PT  - JOURNAL ARTICLE
AU  - Shinya Ito
AU  - David A. Feldheim
AU  - Alan M. Litke
TI  - Segregation of visual response properties in the mouse superior colliculus and their modulation during locomotion
AID  - 10.1523/JNEUROSCI.3689-16.2017
DP  - 2017 Jul 31
TA  - The Journal of Neuroscience
PG  - 3689-16
4099  - http://www.jneurosci.org/content/early/2017/07/31/JNEUROSCI.3689-16.2017.short
4100  - http://www.jneurosci.org/content/early/2017/07/31/JNEUROSCI.3689-16.2017.full
AB  - The superior colliculus (SC) receives direct input from the retina and integrates it with information about sound, touch and state of the animal that is relayed from other parts of the brain to initiate specific behavioral outcomes. 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. Here we used a large-scale silicon probe recording system to examine the visual response properties of SC cells of head-fixed and alert male mice. We find cells with diverse response properties including: (1) orientation/direction selective (OS/DS) cells with a firing rate that is suppressed by drifting sinusoidal gratings (negative OS/DS cells); (2) suppressed-by-contrast cells; (3) cells with complex-like spatial summation nonlinearity; and (4) cells with Y-like spatial summation nonlinearity. We also find specific response properties that are enriched in different depths of the SC. The sSC is enriched with cells with small receptive fields (RFs), high evoked firing rates (FRs) and sustained temporal responses, while the dSC is enriched with the negative OS/DS cells and with cells with large RFs, low evoked FRs, and transient temporal responses. Locomotion modulates the activity of the SC cells both additively and multiplicatively, and changes the preferred spatial frequency of some SC cells. These results provide the first description of the negative OS/DS cells, demonstrate that the SC segregates cells with different response properties, and demonstrate that the behavioral state of a mouse impacts SC activity.SIGNIFICANCE STATEMENTThe 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 high-density electrode recordings and novel model-based analysis, we find several novel visual response properties of the SC cells, including encoding of a cell's preferred orientation or direction by suppression of the firing rate. The sSC and the dSC are enriched with cells with different visual response properties. Locomotion modulates the cells in the SC. These findings contribute to our understanding of how the SC processes visual inputs, a critical step in comprehending visually-guided behaviors.