism). Here we use a panel of optogenetic technologies in mice to selectively modulate multiple distinct circuit elements in neocortex, alone or in combination. We find that inhibiting parvalbumin interneurons suppresses gamma oscillations in vivo, whereas driving these interneurons (even by means of non-rhythmic principal cell activity) is sufficient to generate emergent gamma-frequency rhythmicity. Moreover, gamma-frequency modulation of excitatory input in turn was found to enhance signal transmission in neocortex by reducing circuit noise and amplifying circuit signals, including inputs to parvalbumin interneurons. As demonstrated here, optogenetics opens the door to a new kind of informational analysis of brain function, permitting quantitative delineation of the functional significance of individual elements in the emergent operation and function of intact neural circuitry.
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In the citing paper
“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 Sohal et al., 2009
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“We used a sensory paradigm to induce a synchronous activated state in the prefrontal neuronal circuitry and, thus, elicit u oscillations with a nested g activity (Sohal et al., 2009)”
From Perineuronal Nets Regulate the Inhibitory Perisomatic Input onto Parvalbumin Interneurons and γ Activity in the Prefrontal Cortex (2020) · cites this paper as Sohal et al., 2009
Experimental — accuracy not yet measuredThe check wasn’t confident either way, so it gives no verdict — never disputed.
In the citing paper
“Fast-spiking properties consequently impose high metabolic demand and increased mitochondrial density, which renders PV cells, but not other interneurons such as calretinin and calbindin cells, particularly sensitive to oxidative stress (3).”
From Perineuronal nets protect fast-spiking interneurons against oxidative stress (2013) · cites this paper as [3]
Experimental — accuracy not yet measuredThe check wasn’t confident either way, so it gives no verdict — never disputed.
In the citing paper
“Furthermore, the antioxidant N-acetylcysteine prevents the GBRinduced PV-cell defect in Gclm KO mice (3).”
From Perineuronal nets protect fast-spiking interneurons against oxidative stress (2013) · cites this paper as [3]
Experimental — accuracy not yet measuredIn the citing paper
“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 Sohal et al., 2009
In the citing paper
“Cortical gamma band oscillations have been attributed to GABAergic cell activity, in particular PV interneurons (Sohal et al., 2009).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Sohal et al., 2009
In the citing paper
“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 [30]
In the citing paper
“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 [202]
In the citing paper
“there is evidence that gamma oscillations may facilitate cortical circuit performance and enhance information transmission by increasing signal-to-noise ratio within neocortical circuits (Sohal et al, 2009).”
From Neural Correlates of Three Promising Endophenotypes of Depression: Evidence from the EMBARC Study (2016) · cites this paper as Sohal et al, 2009
In the citing paper
“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 [77]
In the citing paper
“Inhibition of PV interneurons led to an immediate suppression of 30–80 Hz oscillations while 10–30 Hz oscillations increased in power.”
From Neuronal Dynamics and Neuropsychiatric Disorders: Toward a Translational Paradigm for Dysfunctional Large-Scale Networks (2012) · cites this paper as Sohal et al., 2009
In the citing paper
“Increasingly, evidence is emerging that decreased inhibition is a critical contributor to E/I imbalance in ASD40.”
From Regulation of autism-relevant behaviors by cerebellar-prefrontal cortical circuits (2020) · cites this paper as [40]
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Metadata
- Authors
- Sohal, V. S., Zhang, F., Yizhar, O., & Deisseroth, K.
- Affiliations
- Stanford University (US)
- Corresponding author
- Deisseroth, Karl
- Venue
- Nature
- Published
- 2009-04-26
- Volume
- 459
- Issue
- 7247
- Pages
- 698-702
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC3969859
- OpenAlex
- W2047347093
- Cited by
- 2,606
- References
- 31
- Citations by year
- 2026: 118 · 2025: 143 · 2024: 155 · 2023: 138 · 2022: 169 · 2021: 183 · 2020: 190 · 2019: 143 · 2018: 154 · 2017: 172 · 2016: 171 · 2015: 158 · 2014: 143 · 2013: 151 · 2012: 136
- FWCI
- 67.26
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- 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
- National Institute of Neurological Disorders and Stroke (F31NS059160)
- 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, gamma oscillations, fast-spiking interneurons, cortical circuits, optogenetics, signal-to-noise ratio, sensory input, cortical inhibition, schizophrenia, autism spectrum disorder, neocortex, neuronal synchronization, information processing, attention, signal decoding
- MeSH terms
- Animals, Cell Line, Cerebral Cortex, Cortical Synchronization, Electrophysiology, Evoked Potentials, Interneurons, Parvalbumins, Periodicity, Photic Stimulation, Signal Transduction, Prefrontal Cortex, Neocortex, Mice
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