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A Cortical Circuit for Gain Control by Behavioral State
Open accessAbstract
The brain's response to sensory input is strikingly modulated by behavioral state. Notably, the visual response of mouse primary visual cortex (V1) is enhanced by locomotion, a tractable and accessible example of a time-locked change in cortical state. The neural circuits that transmit behavioral state to sensory cortex to produce this modulation are unknown. In vivo calcium imaging of behaving animals revealed that locomotion activates vasoactive intestinal peptide (VIP)-positive neurons in mouse V1 independent of visual stimulation and largely through nicotinic inputs from basal forebrain. Optogenetic activation of VIP neurons increased V1 visual responses in stationary awake mice, artificially mimicking the effect of locomotion, and photolytic damage of VIP neurons abolished the enhancement of V1 responses by locomotion. These findings establish a cortical circuit for the enhancement of visual response by locomotion and provide a potential common circuit for the modulation of sensory processing by behavioral state.
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“More recently, a number of functional studies in both hippocampus and neocortex have taken advantage of transgenic animals and modern circuit mapping tools to functionally confirm that subsets of CR- and VIP-expressing interneurons do indeed mediate circuit disinhibition by selectively targeting other interneurons over pyramidal cells (185, 363, 652, 906, 908, 1145, 1270).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [363]
In the citing paper
“This disinhibitory motif is also common to the neocortex where a majority of vertically oriented bipolar VIP and CR coexpressing interneurons reside in layer2/3 and emit axons that preferentially innervate dendrite targeting SST expressing interneurons within the same column (168, 363, 425, 475, 553, 652, 906, 928, 1046, 1134, 1270).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [363]
In the citing paper
“Indeed, these driver lines have been successfully used in a number of recent studies to dissect circuit functions of ISIs in both hippocampus and neocortex (363, 553, 652, 906, 908, 1145, 1270).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [363]
In the citing paper
“The targeting of SST interneurons by VIP cells appears to be a generalized motif across brain structures including somatosensory, visual, and auditory cortices, and this specific disinhibitory microcircuit is important in sensory processing that, in some circumstances, demonstrates behavioral state dependence (363, 553, 660, 905, 906, 908, 1246, 1270).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [363]
In the citing paper
“Cholinergic receptors are expressed by inhibitory and excitatory cortical neurons119,124,158–164, as well as on the terminals of thalamocortical neurons165–169.”
From Mechanisms underlying gain modulation in the cortex (2020) · cites this paper as [119]
In the citing paper
“In particular, VIP+ interneurons express nAChRs and are strongly depolarized by nicotine or ACh119,124,163.”
From Mechanisms underlying gain modulation in the cortex (2020) · cites this paper as [119]
In the citing paper
“In particular, VIP+ interneurons express nAChRs and are strongly depolarized by nicotine or ACh119,124,163.”
From Mechanisms underlying gain modulation in the cortex (2020) · cites this paper as [119]
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“studies have not only highlighted an essential role of inhibitory neurons to balance excitation, but also recognized disinhibitory subcircuits, which release pyramidal neurons from strong inhibition (Fishell and Kepecs, 2020; Letzkus et al., 2015; Pi et al., 2013; Walker et al., 2016; Jackson et al., 2016; Fu et al.,…”
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Yogesh, B., & Keller, G. B. (2023) · eLife · doi:10.7554/elife.89986 · Cited by 30
“It has been argued that nicotinic activation of vasoactive intestinal peptide (VIP) expressing interneurons in visual cortex is necessary for this locomotion-induced gain of visual responses ( Fu et al., 2014 ).”
BackgroundHioki, H., Sohn, J., Nakamura, H., Okamoto, S., Hwang, J., Ishida, Y., Takahashi, M., & Kameda, H. (2018) · Brain Research · doi:10.1016/j.brainres.2018.05.029 · Cited by 20
Neuregulin directed molecular mechanisms of visual cortical plasticity
Grieco, S. F., Holmes, T. C., & Xu, X. (2018) · The Journal of Comparative Neurology · doi:10.1002/cne.24414 · Cited by 23
“…cortical plasticity (Tang, Stryker, Alvarez-Buylla, & Espinosa, 2014); PV neurons can be inhibited by SOM-expressing interneurons and VIP preferentially inhibit somatostatin positive (SST) cells (Fu et al., 2014; Jiang et al., 2015; Pakan et al., 2016; Pfeffer, Xue, He, Huang, & Scanziani, 2013).”
