Neural oscillations associated with item and temporal order maintenance in working memory

Abstract

The ability to retain information in working memory (WM) requires not only the active maintenance of information about specific items, but also the temporal order in which the items appeared. Although many studies have investigated the neural mechanisms of item maintenance, little is known about the neural mechanisms of temporal order maintenance in WM. Here, we used electroencephalography (EEG) to compare neural oscillations during WM tasks that required maintenance of item or temporal order information. Behavioral results revealed that accuracy and reaction times were comparable between the two conditions, suggesting that task difficulty was matched between the item and temporal order WM tasks. EEG analyses indicated that theta (5-7 Hz) oscillations over prefrontal sites were increased during temporal order maintenance, whereas alpha oscillations (9-12 Hz) over posterior parietal and lateral occipital sites were increased during item maintenance. The frontal theta enhancement was primarily evident in high performers on the order WM task, whereas the posterior alpha enhancement was primarily evident in high performers on the item WM task. These results support the idea that frontal theta and posterior alpha oscillations are differentially related to maintenance of item and temporal order information.

Figure 1.

Schematic diagram of the working memory tasks.

Figure 2.

Frontal theta is enhanced during order maintenance, whereas posterior alpha is enhanced during item maintenance. Time-frequency spectrograms illustrate the difference in oscillatory power between correct order and correct item trials. The x-axis represents time relative to the onset of the 4 s delay period and the y-axis represents logarithmically spaced frequencies. Effects are separately plotted for each of the nine analyzed electrode clusters. Hotter colors denote relative increases in oscillatory power during order trials; cool colors denote relative increases in oscillatory power during item trials.

Figure 3.

Topography of frontal theta and posterior alpha effects. A, Topographic map of the difference in oscillatory power between correct order and correct item trials in theta (θ) frequency band (5–7 Hz) in the time window of 600–3400 ms following onset of the delay. B, The same as in A, except that oscillatory power is computed from surface Laplacian-transformed single-trial EEG epochs. C, Topographic map of the difference in oscillatory power between correct item and correct order trials in the alpha (α) frequency band (9–12 Hz) in the time window of 600–3400 ms during the delay. D, The same as in C, except that oscillatory power is computed from surface Laplacian-transformed single-trial EEG epochs. CSD, Current source density.

Figure 4.

Theta and alpha effects for high and low performers on the working memory tasks. A, Averaged spectrogram of the order − item power difference for the top 10 order performers at the middle-frontal electrode cluster. B, Averaged spectrogram for the bottom 10 order performers, showing the same contrast and electrode cluster as in A. C, Averaged spectrogram of the order − item power difference for the top 10 item performers at the left-posterior electrode cluster. D, Averaged spectrogram for the bottom 10 item performers, showing the same contrast and electrode cluster as in C.

Figure 5.

Frontal theta enhancements during order maintenance are negatively correlated with posterior alpha enhancements during item maintenance. The scatter plot depicts individual differences in the alpha power enhancement during item trials at the left-posterior electrode cluster (y-axis) relative to the theta enhancement at the middle-frontal electrode cluster during order trials (x-axis). Pearson product-moment correlation coefficient, r = −0.48. Linear least-squares best fits to the data are superimposed.