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Behavioral-state modulation of inhibition is context-dependent and cell type specific in mouse visual cortex
Open accessAbstract
Cortical responses to sensory stimuli are modulated by behavioral state. In the primary visual cortex (V1), visual responses of pyramidal neurons increase during locomotion. This response gain was suggested to be mediated through inhibitory neurons, resulting in the disinhibition of pyramidal neurons. Using in vivo two-photon calcium imaging in layers 2/3 and 4 in mouse V1, we reveal that locomotion increases the activity of vasoactive intestinal peptide (VIP), somatostatin (SST) and parvalbumin (PV)-positive interneurons during visual stimulation, challenging the disinhibition model. In darkness, while most VIP and PV neurons remained locomotion responsive, SST and excitatory neurons were largely non-responsive. Context-dependent locomotion responses were found in each cell type, with the highest proportion among SST neurons. These findings establish that modulation of neuronal activity by locomotion is context-dependent and contest the generality of a disinhibitory circuit for gain control of sensory responses by behavioral state.
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“In the visual cortex, the onset of arousal (as measured by pupil diameter) and locomotion increase neuronal gain32,33,36,37.”
From Mechanisms underlying gain modulation in the cortex (2020) · cites this paper as [36]
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MethodUltrasensitive fluorescent proteins for imaging neuronal activity
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BackgroundMethodInfluentialModulation of visual responses by behavioral state in mouse visual cortex
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“(A) Schematic of the connectivity between pyramidal neurons (Pyr) and subtypes of inhibitory neurons, vasoactive intestinal peptide (VIP), somatostatin (SST) and parvalbumin (PV) expressing neurons, established from in vitro studies in V1 (Pfeffer et al., 2013; Jiang et al., 2015).”
BackgroundResultInfluentialCortical interneurons that specialize in disinhibitory control
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BackgroundInfluentialOntogeny of the VIP+ interneuron sensory-motor circuit prior to active whiskingPreprint
Vagnoni, C., Baruchin, L. J., Ghezzi, F., Ratti, S., Molnár, Z., & Butt, S. J. B. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.07.01.182238 · Cited by 6
“…well positioned to exert varied effects as described in the juvenile and adult cortex (Batista-Brito et al., 2017; Bigelow et al., 2019; Cardin, 2019; Dipoppa et al., 2018; Fu et al., 2014; Garrett et al., 2020; Keller et al., 2020; Millman et al., 2019; Pakan et al., 2016; Pi et al., 2013).”
BackgroundDearnley, B., Dervinis, M., Shaw, M., & Okun, M. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.08.22.457198 · Cited by 8
“…observed that arousal produced a bidirectional modulation of ongoing activity (Niell and Stryker, 2010; Erisken et al., 2014; Vinck et al., 2015; Pakan et al., 2016; Dipoppa et al., 2018), with considerable differences between modulation locked to pupil size in immobile animals and modulation…”
BackgroundJordan, R., & Keller, G. B. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.11.08.515698 · Cited by 7
Liu, J., & Kanold, P. O. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.12.12.520155 · Cited by 9
“In the auditory system, this framework has been proposed to explain phenomena such as Stimulus Specific Adaptation (SSA) and Mismatch Negativity (MMN) (Carbajal and Malmierca, 2018), where less common oddball stimulus evokes larger neuronal responses along the auditory pathway than the common standard stimulus (Parras…”
BackgroundState modulation in spatial networks with three interneuron subtypesPreprint
Edwards, M., Jonathan Rubin, A., & Huang, C. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.08.23.609417 · Cited by 7
“Arousal and locomotion state of an animal have been shown to exert diverse influences on the firing rates of interneuron subtypes [12, 13, 14] and to strongly impact the synchrony level of neural population responses [15, 16].”
State modulation in spatial networks with three interneuron subtypes
Edwards, M. M., Rubin, J. E., & Huang, C. (2025) · Science Advances · doi:10.1126/sciadv.ads9134 · Cited by 13
Feature-tuned synaptic inputs to somatostatin interneurons drive context-dependent processing
Hendricks, W. D., Sadahiro, M., Mossing, D., Veit, J., & Adesnik, H. (2026) · Neuron · doi:10.1016/j.neuron.2025.12.021 · Cited by 8
Functional Roles of Cortical Inhibitory Interneurons
Shin, H., & Adesnik, H. (2023) · Oxford University Press eBooks · doi:10.1093/med/9780197676158.003.0008 · Cited by 4
The essential role of feedback processing for figure-ground perception in micePreprint
Kirchberger, L., Mukherjee, S., Schnabel, U. H., van Beest, E. H., Barsegyan, A., Levelt, C. N., Heimel, J. A., Lorteije, J. A. M., van der Togt, C., Self, M. W., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/456459 · Cited by 8
Spiking activity in the visual thalamus is coupled to pupil dynamics across temporal scalesPreprint
Crombie, D., Spacek, M. A., Leibold, C., & Busse, L. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.04.30.442134 · Cited by 6
Cammarata, C. M., Pei, Y., Hu, T., Shields, B. C., Lim, S. S. X., Hawley, T. M., Li, J. Y., St-Amand, D., Brunel, N., Tadross, M. R., et al. (2025) · Cell Reports · doi:10.1016/j.celrep.2025.115954 · Cited by 8
“18,22,23 25-27 Indeed, optogenetic suppression of SST cells enhances inhibition onto neighboring pyramidal cells, consistent with perturbation of an ISN.”
