Comparison of visual receptive field properties of the superior colliculus and primary visual cortex in rats

• We studied the spatiotemporal receptive field properties of neurons quantitatively.
• Visual cortical and subcortical neurons process signals through different mechanisms.
• Subcortical neurons are responsible for coarse information processing.
• Visual cortical neurons are responsible for extracting detailed information.

The rat visual system comprises cortical and subcortical pathways. The receptive field properties of cells in the visual cortex have been extensively studied; however, the fundamental roles of the two circuits in visual information processing are not well understood. To address this question, we have applied quantitative methods to compare and characterize the spatiotemporal receptive field (RF) properties of neurons in primary visual cortex (V1) cells and superficial layers of the superior colliculus (SC) in rats by means of extracellular recordings. An analysis of visual stimulus processing revealed distinct functional characteristics of the two visual circuits. RF diameters of SC neurons were significantly larger than those of V1 cells. Most cells in both regions had high orientation selectivity, but the mean orientation bandwidth of the SC was broader than that of V1 cells (101.5° vs. 60.2°). The mean optimal spatial frequency (SF) of SC cells was lower but had a broader bandwidth than that of V1 cells (0.03 vs. 0.068 cpd). The majority of SC and V1 cells (70% and 68%, respectively) had RFs with band-pass temporal frequency (TF) tuning profiles and similar optimal TFs. However, temporal band-pass profiles of the SC showed narrower mean temporal bandwidths than those of V1 cells (1.42 vs. 2.36 octaves). The majority of neurons in visual cortical and subcortical structures were activated in response to high-contrast, drifting gratings in the preferred orientation. The percentage of V1 neurons with a low-contrast threshold was larger than the proportion of SC neurons (45.6% vs. 30%), indicating that the former adapt better to contrast. The substantial overlap in latency distributions between SC and V1 areas suggests that the two visual systems process and analyze visual signals in parallel. However, the two areas use different neural encoding mechanisms based on different latency distribution trends. These results indicate that SC cells have poor spatial acuity and are better suited to detecting high-contrast, moving stimuli in larger visual fields. In contrast, V1 cells are adapted to extracting shape information and detailed features of objects.