BackgroundSynaptic dysfunction of Aldh1a1 neurons in the ventral tegmental area causes impulsive behaviors
Li, X., Chen, W., Huang, X., Jing, W., Zhang, T., Yu, Q., Yu, H., Li, H., Tian, Q., Ding, Y., et al. (2021) · Molecular Neurodegeneration · doi:10.1186/s13024-021-00494-9 · Cited by 23
Esmaeili, V., Oryshchuk, A., Asri, R., Tamura, K., Foustoukos, G., Liu, Y., Guiet, R., Crochet, S., & Petersen, C. C. H. (2022) · PLoS Biology · doi:10.1371/journal.pbio.3001667 · Cited by 18
“Neuromodulation could also play an important role, for example through cholinergic reward signals [69], which could drive excitation of vasoactive intestinal peptideexpressing GABAergic neurons [70,71], in turn causing disinhibition through their prominent innervation of PV and somatostatin-expressing GABAergic neuron…”
An adaptive behavioral control motif mediated by cortical axo-axonic inhibition
Jung, K., Chang, M., Steinecke, A., Burke, B., Choi, Y., Oisi, Y., Fitzpatrick, D., Taniguchi, H., & Kwon, H. (2023) · Nature Neuroscience · doi:10.1038/s41593-023-01380-x · Cited by 18
Long‐range cortical dynamics: a perspective from the mouse sensorimotor whisker system
Ni, J., & Chen, J. L. (2017) · European Journal of Neuroscience · doi:10.1111/ejn.13698 · Cited by 19
“…in specific sensorimotor computations, indirect connections through local inhibitory interneurons may provide additional functions that depend on brain state (Castro-Alamancos, 2004; Ferezou et al., 2006; Hentschke et al., 2006; Poulet & Petersen, 2008; Fu et al., 2014; Wester & McBain, 2014).”
BackgroundExtended Temporal Association Memory by Modulations of Inhibitory Circuits
Haga, T., & Fukai, T. (2019) · Physical Review Letters · doi:10.1103/physrevlett.123.078101 · Cited by 20
Mice Preferentially Use Increases in Cerebral Cortex Spiking to Detect Changes in Visual Stimuli
Cone, J. J., Bade, M. L., Masse, N. Y., Page, E. A., Freedman, D. J., & Maunsell, J. H. R. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.1124-20.2020 · Cited by 17
“For comparison, mice can learn to report optogenetic activation of vasoactive intestinal peptide-expressing interneurons (Cone et al., 2019), which potentiate cortical spiking (Fu et al., 2014).”
BackgroundHolter, M. C., Hewitt, L. T., Nishimura, K. J., Knowles, S. J., Bjorklund, G. R., Shah, S., Fry, N., Rees, K. P., Gupta, T. A., Daniels, C. W., et al. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa413 · Cited by 22
Potential and Realized Impact of Astroglia Ca2 + Dynamics on Circuit Function and Behavior
Lim, E. Y., Ye, L., & Paukert, M. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.682888 · Cited by 21
Ebbesen, C. L., Bobrov, E., Rao, R. P., & Brecht, M. (2019) · Nature Communications · doi:10.1038/s41467-019-12511-z · Cited by 17
Visuomotor association orthogonalizes visual cortical population codesPreprint
Failor, S., Carandini, M., & Harris, K. D. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.05.23.445338 · Cited by 19
Neuromodulatory control of inhibitory network arborization in the developing postnatal neocortex
Steinecke, A., Bolton, M. M., & Taniguchi, H. (2022) · Science Advances · doi:10.1126/sciadv.abe7192 · Cited by 18
The brain during free movement – What can we learn from the animal model
Händel, B., & Schölvinck, M. L. (2017) · Brain Research · doi:10.1016/j.brainres.2017.09.003 · Cited by 18
Agnes, E. J., Luppi, A. I., & Vogels, T. P. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0276-20.2020 · Cited by 21
“Direct manipulation of SOM1, PV1, and vasoactive intestinal peptide-positive neurons confirms these respective roles in inhibition and disinhibition in both visual (Fu et al., 2014) and auditory cortices (Pi et al., 2013; Kuchibhotla et al., 2017).”
