Modulation of neural oscillations during working memory update, maintenance, and readout: An hdEEG study

Marianna Semprini, Gaia Bonassi, Federico Barban, Elisa Pelosin, Riccardo Iandolo, Michela Chiappalone, Dante Mantini, Laura Avanzino, Marianna Semprini, Gaia Bonassi, Federico Barban, Elisa Pelosin, Riccardo Iandolo, Michela Chiappalone, Dante Mantini, Laura Avanzino

Abstract

Working memory (WM) performance is very often measured using the n-back task, in which the participant is presented with a sequence of stimuli, and required to indicate whether the current stimulus matches the one presented n steps earlier. In this study, we used high-density electroencephalography (hdEEG) coupled to source localization to obtain information on spatial distribution and temporal dynamics of neural oscillations associated with WM update, maintenance and readout. Specifically, we a priori selected regions from a large fronto-parietal network, including also the insula and the cerebellum, and we analyzed modulation of neural oscillations by event-related desynchronization and synchronization (ERD/ERS). During update and readout, we found larger θ ERS and smaller β ERS respect to maintenance in all the selected areas. γLOW and γHIGH bands oscillations decreased in the frontal and insular cortices of the left hemisphere. In the maintenance phase we observed decreased θ oscillations and increased β oscillations (ERS) in most of the selected posterior areas and focally increased oscillations in γLOW and γHIGH bands in the frontal and insular cortices of the left hemisphere. Finally, during WM readout, we also found a focal modulation of the γLOW band in the left fusiform cortex and cerebellum, depending on the response trial type (true positive vs. true negative). Overall, our study demonstrated specific spectral signatures associated with updating of memory information, WM maintenance, and readout, with relatively high spatial resolution.

Keywords: ERS/ERD; hdEEG; n-back; network; neural oscillations; working memory.

Conflict of interest statement

The authors declare no conflict of interest.

© 2020 The Authors. Human Brain Mapping published by Wiley Periodicals LLC.

Figures

FIGURE 1
FIGURE 1
Outline of working memory task. (a) Graphical representation of n‐back tasks: the current letter (framed in red) must be compared with the one presented n times before, n being either 2 or 3 depending on the task. (b) Contingency matrix of possible behavioral outcomes: true positive (TP), true negative (TN), false positive (FP), and false negative (FN). (c) Timeline representing 2‐back (top) and 3‐back (bottom) task timings and intervals chosen for hdEEG analysis. Letters appear on screen every 2500 ms and remain displayed for 500 ms. Analysis of memory update was performed by comparing baseline (500 ms preceding letter presentation, indicated as “BASE” in the figure) with a portion of signal ranging from 100 to 1000 ms post stimulus‐letter onset (900 ms in total). Analysis of memory update was performed by comparing baseline (500 ms preceding distractor‐letter presentation) with a portion of signal ranging from 1000 to 2000 ms post distractor‐letter onset (1000 ms in total). Analysis of readout was performed by comparing baseline (500 ms preceding probe‐letter presentation) with a portion of signal ranging from 100 to 600 ms post probe‐letter onset (500 ms in total)
FIGURE 2
FIGURE 2
Cognitive performance of n‐back task. (a) Reaction times obtained by single subjects during the 2‐back (light gray) and 3‐back (dark gray) task (mean ± standard error of TP trials). (b) Average reaction time obtained in the two tasks (mean ± standard error of single subjects’ scores). (c) Normalized reaction times distribution of reaction times during the 2‐back (top) and 3‐back (bottom) tasks; data obtained from all the TP trials of all subjects. (d) Accuracy obtained by single subjects during the 2‐back (light gray) and 3‐back (dark gray) task. (e) Average reaction time obtained in the two tasks (mean ± standard error of single subjects’ scores). (f) Accuracy vs mean reaction times of single subjects in the 2‐back (light gray dots) and 3‐back (dark gray dots) task
FIGURE 3
FIGURE 3
Effect of PHASE in the θ and β band. (a) Violin plots of ERS/ERD variation in the θ (blue) and β (light blue) bands during update (top), maintenance (middle) and readout (bottom). Superimposed in grey are boxplots describing the median value (white dot), 25th and 75th percentiles (extremes of the thick grey line), and full data range (extremes of the thin grey line) of the distributions. (b) Temporal evolution of band power in the θ (blue) and β (light blue) during the 2‐back task for PPC‐R, CerT‐R, PPC‐L, and Fus‐L). (c) Temporal evolution (mean – thick lines, standard deviation – shaded areas) of band power in the θ (blue) and β (light blue) during the 3‐back task for PPC‐R, CerT‐R, PPC‐L, and Fus‐L
FIGURE 4
FIGURE 4
Effect of PHASE in the γLOW and γHIGH band. (a) Violin plots of ERS/ERD variation in the γLOW (yellow) and γHIGH (orange) bands during update (top), maintenance (middle) and readout (bottom). Superimposed in grey are boxplots describing the median value (white dot), 25th and 75th percentiles (extremes of the thick grey line), and full data range (extremes of the thin grey line) of the distributions. (b) Temporal evolution (mean – thick lines, standard deviation – shaded areas) of band power in the γLOW (yellow) and γHIGH (orange) during the 2‐back task for FC‐L and InsCl‐L). (c) Temporal evolution of band power in the γLOW (yellow) and γHIGH (orange) during the 3‐back task for FC‐L and InsCl‐L
FIGURE 5
FIGURE 5
Interactions of main effects in the γLOW band. Bar plots of ERS/ERD variation in the γLOW band. Thick bars represent mean across, black thin bars represent standard deviation. Left panels (a1, b1, c1) are referred to TASK*PHASE interaction, central panels (a2, b2, c2) to TRAIL*PHASE interaction, and right panels (a3, b3, c3) to TRIAL*TASK*PHASE interaction. Top panels (a1, a2, a3) represent ERS/ERD during update, central panels (b1, b2, b3) during maintenance and bottom panels (c1, c2, c3) during readout. Level of significance is reported: ** p

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