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Comparative Study
, 29 (39), 12159-66

Color-related Signals in the Primate Superior Colliculus

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Comparative Study

Color-related Signals in the Primate Superior Colliculus

Brian J White et al. J Neurosci.

Abstract

Color is important for segmenting objects from backgrounds, which can in turn facilitate visual search in complex scenes. However, brain areas involved in orienting the eyes toward colored stimuli in our environment are not believed to have access to color information. Here, we show that neurons in the intermediate layers of the monkey superior colliculus (SC), a critical structure for the production of saccadic eye movements, can respond to isoluminant color stimuli with the same magnitude as a maximum contrast luminance stimulus. In contrast, neurons from the superficial SC layers showed little color-related activity. Crucially, visual onset latencies were 30-35 ms longer for color, implying that luminance and chrominance information reach the SC through distinct pathways and that the observed color-related activity is not the result of residual luminance signals. Furthermore, these differences in visual onset latency translated directly into differences in saccadic reaction time. The results demonstrate that the saccadic system can signal the presence of chromatic stimuli only one stage from the brainstem premotor circuitry that drives the eyes.

Figures

Figure 1.
Figure 1.
a, Delayed saccade task. The monkey fixated a central black spot for 500–800 ms, and then a randomly chosen isoluminant color stimulus (Gaussian windowed; SD, 0.7°) appeared in the response field (RF) of the neuron. After a delay (500–800 ms), the fixation spot was removed, serving as a go-signal for a saccade toward the color stimulus. Comparisons were made with an achromatic black stimulus presented at 100% luminance contrast. b, DKL color space (Krauskopf et al., 1982; Derrington et al., 1984) (see Materials and Methods). Color stimuli were chosen from 30° steps around the azimuth of the isoluminant plane at maximum saturation (illustrated by the circles superimposed on the color plane). The stimuli were presented against an isoluminant neutral gray background (20.5 cd/m2) illustrated by the center point in the color plane. The achromatic black control stimulus corresponds to the very most bottom point in this space. c, Rasters and spike density functions of a single sustained-visual SC neuron to each of the color stimuli (aligned on stimulus onset). At the center is a polar plot of the normalized peak responses for each color (colored symbols linked by the thin line). The thicker line shows the responses averaged over a short epoch (80–180 ms) defined by the gray shaded region. d, Color tuning profiles for four additional sustained-visual neurons.
Figure 2.
Figure 2.
Comparison of the visual responses for the optimal color stimuli (colored traces) and maximum contrast luminance stimulus (black traces) across SC cell types. The top two panels show average normalized spike density functions for sustained-visual neurons to their optimal color stimulus (red traces) and the maximum contrast luminance stimulus (black traces) (a), and transient-visual neurons to their optimal color stimulus (blue traces) and the maximum contrast luminance stimulus (black traces) (b). c and d show averages for our sample of visuomotor neurons for the same two visual classifications. Note that transient-visual neurons (b) originated from the superficial SC layers (<1 mm from SC surface). Below each panel is the visual onset latency for each response profile. The shaded regions represent ±1 SEM.
Figure 3.
Figure 3.
Summary of the peak visual responses and visual onset latencies for our sample of 68 neurons. a, Peak visual responses. b, Percentage neurons with greater color response. c, Visual onset latencies. d, A correlation between the color sensitivity index (Johnson et al., 2008) and transient index (Schiller and Malpeli, 1977) of each neuron (see Materials and Methods). TV, Transient-visual; TVM, transient-visuomotor; SV, sustained-visual; SVM, sustained-visuomotor. b and c represent a subset of the total sample of neurons whose peak visual response was greater for the optimal color than the maximum-contrast luminance stimulus. The arrows on the axes in c denote the median visual onset latency for the sample of neurons for color versus luminance.
Figure 4.
Figure 4.
Cumulative SRT distributions for luminance versus color for monkey Y (a) and monkey Q (b) during a gap task (200 ms gap) [cumulative onset latency distributions (c, d) from neural data obtained during the delay task were plotted for comparison]. The black solid traces represent the maximum-contrast luminance stimulus, and the colored traces represent the isoluminant DKL stimuli from the four cardinal color directions (red–green; blue–yellow). The black dashed line represents the average across the colors.

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