BackgroundBehavioral State—Getting “In The Zone”
Wekselblatt, J. B., & Niell, C. M. (2015) · Neuron · doi:10.1016/j.neuron.2015.06.020 · Cited by 19
“On the other hand, studies havedemonstrateda role for cholinergic in- . puts to cortex in regulating the strength of response to a visual stimulus (Fu et al., 2014; Pinto et al., 2013).”
BackgroundCell-specific modulation of plasticity and cortical state by cholinergic inputs to the visual cortex
杉原, 弘., Chen, N., & Sur, M. (2016) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2016.11.004 · Cited by 18
“For example, in gain modulation with associative fear learning (Letzkus et al., 2011) or during locomotion (Fu et al., 2014), VIP/L1 neurons modulate cortical gain via disinhibition through nicotinic ACh receptors, and such repetitive gain modulation can be further facilitated and consolidated by…”
BackgroundInfluentialAggarwal, A., Brennan, C. M., Shortal, B. P., Contreras, D., Kelz, M. B., & Proekt, A. (2019) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2019.00019 · Cited by 17
“Visual-evoked gamma power and frequency has also been shown to increase with arousal and locomotion in mice (Niell and Stryker, 2010; Polack et al., 2013; Fu et al., 2014).”
BackgroundKoay, S. A., Thiberge, S. Y., Brody, C. D., & Tank, D. W. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/568766 · Cited by 17
Homeostasis of a representational map in the neocortex
Noda, T., Kienle, E., Eppler, J.-B., Aschauer, D. F., Kaschube, M., Loewenstein, Y., & Rumpel, S. (2025) · Nature Neuroscience · doi:10.1038/s41593-025-01982-7 · Cited by 19
Magnitude, time course, and specificity of rapid adaptation across mouse visual areas
Jin, M., & Glickfeld, L. L. (2020) · Journal of Neurophysiology · doi:10.1152/jn.00758.2019 · Cited by 17
Modular microcircuit organization of the presubicular head-direction map
Balsamo, G., Blanco-Hernández, E., Liang, F., Naumann, R. K., Coletta, S., Burgalossi, A., & Preston‐Ferrer, P. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110684 · Cited by 17
Simple synaptic modulations implement diverse novelty computations
Aitken, K., Campagnola, L., Garrett, M., Olsen, S. R., & Mihalaş, Ş. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114188 · Cited by 21
Rem2 stabilizes intrinsic excitability and spontaneous firing in visual circuits
Moore, A. R., Richards, S. E. V., Kenny, K., Royer, L. O., Chan, U., Flavahan, K., Hooser, S. D. V., & Paradis, S. (2018) · eLife · doi:10.7554/elife.33092 · Cited by 17
“Vasoactive intestinal peptide (Vip) positive interneurons regulate cortical gain control during arousal (Fu et al., 2014), are integral to a disinhibitory circuit that enhances adult OD plasticity (Fu et al.”
