Laminar profile of visual response properties in ferret superior colliculus

Abstract

In the superior colliculus (SC), visual afferent inputs from various sources converge in a highly organized way such that all layers form topographically aligned representations of contralateral external space. Despite this anatomical organization, it remains unclear how the layer-specific termination of different visual input pathways is reflected in the nature of visual response properties and their distribution across layers. To uncover the physiological correlates underlying the laminar organization of the SC, we recorded multiunit and local field potential activity simultaneously from all layers with dual-shank multichannel linear probes. We found that the location of spatial receptive fields was strongly conserved across all visual responsive layers. There was a tendency for receptive field size to increase with depth in the SC, with superficial receptive fields significantly smaller than deep receptive fields. Additionally, superficial layers responded significantly faster than deeper layers to flash stimulation. In some recordings, flash-evoked responses were characterized by the presence of gamma oscillatory activity (40–60 Hz) in multiunit and field potential signals, which was strongest in retinorecipient layers. While SC neurons tended to respond only weakly to full-field drifting gratings, we observed very similar oscillatory responses to the offset of grating stimuli, suggesting gamma oscillations are produced following light offset. Oscillatory spiking activity was highly correlated between horizontally distributed neurons within these layers, with oscillations temporally locked to the stimulus. Together, visual response properties provide physiological evidence reflecting the laminar-specific termination of visual afferent pathways in the SC, most notably characterized by the oscillatory entrainment of superficial neurons.