InfluentialBehavioral and neuro-functional consequences of eliminating the KCNQ3 GABA binding site in mice
Chen, K. J., Yoshimura, R. F., Edmundo, C. A., Truong, T. M., Civelli, O., Alachkar, A., & Abbott, G. W. (2023) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2023.1192628 · Cited by 4
“For example, the activity of GABAergic-VIP neurons increases, whereas the activities of GABAergic-SST neurons increase or decrease during locomotion (Pfeffer et al., 2013; Polack et al., 2013; Fu et al., 2014; Reimer et al., 2014; Pakan et al., 2016; Urban-Ciecko and Barth, 2016; Dipoppa et al., 2018).”
BackgroundThe generation of cortical interneurons
Batista‐Brito, R., Ward, C., & Fishell, G. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-814405-3.00020-5 · Cited by 6
Running modulates primate and rodent visual cortex differentlyPreprint
Liska, J. P., Rowley, D. P., Nguyen, T. T. K., Muthmann, J.-O., Butts, D. A., Yates, J. L., & Huk, A. C. (2023) · eLife · doi:10.7554/elife.87736.1 · Cited by 5
Ding, X., Vogler, N. W., Tobin, M., Garami, L., Lesicko, A. M. H., Wood, K. C., & Geffen, M. N. (2026) · Journal of Neuroscience · doi:10.1523/jneurosci.0827-25.2026 · Cited by 3
“While VIP neurons have been implicated in disinhibitory circuits across sensory cortical regions (Mesik et al., 2015; Pakan et al., 2016; Kuchibhotla et al., 2017; Cone et al., 2019; Millman et al., 2020; Myers-Joseph et al., 2024; Tobin et al., 2024) and have been implicated in oddball and…”
Brain region-specific gain modulation of place cells by VIP neurons
Lenkey, N., Garvert, A. C., Neubrandt, M., Kriener, B., & Vervaeke, K. (2025) · Nature Communications · doi:10.1038/s41467-025-60679-4 · Cited by 5
Kaneko, M., Hoseini, M. S., Waschek, J. A., & Stryker, M. P. (2024) · Journal of Neurophysiology · doi:10.1152/jn.00463.2023 · Cited by 4
Dai, J., & Sun, Q. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114672 · Cited by 3
“14,25,36,37 Increased locomotion following the delivery of air puff suggests an increase in the arousal levels.”
Chronic Two-Photon Calcium Imaging in the Visual Cortex of Awake Behaving Mice
Dylda, E., Pakan, J. M. P., & Rochefort, N. L. (2018) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-812028-6.00013-6 · Cited by 5
Self-citationFrancioni, V., Padamsey, Z., & Rochefort, N. L. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/664177 · Cited by 5
Self-citationVisual acuity performance level is independent of locomotionPreprint
Swain, A. D., Park, E., Cheng, Z., Kowalewski, N. N., Sun, A., Allen, T., & Kuhlman, S. J. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/750844 · Cited by 4
“…activates a powerful subcortical circuit that is associated with an increase in response gain in the visual cortex of mice (Ayaz et al., 2013; Bennett et al., 2013; Dipoppa et al., 2018; Erisken et al., 2014; Keller et al., 2012; Lee et al., 2014; Niell and Stryker, 2010; Pakan et al., 2016).”
BackgroundHeintz, T. G., Hinojosa, A. J., & Lagnado, L. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.01.16.909788 · Cited by 4
“For instance, larger stimuli (>30°) increase the activity of SST interneurons particularly strongly (Dipoppa et al., 2018; Pakan et al., 2016).”
BackgroundInfluentialDevelopmental trajectory of cortical somatostatin interneuron functionPreprint
Wang, A. Y., Ferguson, K., Gupta, J., Higley, M. J., & Cardin, J. A. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.03.05.583539 · Cited by 5
“SST-IN activity increases during locomotion 11 , leading to a locomotion-induced increase in SST-IN visual response gain 8,16,19 that may contribute to state-dependent visual perceptual performance via inhibition of nearby PN dendrites.”
BackgroundUnexpected Events Modulate Context Signaling in VIP and Excitatory Cells of the Visual CortexPreprint
Najafi, F., Russo, S., & Lecoq, J. A. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.05.15.594366 · Cited by 4
“VIP activity increases with pupil dilation 21 , locomotion 4,22 , and whisking 3,23 , leading to enhanced sensory modulation during high attention and arousal states that follow surprising and reinforcement signals 4,20–22, 24, 25 .”
