Low-level and high-level modulations of fixational saccades and high frequency oscillatory brain activity in a visual object classification task

Abstract

Until recently induced gamma-band activity (GBA) was considered a neural marker of cortical object representation. However, induced GBA in the electroencephalogram (EEG) is susceptible to artifacts caused by miniature fixational saccades. Recent studies have demonstrated that fixational saccades also reflect high-level representational processes. Do high-level as opposed to low-level factors influence fixational saccades? What is the effect of these factors on artifact-free GBA? To investigate this, we conducted separate eye tracking and EEG experiments using identical designs. Participants classified line drawings as objects or non-objects. To introduce low-level differences, contours were defined along different directions in cardinal color space: S-cone-isolating, intermediate isoluminant, or a full-color stimulus, the latter containing an additional achromatic component. Prior to the classification task, object discrimination thresholds were measured and stimuli were scaled to matching suprathreshold levels for each participant. In both experiments, behavioral performance was best for full-color stimuli and worst for S-cone isolating stimuli. Saccade rates 200-700 ms after stimulus onset were modulated independently by low and high-level factors, being higher for full-color stimuli than for S-cone isolating stimuli and higher for objects. Low-amplitude evoked GBA and total GBA were observed in very few conditions, showing that paradigms with isoluminant stimuli may not be ideal for eliciting such responses. We conclude that cortical loops involved in the processing of objects are preferentially excited by stimuli that contain achromatic information. Their activation can lead to relatively early exploratory eye movements even for foveally-presented stimuli.

Keywords: EEG; color; fixational saccades; gamma-band activity; luminance; microsaccades; parallel visual pathways; visual object representation.

Figure 1

(A) The chromaticities of stimuli in the DKL color space. Along the achromatic axis, cone contrasts in all three cone classes vary (L + M + S). Along the L − M axis, only the difference between L- and M-cone varies, keeping L + M constant. Along the S − (L + M) axis, the difference between S cones and the sum of L and M cones varies. Colors along the S-cone-isolating line range from violet to lime; intermediate isoluminant colors range from magenta to greenish; addition of an achromatic component to the magenta and greenish stimuli results in bright magenta to dark greenish. (B) Examples of stimuli: objects and non-objects, represented in colors that excite different directions in color space.

Figure 2

Trail outlooks. (A) Baseline experiment: Participants responded if the object was located in the first or the second interval. (B) Main experiment: Participants responded whether the presented item was an object or a non-object.

Figure 3

Suprathreshold and threshold contrasts for the eye movement experiment. Left side of the figure shows chromatic contrasts (S and L − M) while right side of the figure shows the luminance contrast in relation to S-cone contrast (S and L + M). Contrasts for each participant are represented with a single dot. C1: S-cone increment; C2: S-cone decrement; C3: intermediate isoluminant increment; C4: intermediate isoluminant decrement; C5: full-colour increment; C6: full-colour decrement.

Figure 4

Suprathreshold and threshold contrasts for the EEG experiment. Left side of the figure shows chromatic contrasts (S and L − M) while right side of the figure shows the luminance contrast in relation to S-cone contrast (S and L + M). Contrasts for each participant are represented with a single dot. C1: S-cone increment; C2: S-cone decrement; C3: intermediate isoluminant increment; C4: intermediate isoluminant decrement; C5: full-colour increment; C6: full-colour decrement.

Figure 5

Behavioral data. (A) accuracy; (B) mean of median response times. Error bars represent 95% confidence intervals.

Figure 6

Eye movement data: saccade properties. (A) Distribution of saccades by size. Black line depicts saccades during fixation cross and red line depicts saccades during picture presentation. (B) main sequence relation between speed and size of saccades for the period of picture presentation.

Figure 7

Eye movement data: saccade rates across time. Frequency plot of all fixational saccades in the period including −500 ms before picture onset and 1500 ms after picture onset. Solid red line indicates stimulus onset and the magenta rectangle highlights the period 200–700 ms post-stimulus which was the main focus of our analysis.

Figure 8

Evoked GBA. (A) Grand mean baseline-corrected TF-plot averaged at the regional mean sites (see panel B) across all conditions. Box indicates the time window for statistical analysis. (B) Grand mean amplitude-map (average across all conditions) for activity within the black box in Panel A). Box indicates electrode sites included in the regional mean. (C) Bar plot of amplitudes of evoked GBA for each condition at the regional mean during the selected time window, with 95% confidence interval bars.

Figure 9

Total GBA. (A) Grand mean baseline-corrected TF-plot averaged at the regional mean sites (see panel B) across all conditions. Box indicates the time window for statistical analysis. (B) Grand mean amplitude-map (average across all conditions) for activity within the black box in panel A). Box indicates electrode sites included in the regional mean. (C) Bar plot of amplitudes of total GBA for each condition at the regional mean during the selected time window, with 95% confidence interval bars.