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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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 Sohal et al., 2009
The supplied passages (labelled Abstract; no page given) show that manipulating fast-spiking PV interneurons affected gamma oscillations. The paper says further work is needed to distinguish basket cells from other PV-interneuron subtypes, so it does not establish a basket-cell-specific role. Its theta findings concern responses to imposed rhythms, not their generation or maintenance, and the passages do not address ripple oscillations. (LLM, conf=0.90)
Experimental — accuracy not yet measuredA sensory paradigm can induce a synchronous activated state in the prefrontal neuronal circuitry and elicit theta oscillations with nested gamma activity.
“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
The paper reports that rhythmic light stimulation induced theta- or gamma-frequency firing in pyramidal neurons, and it also tested prefrontal pyramidal neurons (section labeled Abstract; page unavailable). It does not show that a sensory paradigm induced a synchronous activated prefrontal state or theta oscillations with gamma activity nested within them; theta and gamma were applied as separate stimulation patterns. (LLM, conf=0.86)
Experimental — accuracy not yet measuredFast-spiking properties impose high metabolic demand and increased mitochondrial density, rendering PV cells, but not other interneurons such as calretinin and calbindin cells, particularly sensitive to oxidative stress.
“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]
The passages on PV interneurons and gamma rhythms (section labeled Abstract; page unavailable) identify PV cells as fast-spiking, but do not address metabolic demand, mitochondrial density, or oxidative-stress sensitivity. Searches for those terms and for the comparison with calretinin and calbindin cells found no passage supporting the attributed causal claim. (LLM, conf=0.72)
Experimental — accuracy not yet measuredThe antioxidant N-acetylcysteine prevents the GBR-induced PV-cell defect in Gclm KO mice.
“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]
The paper’s Abstract and Methods Summary describe optogenetic experiments in PV::Cre mice, not antioxidant treatment in Gclm knockout mice. Searches for N-acetylcysteine, GBR, Gclm knockout mice, and oxidative stress found no passage addressing the claimed prevention of a PV-cell defect; page numbers were unavailable. (LLM, conf=0.78)
Experimental — accuracy not yet measuredCortical 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 Sohal et al., 2009
Cortical gamma band oscillations have been attributed to GABAergic cell activity, in particular PV interneurons.
“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
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 [30]
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 [202]
There is evidence that gamma oscillations may facilitate cortical circuit performance and enhance information transmission by increasing signal-to-noise ratio within neocortical circuits.
“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
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 [77]
Inhibition of PV interneurons leads to an immediate suppression of 30-80 Hz oscillations while 10-30 Hz oscillations increase in power.
“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
Decreased inhibition is a critical contributor to E/I imbalance in ASD.
“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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- 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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