BackgroundHuang, S., Rizzo, D., Wu, S. J., Xu, Q., Ziane, L., Alghamdi, N., Stafford, D. A., Daigle, T. L., Tasic, B., Zeng, H., et al. (2024) · Research Square · doi:10.1101/2024.06.05.597539 · Cited by 5
“Our findings, along with those of others, have indicated that both LAMP5+ cINs and VIP+ cINs exhibit spontaneous activity highly correlated with locomotion speed in awake, behaving mice 38,39 .”
Bogaj, K., & Urban‐Ciećko, J. (2025) · The Journal of Physiology · doi:10.1113/jp286439 · Cited by 3
Characterization of iGABASnFR2 for in vivo mesoscale imaging of intracortical GABA dynamics
Rezaei, E., Tohidi, S., Nazari, M., & Abadchi, J. K. (2025) · Neurophotonics · doi:10.1117/1.nph.12.3.035006 · Cited by 4
“47”
Quantitative synapse analysis for cell-type specific connectomicsPreprint
Kuljis, D. A., Zemoura, K., Telmer, C. A., Lee, J., Park, E., Ackerman, D. S., Xu, W., Watkins, S. C., Arnold, D. B., Bruchez, M. P., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/386912 · Cited by 3
“Although this may be incongruous with the simplified model that contrasts soma-targeting PV and dendrite-targeting SST inputs (Chen et al., 2015; Higley, 2014; Lazarus and Huang, 2011; Pakan et al., 2016; Pi et al., 2013), prior experimental data are much less categorical than these schema suggest.”
MethodPrinciples Governing the Dynamics of GABAergic Interneurons in the Barrel CortexPreprint
Yu, J., Hu, H., Agmon, A., & Svoboda, K. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/554949 · Cited by 3
“…electrophysiology as a critical tool for unraveling functional relationships between neural activity and behavior at fine time-scales, which cannot be substituted with other methods, including monosynaptic tracing (Wall et al., 2016), or calcium imaging (Dipoppa et al., 2018; Pakan et al., 2016).”
Richter, L. M. A., & Gjorgjieva, J. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.05.25.445562 · Cited by 3
“…2010), response reversal during top-down modulation (Dipoppa et al., 2018; Fu et al., 2014; Garcia del Molino et al., 2017; Keller et al., 2020; Pakan et al., 2016), and shown to affect surround suppression (Adesnik et al., 2012; Ayaz et al., 2013; Litwin-Kumar et al., 2016; Ozeki et al.,…”
BackgroundSomatostatin interneurons in auditory cortex contribute to perceptual categorizationPreprint
Chai, R., Zhang, Y., Xin, Y., Deng, L., & Xu, N.-L. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.07.06.498950 · Cited by 4
Metadata
- Authors
- Pakan, J. M., Lowe, S. C., Dylda, E., Keemink, S. W., Currie, S. P., Coutts, C. A., & Rochefort, N. L.
- Affiliations
- University of Edinburgh (GB)
- University of Freiburg (DE)
- Corresponding author
- Rochefort, Nathalie L
- ORCID
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2016-08-23
- Volume
- 5
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC5030095
- OpenAlex
- W2515318112
- Cited by
- 282
- References
- 43
- Citations by year
- 2026: 12 · 2025: 25 · 2024: 34 · 2023: 47 · 2022: 31 · 2021: 17 · 2020: 29 · 2019: 29 · 2018: 30 · 2017: 26 · 2016: 2
- FWCI
- 18.46
- Type
- journal article
- Language
- en
- Update notices
- correction (2017-09-06)
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, cc-by)
- Funders
- European Commission (Marie Curie Actions (FP7), IEF 624461, EuroSpin Erasmus Mundus Program, Marie Curie Actions (FP7), MC-CIG 631770)
- University Of Edinburgh (Doctoral Training Centre in Neuroinformatics, Graduate School of Life Sciences, Chancellor's fellow starting grant)
- Engineering and Physical Sciences Research Council (Doctoral Training Centre in Neuroinformatics, EP/F500385/1, Doctoral Training Centre in Neuroinformatics, BB/F529254/1)
- Patrick Wild Centre
- The Shirley Foundation
- RS MacDonald Charitable Trust (Seedcorn Grant 21)
- Wellcome Trust (Sir Henry Dale fellowship, 102857/Z/13/Z)
- Royal Society (Sir Henry Dale fellowship, 102857/Z/13/Z)
- 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
- primary visual cortex, locomotion, behavioral state, disinhibition, gain control, vasoactive intestinal peptide interneurons, somatostatin interneurons, parvalbumin interneurons, pyramidal neurons, inhibitory interneurons, context-dependent responses
- MeSH terms
- Animals, Behavior, Animal, Interneurons, Locomotion, Models, Neurological, Visual Cortex, Pyramidal Cells, Mice
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