Automatic, Early Color-Specific Neural Responses to Object Color Knowledge

Abstract

Some familiar objects are associated with specific colors, e.g., rubber ducks with yellow. Whether and at what stage neural responses occur to these color associations remain open questions. We recorded frequency-tagged electroencephalogram (EEG) responses to periodic presentations of yellow-associated objects, shown among sequences of non-periodic blue-, red-, and green-associated objects. Both color and grayscale versions of the objects elicited yellow-specific responses, indicating an automatic activation of color knowledge from object shape. Follow-up experiments replicated these effects with green-specific responses, and demonstrated modulated responses for incongruent color/object associations. Importantly, the onset of color-specific responses was as early to grayscale as actually colored stimuli (before 100 ms), the latter additionally eliciting a conventional later response (approximately 140-230 ms) to actual stimulus color. This suggests that the neural representation of familiar objects includes both diagnostic shape and color properties, such that shape can elicit associated color-specific responses before actual color-specific responses occur.

Keywords: Cortex; EEG; Frequency tagging; Memory; Shape; Vision.

Fig. 1.

a) The 24 color-associated stimuli used in the experiments, shown as appearing in diagnostic color (left), grayscale (middle), and incongruent color (right) conditions. b) The trial design of Experiment 1, targeting yellow-associated objects, is depicted for each the grayscale and color conditions. Stimuli were presented every 250 ms (at 4 Hz) in 50 s sequences, throughout which a yellow-associated object appeared every 1 s (1 Hz), i.e., as every fourth image. The order of the green-, red-, and blue-associated images was fully randomized within every sequence for each participant. c) The trial design of Experiments 2 and 3, targeting green-associated object responses. Experiment 3 consisted of an incongruent condition, in which targeted non-green-associated objects appeared in green.

Fig. 2.

a) The frequency-domain amplitude spectra for the color condition of Experiment 1, plotted over the occipito-parietal ROI. Dotted vertical lines indicate the frequencies of 1 Hz and its harmonics. (For corresponding spectra of all conditions, see Fig. S1.) The visual stimulation responses at 4 Hz and its harmonics are indicated with x-axis labels. b & c) Summed baseline-subtracted harmonic responses: a frequency range of 0.6 Hz is plotted relative to the summed frequency-of-interest and its specific harmonics (f*) set at 0 Hz (the x-axis represents frequency – f*). The surrounding frequency range from 0.3 Hz below to above f* is included to display the local noise amplitude and variability; average noise level is expected at 0 μV. Key: *** = Z>3.1, p<.001.

Fig. 3.

Summed-harmonic, baseline-subtracted response amplitude (μV) over the occipito-parietal ROI, at the group- (gray bars) and individual- (colored lines) levels. a) Yellow-selective responses (1–25 Hz) from Experiment 1. b) Stimulus-presentation responses (4–56 Hz) from Experiment 1. c) Green-selective responses (1–25 Hz) from Experiments 2 and 3. b) Stimulus-presentation responses (4–56 Hz) from Experiments 2 and 3.

Fig. 4.

a & c) Summed-harmonic response scalp topographies in the grayscale and color conditions (Experiments 1 and 2), and incongruent condition (Experiment 3), as well as their differences. b & d) Mean summed-harmonic responses at the occipito-parietal (OP) ROI and its three subregions: left, medial, and right (illustrated on the head plots on the right of panel b).

Fig. 5.. Temporal dynamics.

a) Time-domain responses in the grayscale (blue waveform) and color (red waveform) conditions, related to yellow-associated object stimulus onset (0 ms; exemplified with a yellow/gray rubber duck; in Experiment 1), at the three scalp subregions (left, middle, and right panels, respectively). These responses reflect the responses to all objects (presented at 4 Hz, i.e., every 250 ms) as well as the responses specific to yellow-associated objects. The dark waveforms are the average across subjects, with the shaded areas indicating ± 1 SE. b) After filtering out the general visual EEG responses at 4 Hz and its harmonics, the time-course of the yellow-associated object responses may be isolated. This panel is plotted as in (a), except with a different amplitude scale. Additionally, the time windows of significant deflections for each condition are indicated by solid lines below the waveforms in the corresponding color by condition; significant differences across conditions, occurring only at the middle subregion, are indicated in yellow-green. c) Response scalp topographies across time: sampled every 30 ms from stimulus onset. The approximate time window of significant differences between conditions, i.e., a positive deflection over the middle subregion in the color condition, is highlighted with a yellow outline over that condition. d) Responses including those to stimulus-presentation as well as those specific to green-associated (Experiment 2) or incongruently-green (Experiment 3; purple waveform) objects; e) stimulus-presentation filtered. f) Response scalp topographies for Experiments 2 and 3, plotted as in (c), with a green outline over the color condition; differences between the color and incongruent conditions are outlined in orange over the incongruent condition.