Parvalbumin-expressing interneurons linearly transform cortical responses to visual stimuli
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The response of cortical neurons to a sensory stimulus is shaped by the network in which they are embedded. Here we establish a role of parvalbumin (PV)-expressing cells, a large class of inhibitory neurons that target the soma and perisomatic compartments of pyramidal cells, in controlling cortical responses. By bidirectionally manipulating PV cell activity in visual cortex we show that these neurons strongly modulate layer 2/3 pyramidal cell spiking responses to visual stimuli while only modestly affecting their tuning properties. PV cells' impact on pyramidal cells is captured by a linear transformation, both additive and multiplicative, with a threshold. These results indicate that PV cells are ideally suited to modulate cortical gain and establish a causal relationship between a select neuron type and specific computations performed by the cortex during sensory processing.
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In mouse visual cortex, fast-spiking neurons are more broadly selective for orientation, direction and spatial frequency than pyramidal cells.
“in mouse visual cortex, selectivity to visual stimuli such as orientation, direction, and spatial frequency are broader for FS neurons than for pyramidal cells”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as Atallah et al., 2012
The Results section, “Visual Responses of PV Cells Are Distinct from Those of Pyr Cells” (page unavailable), reports that PV cells—identified there as fast-spiking—were less orientation-selective and more broadly orientation-tuned than pyramidal cells. The paper discusses direction selectivity when PV-cell activity is perturbed, but does not establish that PV cells are more broadly direction-selective than pyramidal cells. The Visual Stimulation methods (page unavailable) say spatial frequency was set to each cell’s preference; they do not report the claimed comparison in spatial-frequency selectivity. (LLM, conf=0.88)
Experimental — accuracy not yet measuredCortical interneurons are generally more broadly tuned than nearby principal cells, but different interneuron types show varying degrees of sensory tuning.
“It appears that for the most part cortical INs are more broadly tuned than nearby PCs, yet different INs show various degrees of sensory tuning.”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as Atallah et al., 2012
The Results section, “Visual Responses of PV Cells Are Distinct from Those of Pyr Cells,” reports that parvalbumin-expressing interneurons were more broadly tuned to visual-stimulus orientation than pyramidal cells. But the paper studies this one interneuron class; its Discussion calls for future comparisons with other classes rather than establishing that different interneuron types have varying degrees of sensory tuning. The claim also generalizes the PV-cell finding to cortical interneurons overall. (LLM, conf=0.87)
Experimental — accuracy not yet measuredResults from optogenetic studies disagree about the specific role of each interneuron group in tuning.
“However, the results from these studies do not agree on the specific role of each interneuron group.”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as Atallah et al., 2012
The Introduction says the specific roles of distinct inhibitory-neuron types in sensory processing were unknown. The Results also contrast this paper’s findings on PV-cell visual responses with a previous report. Neither passage establishes that optogenetic studies disagree about the role of each interneuron group in tuning; this study directly tests PV cells, not each group. (LLM, conf=0.76)
Experimental — accuracy not yet measuredPV and Sst inhibitory neurons play distinct roles in tuning excitatory neurons, producing either divisive or subtractive inhibition.
“These studies demonstrated that PV and Sst inhibitory neurons play distinct roles in the tuning of excitatory neurons producing either divisive or subtractive inhibition.”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as Atallah et al., 2012
The Results section, “A Linear Function Describes How PV Cells Control Pyr Cell Visual Responses” (page unavailable), reports that activating PV cells both multiplied pyramidal-cell responses by 0.7 and subtracted a constant amount. The paper studies PV cells, not Sst cells; its Discussion calls comparisons with other inhibitory cell types a subject for future work. It therefore does not establish distinct PV and Sst roles or assign divisive versus subtractive inhibition to the two types. (LLM, conf=0.89)
Experimental — accuracy not yet measuredSome studies found that Sst interneurons sharpen orientation tuning, while activating PV interneurons has a minor effect on tuning but changes response gain.
“Some studies found that Sst INs sharpen orientation tuning (Wilson et al., 2012), while activation of PV INs was found to have a minor effect on tuning but changed response gain”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as Atallah et al., 2012
Brief spikes in the axon and terminals contribute to fast and synchronous transmitter release.
“Brief spikes in the axon and terminals contribute to fast and synchronous transmitter release12.”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as [12]
The Results and Conductance-Based Model sections address how parvalbumin interneurons affect visual responses and synaptic inhibition, not whether brief spikes in axons or terminals enable fast, synchronous transmitter release. Searches for axon terminals, spike duration, and synchronous release found no passage addressing that mechanism; page numbers were unavailable in our copy. (LLM, conf=0.74)
Experimental — accuracy not yet measuredFS cell axons contain a very high density of Na+ channels and prominent Kv3 channels.
“FS cell axons contain an excessively high density of Na+ channels and prominent expression of Kv3 channels12.”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as [12]
The Results section (‘Visual Responses of PV Cells Are Distinct from Those of Pyr Cells’; page unavailable) describes PV cells as consistent with the fast-spiking type, but does not address ion channels in their axons. Searches for axonal Na+ channel density and Kv3 expression found no passage supporting either part of the claim. (LLM, conf=0.74)
Experimental — accuracy not yet measuredInterneuron dysfunction could contribute to altered sensory perception and deficits in working memory, attention, and learning.
