Stimulus Load and Oscillatory Activity in Higher Cortex

Abstract

Exploring and exploiting a rich visual environment requires perceiving, attending, and remembering multiple objects simultaneously. Recent studies have suggested that this mental "juggling" of multiple objects may depend on oscillatory neural dynamics. We recorded local field potentials from the lateral intraparietal area, frontal eye fields, and lateral prefrontal cortex while monkeys maintained variable numbers of visual stimuli in working memory. Behavior suggested independent processing of stimuli in each hemifield. During stimulus presentation, higher-frequency power (50-100 Hz) increased with the number of stimuli (load) in the contralateral hemifield, whereas lower-frequency power (8-50 Hz) decreased with the total number of stimuli in both hemifields. During the memory delay, lower-frequency power increased with contralateral load. Load effects on higher frequencies during stimulus encoding and lower frequencies during the memory delay were stronger when neural activity also signaled the location of the stimuli. Like power, higher-frequency synchrony increased with load, but beta synchrony (16-30 Hz) showed the opposite effect, increasing when power decreased (stimulus presentation) and decreasing when power increased (memory delay). Our results suggest roles for lower-frequency oscillations in top-down processing and higher-frequency oscillations in bottom-up processing.

Keywords: frontal eye fields; lateral intraparietal area; power; prefrontal cortex; synchrony; working memory.

© The Author 2015. Published by Oxford University Press. All rights reserved. For Permissions, please e-mail: journals.permissions@oup.com.

Figures

Figure 1.

(A) Change localization task. After fixating for 500 ms, animals saw an array of colored squares for 800 ms. These squares then disappeared, and subjects were required to maintain the colors of these squares in memory for a variable delay of 800–1000 ms. The array then reappeared with a change to the color of one square. The animal was rewarded for saccading to the changed square. (B) Average behavioral performance according to the number of squares on the same side as the changed stimulus (“target side”) and the number of squares on the opposite side. Performance depended on the number of squares on the target side, not the total number of squares. (C) Mutual information between the location of the target stimulus and the animal's choice given the display for total loads 2 through 5. (D) Mutual information between the location of the target stimulus and the animal's choice given the display for loads 1, 2, and 3 in the target hemifield. Error bars reflect 95% confidence intervals based on nonparametric bootstrapping across sessions.

Figure 2.

(A) Percent power change for contralateral loads 1, 2, and 3 relative to the model intercept across frequencies and time. First dashed line indicates time of sample onset. Second dashed line indicates time of sample offset. (B) Percent power change per contralateral stimulus. Boxes indicate significant modulations (bootstrap Z-test, P < 0.05, Holm corrected for 22 frequencies × 211 time points).

Figure 3.

(A) Percent power change for ipsilateral loads 1, 2, and 3 relative to the model intercept across frequencies and time. (B) Percent power change per ipsilateral stimulus. Boxes indicate significant modulations (bootstrap Z-test, P < 0.05, Holm corrected for 22 frequencies × 211 time points).

Figure 4.

Percent power change per contralateral (left) and ipsilateral (right) item by region, grouped by lower frequencies (left bar group) and higher frequencies (right bar group) during the early sample (A), late sample/early delay (B), and late delay (C). Error bars are standard error of the mean. Asterisks indicate significant differences (bootstrap Z-test, P < 0.05, Holm corrected for 2 bands × 3 epochs × 3 regions). White hatching indicates significant differences in modulation by ipsilateral and contralateral load (bootstrap Z-test, P < 0.05, Holm corrected). P-values above bars indicate significant differences between regions (F-test, P < 0.05).

Figure 5.

Percent power change for contralateral loads (left) and ipsilateral loads (right) 1, 2, and 3 relative to load 0, for epochs and frequency bands. Asterisks indicate significance of all pairwise differences for the band, region, and epoch (permutation test, P < 0.05, Holm corrected for 2 bands × 3 epochs × 3 regions).

Figure 6.

Comparison of position information (adjusted R2) for contralateral and ipsilateral stimuli. Error bars are standard error of the mean. Asterisks indicate significant information (nonparametric bootstrap test, P < 0.05, Holm corrected for 2 bands × 3 epochs × 3 regions). White hatching indicates significant differences in modulation by ipsilateral and contralateral load (nonparametric paired bootstrap test, P < 0.05, Holm corrected).

Figure 7.

Percent power change per contralateral item for position-selective and nonposition-selective electrodes. Asterisks indicate significant modulation by load (one-sample t-test, P < 0.05, Holm corrected for 2 bands × 3 epochs). P-values above bars indicate significant differences between position-selective and nonposition-selective electrodes (unequal variance t-test, P < 0.05, Holm corrected).

Figure 8.

Correlation of single-trial coherence surrogates with contralateral load. Boxes indicate significant modulations (bootstrap Z-test, P < 0.05, Holm corrected for 22 frequencies × 211 time points). The same analysis for ipsilateral load is shown in Supplementary Figure S2.

Figure 9.

Correlation of single-trial coherence surrogates with contralateral load for frequency bands and epochs. Asterisks indicate significant differences (bootstrap Z-test, P < 0.05, Holm corrected for 5 bands × 4 epochs × 6 region pairs). White hatching indicates significant differences in modulation by ipsilateral and contralateral load (bootstrap Z-test, P < 0.05, Holm corrected). The same analysis for ipsilateral load is shown in Supplementary Figure S3.