Segregation of Visual Response Properties in the Mouse Superior Colliculus and Their Modulation during Locomotion
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Abstract
Abstract The superior colliculus (SC) is an integrative sensorimotor structure that contributes to multiple visiondependent behaviors. It is a laminated structure; the superficial SC layers (sSC) contain cells that respond to visual stimuli, while the deep SC layers (dSC) contain cells that also respond to auditory and somatosensory stimuli. Despite the increasing interest in mice for visual system study, the differences in the visual response properties between the sSC and the dSC are largely unknown. Here we used a large-scale silicon probe recording system to examine the visual response properties of neurons within the SC of head-fixed, awake and behaving mice. We find that both the sSC and dSC cells respond to visual stimuli, but dSC cells have three key differences. (1) The majority of the dSC orientation/direction selective (OS/DS) cells have their firing rate suppressed by drifting sinusoidal gratings (negative OS/DS cells) rather than being stimulated like the sSC cells (positive OS/DS cells). (2) Almost all the dSC cells have complex-cell-like spatial summation nonlinearity, and a significantly smaller fraction of the positive OS/DS cells in the dSC respond to flashing spots than those in the sSC. (3) The dSC cells lack Y-like spatial summation nonlinearity unlike the sSC cells. These results provide the first description of cells that are suppressed by a visual stimulus with a specific orientation or direction, show that neurons in the dSC have properties analogous to cortical complex cells, and show the presence of Y-like nonlinearity in the sSC but their absence in the dSC. Significance statement The superior colliculus receives visual input from the retina in its superficial layers (sSC) and induces eye/head orientating movements and innate defensive responses in its deeper layers (dSC). Despite their importance, very little is known about the visual response properties of dSC neurons. Using highdensity electrode recordings and novel model-based analysis, we find that the dSC contains cells with a novel property; they are suppressed by the orientation or direction of specific stimuli. We also show that dSC cells have properties similar to cortical “complex” cells. Conversely, cells with Y-like nonlinear spatial summation properties are located only in the sSC. These findings contribute to our understanding of how the SC processes visual inputs, a critical step in comprehending visually-guided behaviors. Acknowledgements This work was supported by the Brain Research Seed Funding provided by UCSC and from the National Institutes of Health Grant NEI R21EYO26758 to D. A. F. and A. M. L. We thank Michael Stryker for training on the electrophysiology experiments and his very helpful comments on the manuscript, Sotiris Masmanidis for providing us with the silicon probes, Forest Martinez-McKinney and Serguei Kachiguin for their technical contributions to the silicon probe system, Jeremiah Tsyporin for taking an image of neural tissues and the training of mice, Jena Yamada, Anahit Hovhannisyan, Corinne Beier, and Sydney Weiser, for their helpful comments on the manuscript.
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Monosynaptic rabies-based retrograde tracing identified projections from medial superficial layers of ipsilateral superior colliculus (sSC→PVN), involved in visual processing.
“We performed monosynaptic rabies-based retrograde tracing to identify visual inputs onto oxytocin neurons, and found projections from medial superficial layers of ipsilateral superior colliculus (sSC→PVN; Extended Data Fig. 9a, b), involved in visual processing18.”
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Spectral cues are necessary to encode azimuthal auditory space in the mouse superior colliculus
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Kinetic features dictate sensorimotor alignment in the superior colliculus
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Stimulus edges induce orientation tuning in superior colliculus
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Look-up and look-down neurons in the mouse visual thalamus during freely moving exploration
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Reward Modulates Visual Responses in the Superficial Superior Colliculus of Mice
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The “Primitive Brain Dysfunction” Theory of Autism: The Superior Colliculus Role
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Neural dynamics in superior colliculus of freely moving mice
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Pupil-linked Arousal Signals in the Midbrain Superior Colliculus
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2MDR, a Microcomputer-Controlled Visual Stimulation Device for Psychotherapy-Like Treatments of Mice
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Whisking and locomotion are jointly represented in superior colliculus neurons
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Functional segregation and dynamic integration of the corticotectal descending signal in rat
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Spectral cues are necessary to encode azimuthal auditory space in the mouse superior colliculusPreprint
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Multiple groups of neurons in the superior colliculus convert value signals into saccadic vigor
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- Authors
- Ito, S., Feldheim, D. A., & Litke, A. M.
- Affiliations
- University of California, Santa Cruz (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2017-07-31
- Volume
- 37
- Issue
- 35
- Pages
- 8428-8443
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC5577856
- OpenAlex
- W2740321704
- Cited by
- 92
- References
- 70
- Citations by year
- 2026: 7 · 2025: 15 · 2024: 12 · 2023: 14 · 2022: 14 · 2021: 5 · 2020: 13 · 2019: 4 · 2018: 7 · 2017: 1
- FWCI
- 3.88
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Stryker
- National Institutes of Health
- National Eye Institute (R01EY022117, NEI R21EYO26758, R21EY026758)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Multisensory perception and integration
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- superior colliculus, visual response properties, orientation selectivity, direction selectivity, receptive field size, mouse visual cortex
- MeSH terms
- Adaptation, Physiological, Animals, Gait, Locomotion, Male, Mice, Inbred C57BL, Nerve Net, Neuronal Plasticity, Superior Colliculi, Visual Perception, Mice, Spatial Navigation
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