Cellular mechanisms of brain state-dependent gain modulation in visual cortex
Open accessAbstract
Visual cortical neurons fire at higher rates to visual stimuli during locomotion than during immobility, while maintaining orientation selectivity. The mechanisms underlying this change in gain are not understood. We performed whole-cell recordings from layer 2/3 and layer 4 visual cortical excitatory neurons and from parvalbumin-positive and somatostatin-positive inhibitory neurons in mice that were free to rest or run on a spherical treadmill. We found that the membrane potential of all cell types became more depolarized and (with the exception of somatostatin-positive interneurons) less variable during locomotion. Cholinergic input was essential for maintaining the unimodal membrane potential distribution during immobility, whereas noradrenergic input was necessary for the tonic depolarization associated with locomotion. Our results provide a mechanism for how neuromodulation controls the gain and signal-to-noise ratio of visual cortical neurons during changes in the state of vigilance.
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Head-restrained preparations have shown that behavioral state fluctuations have a strong impact on neuronal gain and coding properties in primary sensory areas and modulate neuronal firing within brain-wide neuronal networks.
“By employing head-restrained preparations, a growing body of work has demonstrated that behavioral state fluctuations have a strong impact on neuronal gain and coding properties in primary sensory areas36,43,66–70 and modulate neuronal firing within brain-wide neuronal networks44,71–74.”
From Place and behavioral modulation of hippocampal neurons during immobility (2026) · cites this paper as [69]
In some studies, cortical neurons transition to slow oscillatory activity quickly after a bout of locomotion or whisking even though the pupil is usually still large at the end of running periods.
“In some studies, cortical neurons have been observed to transition to slow oscillatory activity quickly following a bout of locomotion or whisking (e.g. (Crochet and Petersen, 2006; Gentet et al., 2010; Polack et al., 2013)) (Figures 1B), even though the pupil usually is still large at the end of running periods”
From Waking state: rapid variations modulate neural and behavioral responses (2015) · cites this paper as Polack et al., 2013
In V1, locomotion causes both multiplicative and additive enhancements of responses to drifting gratings.
“In V1, locomotion causes both multiplicative and additive enhancements of responses to drifting gratings”
From Waking state: rapid variations modulate neural and behavioral responses (2015) · cites this paper as Polack et al., 2013
Locomotion is associated with suppression of slow rhythmic activity in cortical networks, depolarization of cortical neurons closer to action potential threshold, and enhanced visually evoked responses.
“Locomotion, as we have mentioned, is associated with a suppression of slow rhythmic activity in cortical networks, a depolarization of cortical neurons closer to action potential threshold, and enhanced visually evoked responses (Bennett et al., 2013; Polack et al., 2013; Reimer et al., 2014).”
From Waking state: rapid variations modulate neural and behavioral responses (2015) · cites this paper as Polack et al., 2013
Pharmacological block of both cholinergic and noradrenergic receptors locally in the cortex is associated with a strong reduction of the ability of locomotion to modulate cortical state.
“Pharmacological block of both cholinergic and noradrenergic receptors locally in the cortex is associated with a strong reduction of the ability of locomotion to modulate cortical state (Eggermann et al., 2014; Polack et al., 2013), suggesting that movement may reduce low frequency, and promote higher frequency, rhythms largely through its association with arousal.”
From Waking state: rapid variations modulate neural and behavioral responses (2015) · cites this paper as Polack et al., 2013
Depolarization of layer 2/3 visual cortical neurons with locomotion is suppressed by block of noradrenergic receptors.
“Depolarization of layer 2/3 visual cortical neurons with locomotion (e.g. Figure 1B) is suppressed by block of noradrenergic receptors (Polack et al., 2013).”
From Waking state: rapid variations modulate neural and behavioral responses (2015) · cites this paper as Polack et al., 2013
Parvalbumin-containing interneurons exhibit a more diverse response to locomotion, with some increasing and others decreasing their average firing rate.
“Parvalbumin-containing interneurons exhibit a more diverse response to locomotion, with some increasing (e.g. Figure 1B) and others decreasing their average firing rate (Fu et al., 2014; Gentet et al., 2010; Polack et al., 2013).”
From Waking state: rapid variations modulate neural and behavioral responses (2015) · cites this paper as Polack et al., 2013
The degree to which the synaptic input underlying Vm fluctuations is temporally correlated can vary with overall drive to a network or with firing rates and is regulated by behavioural state transitions during wakefulness.
“The degree to which the synaptic input underlying Vm fluctuations is temporally correlated can vary with overall drive to a network or with firing rates70 and is regulated by behavioural state transitions during wakefulness29,71–74.”
From Mechanisms underlying gain modulation in the cortex (2020) · cites this paper as [73]
Neuromodulatory inputs, such as acetylcholine, alter the correlation statistics of synaptic activity in the cortex.
“Neuromodulatory inputs, such as acetylcholine (ACh), also alter the correlation statistics of synaptic activity in the cortex73,75.”
From Mechanisms underlying gain modulation in the cortex (2020) · cites this paper as [73]
Depolarization and increased firing of mouse V1 neurons associated with locomotion require noradrenergic transmission.
“The depolarization and increased firing of mouse V1 neurons associated with locomotion require noradrenergic transmission”
From Mechanisms underlying gain modulation in the cortex (2020) · cites this paper as [73]
Blocking noradrenergic receptors results in hyperpolarization of pyramidal neurons, decreases their firing and prevents locomotion-induced increases in visual response gain.
“blocking noradrenergic receptors results in hyperpolarization of pyramidal neurons, decreases their firing and prevents locomotion-induced increases in visual response gain73.”
From Mechanisms underlying gain modulation in the cortex (2020) · cites this paper as [73]
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“However, a previous study has reported an increase of SST spiking activity in layer 2/3 during locomotion (Polack et al., 2013), an observation that challenges the hypothesis of an SST-cell mediated”
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- Authors
- Polack, P.-O., Friedman, J., & Golshani, P.
- Affiliations
- University of California, Los Angeles (US)
- Corresponding author
- Golshani, Peyman
- Venue
- Nature Neuroscience
- Published
- 2013-07-21
- Volume
- 16
- Issue
- 9
- Pages
- 1331-1339
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC3786578
- OpenAlex
- W2047964244
- Cited by
- 628
- References
- 53
- Citations by year
- 2026: 28 · 2025: 39 · 2024: 56 · 2023: 60 · 2022: 44 · 2021: 44 · 2020: 54 · 2019: 60 · 2018: 58 · 2017: 44 · 2016: 53 · 2015: 36 · 2014: 43 · 2013: 9
- FWCI
- 25.68
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- U.S. Department of Veterans Affairs (I01 BX001524)
- National Institute of Mental Health (R01MH101198)
- National Institute of Neurological Disorders and Stroke (K08NS056210, K08 NS0562101)
- 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 › Visual perception and processing mechanisms
- Keywords
- gain modulation, visual cortex, cholinergic modulation, noradrenergic modulation, locomotion, immobility, membrane potential, parvalbumin interneurons, somatostatin interneurons, sleep-wake states, signal-to-noise ratio, orientation selectivity, neuromodulation
- MeSH terms
- Action Potentials, Animals, DNA-Binding Proteins, Female, Immobilization, Locomotion, Male, Mice, Inbred C57BL, Mice, Transgenic, Models, Neurological, Neurons, Orientation, Parvalbumins, Photic Stimulation, Transcription Factors, Visual Cortex, Visual Pathways, Neurotransmitter Agents, Patch-Clamp Techniques, Mice, Signal-To-Noise Ratio
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