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Enhanced Spatial Resolution During Locomotion and Heightened Attention in Mouse Primary Visual Cortex
Open accessAbstract
UNLABELLED: We do not fully understand how behavioral state modulates the processing and transmission of sensory signals. Here, we studied the cortical representation of the retinal image in mice that spontaneously switched between a state of rest and a constricted pupil, and one of active locomotion and a dilated pupil, indicative of heightened attention. We measured the selectivity of neurons in primary visual cortex for orientation and spatial frequency, as well as their response gain, in these two behavioral states. Consistent with prior studies, we found that preferred orientation and spatial frequency remained invariant across states, whereas response gain increased during locomotion relative to rest. Surprisingly, relative gain, defined as the ratio between the gain during locomotion and the gain during rest, was not uniform across the population. Cells tuned to high spatial frequencies showed larger relative gain compared with those tuned to lower spatial frequencies. The preferential enhancement of high-spatial-frequency information was also reflected in our ability to decode the stimulus from population activity. Finally, we show that changes in gain originate from shifts in the operating point of neurons along a spiking nonlinearity as a function of behavioral state. Differences in the relative gain experienced by neurons with high and low spatial frequencies are due to corresponding differences in how these cells shift their operating points between behavioral states. SIGNIFICANCE STATEMENT: How behavioral state modulates the processing and transmission of sensory signals remains poorly understood. Here, we show that the mean firing rate and neuronal gain increase during locomotion as a result in a shift of the operating point of neurons. We define relative gain as the ratio between the gain of neurons during locomotion and rest. Interestingly, relative gain is higher in cells with preferences for higher spatial frequencies than those with low-spatial-frequency selectivity. This means that, during a state of locomotion and heightened attention, the population activity in primary visual cortex can support better spatial acuity, a phenomenon that parallels the improved spatial resolution observed in human subjects during the allocation of spatial attention.
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“Contrast-invariant tuning is an example of gain modulation that is induced by changes in sensory stimulation, in which neurons respond to stimuli of different levels of contrast while preserving their selectivity for other properties, such as orientation and spatial frequency27–29.”
From Mechanisms underlying gain modulation in the cortex (2020) · cites this paper as [27]
In the citing paper
“Using two separate decoders during still and active periods does not improve stimulus prediction, indicating that a model with a single mode of gain modulation best reflects the improvements in encoding between the two states27,37.”
From Mechanisms underlying gain modulation in the cortex (2020) · cites this paper as [27]
In the citing paper
“Decoders that predict the presence of visual stimuli on the basis of neural responses are more accurate when they use neural activity recorded in the mouse cortex during locomotion than that during quiescence27,37”
From Mechanisms underlying gain modulation in the cortex (2020) · cites this paper as [27]
In the citing paper
“Variability in stimulus-tuning preferences may further contribute to the heterogeneous distribution of gain modulation27”
From Mechanisms underlying gain modulation in the cortex (2020) · cites this paper as [27]
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Metadata
- Authors
- Mineault, P. J., Tring, E., Trachtenberg, J. T., & Ringach, D. L.
- Affiliations
- University of California, Los Angeles (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2016-06-15
- Volume
- 36
- Issue
- 24
- Pages
- 6382-6392
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC4909779
- OpenAlex
- W2443622370
- Cited by
- 148
- References
- 52
- Citations by year
- 2026: 12 · 2025: 5 · 2024: 18 · 2023: 15 · 2022: 10 · 2021: 30 · 2020: 12 · 2019: 12 · 2018: 20 · 2017: 12 · 2016: 2
- FWCI
- 9.66
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Neuroscience (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Eye Institute (R01EY018322, R01EY023871)
- 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
- primary visual cortex, behavioral state, locomotion, attention, miosis, relative gains, spatial frequency selectivity, orientation selectivity, spatial acuity, mice
- MeSH terms
- Orientation, Spatial, Action Potentials, Animals, Attention, Female, Locomotion, Male, Mice, Inbred C57BL, Neurons, Photic Stimulation, Transduction, Genetic, Visual Cortex, Linear Models, Mice
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