“Ultimately, interneuron dysfunction could contribute to altered sensory perception (Atallah et al., 2012), deficits in working memory (Korotkova et al., 2010; Roux et al., 2012), attention (Rouhinen et al., 2013), and learning (Carlen et al., 2012).”
From Redox dysregulation, neuroinflammation, and NMDA receptor hypofunction: A “central hub” in schizophrenia pathophysiology? (2016) · cites this paper as Atallah et al., 2012
This dynamic range can be adjusted through gain control mediated by the overall level of synaptic inhibition.
“In turn, this dynamic range can be adjusted through gain control that is mediated by the overall level of synaptic inhibition4,59,68,69.”
From Mechanisms underlying gain modulation in the cortex (2020) · cites this paper as [68]
GABAergic inhibition controls the sensitivity of V1 neurons in rodents and cats by specifically adjusting their response gain without altering local selectivity or input gain.
“GABAergic inhibition controls the sensitivity of V1 neurons in rodents and cats by specifically adjusting their response gain without altering local selectivity or input gain2,68,69,101–104.”
From Mechanisms underlying gain modulation in the cortex (2020) · cites this paper as [68]
Optogenetic manipulations of interneurons provide evidence of cell type-specific effects of inhibitory interneurons on gain regulation.
“Optogenetic manipulations of interneurons provide evidence of cell type-specific effects of inhibitory interneurons on gain regulation2,68,104,105,107.”
From Mechanisms underlying gain modulation in the cortex (2020) · cites this paper as [68]
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Massi, L., Lagler, M., Hartwich, K., Borhegyi, Z., Somogyi, P., & Klausberger, T. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.3475-12.2012 · Cited by 88 · see citing works
Kaplan, E. S., Cooke, S. F., Komorowski, R. W., Chubykin, A. A., Thomazeau, A., Khibnik, L. A., Gavornik, J. P., & Bear, M. F. (2016) · eLife · doi:10.7554/elife.11450 · Cited by 77 · see citing works
Runyan, C. A., & Sur, M. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2196-12.2013 · Cited by 67 · see citing works
Interneuron control of hippocampal oscillations
Allen, K., & Monyer, H. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.08.016 · Cited by 64 · see citing works
Cortical balance of excitation and inhibition is regulated by the rate of synaptic activity
Taub, A. H., Katz, Y., & Lampl, I. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.1748-13.2013 · Cited by 63 · see citing works
The contribution of synaptic location to inhibitory gain control in pyramidal cells
Pouille, F., Watkinson, O., Scanziani, M., & Trevelyan, A. J. (2013) · Physiological Reports · doi:10.1002/phy2.67 · Cited by 65 · see citing works
Self-citationResponse-dependent dynamics of cell-specific inhibition in cortical networks in vivo
El-Boustani, S., & Sur, M. (2014) · Nature Communications · doi:10.1038/ncomms6689 · Cited by 61 · see citing works
Rupert, D. D., & Shea, S. D. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2022.886629 · Cited by 58 · see citing works
Serotonin Decreases the Gain of Visual Responses in Awake Macaque V1
Seillier, L., Lorenz, C., Kawaguchi, K., Ott, T., Nieder, A., Pourriahi, P., & Nienborg, H. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.1339-17.2017 · Cited by 57 · see citing works
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Cortical Control of Spatial Resolution by VIP<sup>+</sup>Interneurons
Ayzenshtat, I., Karnani, M. M., Jackson, J., & Yuste, R. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.1920-16.2016 · Cited by 50 · see citing works
Inhibitory Neurons: Vip Cells Hit the Brake on Inhibition
Pfeffer, C. K. (2014) · Current Biology · doi:10.1016/j.cub.2013.11.001 · Cited by 43 · see citing works
Atallah, B. V., Scanziani, M., & Carandini, M. (2014) · Nature · doi:10.1038/nature13129 · Cited by 34 · see citing works
Self-citationRegulation of Cortical Dynamic Range by Background Synaptic Noise and Feedforward Inhibition
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- Authors
- Atallah, B. V., Bruns, W., Carandini, M., & Scanziani, M.
- Affiliations
- University of California San Diego (US)
- Howard Hughes Medical Institute (US)
- University College London (GB)
- Corresponding author
- Atallah, Bassam V.
- Scanziani, Massimo
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2012-01
- Volume
- 73
- Issue
- 1
- Pages
- 159-170
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC3743079
- OpenAlex
- W2009759904
- Cited by
- 612
- References
- 52
- Citations by year
- 2026: 23 · 2025: 43 · 2024: 39 · 2023: 31 · 2022: 46 · 2021: 46 · 2020: 62 · 2019: 36 · 2018: 43 · 2017: 44 · 2016: 45 · 2015: 36 · 2014: 46 · 2013: 49 · 2012: 22
- FWCI
- 24.74
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 1054 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- Gatsby Charitable Foundation
- National Institutes of Health (NS061521)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- parvalbumin interneurons, inhibitory interneurons, visual cortex, layer 2/3 pyramidal cells, linear operators, perisomatic inhibition, sensory processing
- MeSH terms
- Channelrhodopsins, Action Potentials, Animals, Animals, Newborn, Evoked Potentials, Visual, Interneurons, Light, Mice, Transgenic, Models, Neurological, Orientation, Parvalbumins, Photic Stimulation, Transduction, Genetic, Visual Cortex, Visual Pathways, Linear Models, Pyramidal Cells, Patch-Clamp Techniques, Mice
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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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