Oscillatory activity during maintenance of spatial and temporal information in working memory

Abstract

Working memory (WM) processes help keep information in an active state so it can be used to guide future behavior. Although numerous studies have investigated brain activity associated with spatial WM in humans and monkeys, little research has focused on the neural mechanisms of WM for temporal order information, and how processing of temporal and spatial information might differ. Available evidence indicates that similar frontoparietal regions are recruited during temporal and spatial WM, although there are data suggesting that they are distinct processes. The mechanisms that allow for differential maintenance of these two types of information are unclear. One possibility is that neural oscillations may differentially contribute to temporal and spatial WM. In the present study, we used scalp electroencephalography (EEG) to compare patterns of oscillatory activity during maintenance of spatial and temporal information in WM. Time-frequency analysis of EEG data revealed enhanced left frontal theta (5-8 Hz), enhanced posterior alpha (9-12 Hz), and enhanced left posterior beta (14-28 Hz) power during the delay period of correct temporal order trials compared to correct spatial trials. In contrast, gamma (30-50 Hz) power at right lateral frontal sites was increased during the delay period of spatial WM trials, as compared to temporal WM trials. The present results are consistent with the idea that neural oscillatory patterns provide distinct mechanisms for the maintenance of temporal and spatial information in WM. Specifically, theta oscillations are most critical for the maintenance of temporal information in WM. Possible roles of higher frequency oscillations in temporal and spatial memory are also discussed.

Figure 1

Schematic depiction of stimuli and timing of trial events in the WM task.

Figure 2

Theta, alpha, and beta oscillations are enhanced during maintenance of temporal order relative to maintenance of spatial location. A. Topographic maps of the difference in oscillatory power between correct order and correct spatial location trials are shown in theta (5–8 Hz; top), alpha (9–12 Hz; middle), and beta (14–28 Hz; bottom) frequency bands during the delay period. B. Averaged time-frequency spectrograms of the temporal – spatial power difference are shown across all electrode clusters. The distribution of electrode sites is depicted in the cluster map within the legend. Time (ms) during the delay period is plotted on the x-axis and frequency (log scale) is plotted on the y-axis. These plots display activity throughout the entire duration of the delay period. Time zero indicates the offset of the final encoding stimulus, and the last time point (4000 ms) represents the offset of the delay period fixation cross. Warm/hot colors represent enhanced power in temporal order trials as compared to spatial location trials, whereas cool/cold colors represent enhanced power in spatial location trials as compared to temporal order trials. Dashed boxes highlight the effects observed in the theta band at left frontal electrode sites, and the alpha and beta effects at left posterior electrode sites. Dashed boxes also reflect the time window used in statistical analyses (from 1000 – 3000 ms).

Figure 3

Gamma oscillations are enhanced during maintenance of spatial location relative to maintenance of temporal order. A. The topographic map of the difference in oscillatory power between correct spatial and correct temporal trials is shown in the gamma (30–50 Hz) frequency band during the delay period. B. The averaged time-frequency spectrogram of the spatial – temporal power difference is shown for the right frontal electrode cluster (see the cluster map in the legend for the locations of these electrodes). Time (ms) during the delay period is plotted on the x-axis; frequency is plotted on the y-axis. Warm/hot colors represent enhanced power in spatial location compared to temporal order trials. The dashed box highlights the frequency band and time window (1000–3000 ms) used in statistical analysis.

Figure 4

CSD demonstrates enhancement of gamma oscillations in spatial trials relative to temporal trials. A. The averaged time-frequency spectrogram (calculated from analyses of CSD waveforms) of the spatial – temporal power difference is shown across all electrode clusters (see the cluster map in the legend for the distribution of electrode sites for all clusters). Time (ms) during the delay period is plotted on the x-axis; frequency is plotted on the y-axis. Warm/hot colors represent enhanced power in spatial location compared to temporal order trials. Enhanced gamma (30–50 Hz) effects are highlighted in the dashed box, and represent the frequency band and time window (1000–3000 ms) used in statistical analysis. B. The topographic map of the difference in oscillatory power between correct spatial and correct temporal trials is shown in the gamma (30–50 Hz) frequency band during the delay period. Warm/hot colors represent enhanced power in spatial location compared to temporal order trials.