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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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Hippocampal neuronal and astrocytic responses to noradrenaline and natural arousalPreprint
Duss, S. N., Wilhelm, M., Marinescu, A., Zhang, R., Helmchen, F., Bohacek, J., & Rupprecht, P. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.01.16.699885
“ACh release correlates with pupil diameter, a common proxy for arousal (Reimer et al., 2016) and has been demonstrated to drive locomotion-related activity of cortical interneurons (Fu et al., 2014) and hippocampal pyramidal cells (Fuhrmann et al., 2015).”
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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