Gamma-band activity in human prefrontal cortex codes for the number of relevant items maintained in working memory

Abstract

Previous studies in electrophysiology have provided consistent evidence for a relationship between neural oscillations in different frequency bands and the maintenance of information in working memory (WM). While the amplitude and cross-frequency coupling of neural oscillations have been shown to be modulated by the number of items retained during WM, interareal phase synchronization has been associated with the integration of distributed activity during WM maintenance. Together, these findings provided important insights into the oscillatory dynamics of cortical networks during WM. However, little is known about the cortical regions and frequencies that underlie the specific maintenance of behaviorally relevant information in WM. In the current study, we addressed this question with magnetoencephalography and a delayed match-to-sample task involving distractors in 25 human participants. Using spectral analysis and beamforming, we found a WM load-related increase in the gamma band (60-80 Hz) that was localized to the right intraparietal lobule and left Brodmann area 9 (BA9). WM-load related changes were also detected at alpha frequencies (10-14 Hz) in Brodmann area 6, but did not covary with the number of relevant WM-items. Finally, we decoded gamma-band source activity with a linear discriminant analysis and found that gamma-band activity in left BA9 predicted the number of target items maintained in WM. While the present data show that WM maintenance involves activity in the alpha and gamma band, our results highlight the specific contribution of gamma band delay activity in prefrontal cortex for the maintenance of behaviorally relevant items.

Figure 1.

The visuospatial working memory task. a, Example of a trial with distractors during the encoding. On one-third of the trials, participants were shown three red discs together with three blue discs (distractors), and participants were asked to memorize the positions of the red discs only and to ignore the positions of the blue discs. In the remaining trials, distractors were absent and either three or six red discs were presented. After a maintenance phase of 1.2 s, a test item was presented at a position identical (match) or different (nonmatch) to the sample array. b, Example of the memory arrays for the three conditions: load 3, distractor, and load 6. c, Sample traces of bandpass (60–80 Hz)-filtered MEG signals during the load 3, distractor, and load 6 conditions from one single subject. The recording comprises the baseline, encoding, delay, and retrieval periods. Note the enhanced oscillations in the gamma frequency in the delay phase of the load 6 condition.

Figure 2.

MEG power spectrum of delay activity. a, Power spectrum for frequencies from 4 to 20 Hz. b, Power spectrum for frequencies from 20 to 200 Hz. x-axis represents frequency and y-axis represents power. Spectral power is expressed in percent change relative to baseline activity. The solid horizontal black lines mark the frequency bands considered for analysis. The shaded area around the curve corresponds to SEM.

Figure 3.

MEG spectrograms for 20–120 Hz activity. a, Two-dimensional plots of the spectrograms for each condition. Note the transient increase of 10–14 Hz harmonic activity in the 20–28 Hz range. x-axis represents time and y-axis represents frequency. Spectral power is expressed in percent change relative (Rel. change) to baseline activity. b, Gamma-band activity was significantly modulated by task conditions in 100 (38%) sensors (p < 0.025; corrected; ANOVA). c, 60–80 Hz activity averaged across trials. The shaded area around the traces corresponds to the SEM. The light gray region marks the temporal interval of significant differences between conditions (p < 0.001; corrected; post hoc t test).

Figure 4.

Relationship between spectral power and behavioral performances. a, Linear regression between the increase of gamma band (60–80 Hz) delay activity from load 6 relative to load 3 and WM capacity. b, Linear regression between the increase of 60–80 Hz delay activity from load 6 relative to load 3 and the increase in reaction times from load 6 to load 3. c, Linear regression between alpha-band (10–14 Hz) delay activity and reaction times in the distractor condition. D, Linear regression between 10 and 14 Hz delay activity and reaction times in the load 6 condition. rel. change, Relative change.

Figure 5.

MEG spectrograms for 6–20 Hz activity (same convention as in Fig. 2). a, Two-dimensional plots of the spectrograms for each condition. x-axis represents time and y-axis represents frequency. Spectral power is expressed in percent change relative to baseline activity. b, Alpha-band power was significantly modulated across task conditions in 137 (58%) sensors (p < 0.025; corrected; ANOVA). c, Ten to fourteen hertz activity averaged across trials (p < 0.01; corrected; post hoc t test). Rel. change, Relative change.

Figure 6.

Delay activity at cortical source level. a, b, Images of the differences in 60–80 Hz activity (0.6 to 1.6 s) across task conditions during the delay period for the left BA 9 (a) and the intraparietal lobule (b). Effects are separately shown for the two brain regions and are displayed on axial, sagittal, and coronal sectional views of the MNI template brain. The locations of BA 9 and IPL are marked for orientation. All functional maps display dependent F values thresholded at p < 0.001 (uncorrected). c, d, Time course of 60–80 Hz activity for peak voxels averaged across trials in BA 9 (c) and IPL (d). The light gray region corresponds to the temporal interval of significant differences between conditions (p < 0.001; corrected; post hoc t test). c, In BA9 there was a significant increase of 60–80 Hz activity from 0.6 to 1.6 s during load 6 as compared to the load 3 and distractor conditions, while activity during load 3 and the distractor was similar. d, In contrast, in the IPL 60–80 Hz delay activity was increased during load 6 and the distractor as compared to load 3 and did not differ between the distractor and load 6 condition. e, Statistical map of the differences in 10–14 Hz activity (0.6 to 1.6 s) across task conditions during the delay period for Brodmann area 6. f, Time course of 10–14 Hz source activity averaged across trials for BA 6. Source activity in the 10–14 Hz range was significantly elevated during the delay (0.6 to 1.6 s) in the distractor and load 6 conditions as compared to load 3 and remained similar in the distractor and load 6 conditions.

Figure 7.

Single trial decoding of 60–80 Hz delay activity. a, Each dot represents classification performance in BA 9 (blue) and IPL (red) for each participant. Horizontal axis is the probability that a trial corresponding to load 6 is decoded correctly. Vertical axis is the probability that a trial corresponding to load 3 is decoded correctly. Line plots show the histograms of participant counts for the decode in each condition. b, Decoding of distractor trials for 60–80 Hz delay activity in BA9 (blue) and IPL (red). Vertical axis is the count of participants for which single trial gamma-band source activity in the distractor condition was decoded as load 3 or as load 6. Delay activity in BA 9 corresponding to distractor trials was decoded as load 3 with a probability of p = 0.77 (p < 0.025; corrected; two-sided binomial test), while in the IPL distractor trials had equal probability (p = 0.5) to be decoded as load 3 or load 6 (p = n.s.; two-sided binomial test).