BackgroundInhibitory and disinhibitory VIP IN-mediated circuits in neocortexPreprint
Dellal, S. S., Zurita, H., Kruglikov, I., Valero, M., Abad-Perez, P., Geron, E., Meng, J. H., Prönneke, A., Hanson, J. L., Mir, E., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.02.26.640383 · Cited by 24
Hippocampal OLM interneurons regulate CA1 place cell plasticity and remapping
Udakis, M., Claydon, M. D. B., Zhu, H. W., Oakes, E. C., & Mellor, J. R. (2025) · Nature Communications · doi:10.1038/s41467-025-64859-0 · Cited by 19
The Sensory Neocortex and Associative Memory
Aschauer, D. F., & Rumpel, S. (2016) · Current topics in behavioral neurosciences · doi:10.1007/7854_2016_453 · Cited by 17
Antagonistic inhibitory subnetworks control cooperation and competition across cortical spacePreprint
Mossing, D. P., Veit, J., Palmigiano, A., Miller, K. D., & Adesnik, H. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.03.31.437953 · Cited by 16
Experience shapes chandelier cell function and structure in the visual cortex
Seignette, K., Jamann, N., Papale, P., Terra, H., Porneso, R. P. O., de Kraker, L., van der Togt, C., van der Aa, M., Neering, P., Ruimschotel, E., et al. (2023) · eLife · doi:10.7554/elife.91153 · Cited by 18
“…segmentation, predictive processing, and plasticity ( Karnani et al., 2016 ; Kirchberger et al., 2023 ; Kirchberger et al., 2021 ; Pfeffer et al., 2013 ; van Versendaal and Levelt, 2016 ; Zhang et al., 2014 ; Attinger et al., 2017 ; Adesnik et al., 2012 ; Keller et al., 2020 ; Fu et al., 2014 ).”
BackgroundMultimodal gradients of basal forebrain connectivity across the neocortex
Chakraborty, S., Haast, R. A. M., Onuska, K. M., Kanel, P., Prado, M. A. M., Prado, V. F., KHAN, A. R., & Schmitz, T. W. (2024) · Nature Communications · doi:10.1038/s41467-024-53148-x · Cited by 18
Mediodorsal thalamus regulates task uncertainty to enable cognitive flexibility
Zhang, X., Mukherjee, A., Halassa, M. M., & Chen, Z. S. (2025) · Nature Communications · doi:10.1038/s41467-025-58011-1 · Cited by 19
Meng, Q., Ding, Y., Chen, L., & Li, L. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112511 · Cited by 15
Probing neuronal functions with precise and targeted laser ablation in the living cortex
Cheng, Z., Han, Y., Wei, B., Lai, B., Li, B., Cui, M., & Gan, W. (2021) · Optica · doi:10.1364/optica.433562 · Cited by 15
Kalogeraki, E., Pielecka-Fortuna, J., Hüppe, J. M., & Löwel, S. (2016) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2016.00212 · Cited by 17
“We focused on running because locomotion has recently been shown to massively increase pyramidal cell firing in V1 (Niell and Stryker, 2010; Fu et al., 2014) and promote activity-dependent changes in V1 circuitry (Kaneko and Stryker, 2014).”
Metadata
- Authors
- Fu, Y., Tucciarone, J. M., Espinosa, J. S., Sheng, N., Darcy, D. P., Nicoll, R. A., Huang, Z. J., & Stryker, M. P.
- Affiliations
- University of California, San Francisco (US)
- Cold Spring Harbor Laboratory (US)
- Corresponding author
- Fu, Yu
- Stryker, Michael P.
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2014-03
- Volume
- 156
- Issue
- 6
- Pages
- 1139-1152
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC4041382
- OpenAlex
- W2097237250
- Cited by
- 937
- References
- 62
- Citations by year
- 2026: 45 · 2025: 69 · 2024: 77 · 2023: 75 · 2022: 75 · 2021: 77 · 2020: 90 · 2019: 106 · 2018: 84 · 2017: 89 · 2016: 73 · 2015: 51 · 2014: 26
- FWCI
- 44.43
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institute of Mental Health (R01MH094705, R37MH038256)
- National Eye Institute (P30EY002162, R01EY002874, EY002874, R37EY002874)
- National Institute of General Medical Sciences (T32GM008444)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- gain control, behavioral state, locomotion, primary visual cortex, vasoactive intestinal peptide neurons, nicotinic acetylcholine receptors, basal forebrain, cortical state
- MeSH terms
- Animals, Female, gamma-Aminobutyric Acid, Male, Neurons, Receptors, Nicotinic, Running, Vasoactive Intestinal Peptide, Visual Pathways, Neocortex, Mice, GABAergic Neurons
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