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Research ArticleNew Research, Cognition and Behavior

Working Memory Replay Prioritizes Weakly Attended Events

Anna Jafarpour, Will Penny, Gareth Barnes, Robert T. Knight and Emrah Duzel
eNeuro 14 August 2017, 4 (4) ENEURO.0171-17.2017; DOI: https://doi.org/10.1523/ENEURO.0171-17.2017
Anna Jafarpour
1Department of Psychology, University of California, Berkeley, California 94720
2Helen Wills Neuroscience Institute, University of California, Berkeley, California 94720
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Will Penny
3Wellcome Trust Centre for Neuroimaging at University College London, London WC1N 3BG, United Kingdom
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Gareth Barnes
3Wellcome Trust Centre for Neuroimaging at University College London, London WC1N 3BG, United Kingdom
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Robert T. Knight
1Department of Psychology, University of California, Berkeley, California 94720
2Helen Wills Neuroscience Institute, University of California, Berkeley, California 94720
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Emrah Duzel
4Institute of Cognitive Neuroscience, London WC1N 3AR, United Kingdom
5German Centre for Neurodegenerative Diseases (DZNE), 39120 Magdeburg, Germany
6Institute of Cognitive Neurology and Dementia Research, Otto-Von-Guericke, University of Magdeburg, 39120 Magdeburg, Germany
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    Figure 1.

    Working memory experimental paradigm. A, Three stimuli were presented sequentially, each for 500 ms and with a 500 ms gap between them. There was a 5000 ms retention period in between the presentation of the third stimulus and memory probe tests. The memory probe tests entailed a “same” or “different” judgment and a temporal order decision. A 4000 ms intertrial interval preceded the next trial. The R period is shown in blue, and the ITI is shown in red. B, The stimuli were used in this experiment as follows a B, an F, and a C from three points of view, 60° to the left, front on, 60° to the right.

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    Figure 2.

    Schema of the multivariate pattern analysis using SVM. A, The state of neural activity during delay periods (R period or ITI) was decoded at each time bin, using three pairwise classifiers. A conservative threshold of d* (depicted in red) was used to reject representations that were close to the boundary and categorize them as N (the shaded area). B, A schematic example of decoded states during a delay period. C, The discrete time Markov chain model of state transition extracted from the schematic sequence in B.

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    Figure 3.

    Multivariate classification of stimulus categories: cross-validation performance, these plots show the mean classification performance of 3 pairwise classifiers across the group: left, F vs B; middle, F vs C; and right, B vs C. The x-axis is the time from stimulus (0 ms), and the y-axis is the classification performance in percentage. The error bars show the SEM. The gray area indicates significant classification after correction for multiple comparisons.

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    Figure 4.

    Decoding maintained categories in the delay period. A, The plot shows a representative example (from one subject) of the decoded R period and ITI before thresholding. The x-axis is the decoded time bins, and the y-axis is the trial number. B, The histogram of length of replay epochs during the R period (in blue) and during the ITI (in red) before threshold: the x-axis shows the epoch length. The top plot is the averaged epoch length from 20 to 3000 ms, and the bottom plot is the bar plot for bins of epoch lengths (20–140, 160–400, 420–1100, and 1200–3000 ms). Error bars show the SEM. The x-axis is length of the epoch of stimuli replay. C, The probability distribution of distance from classification boundaries during the R period (blue) and ITI (red). d* shows the threshold for rejecting 22% of classification outputs during retention. This threshold rejected 94% of classification outputs during ITI. D, The same histograms as in B but after applying the threshold. E, The bar plots show the percentage of trials where the stimuli from the selected category (left plot) or order in the sequence (right plot) was predominantly maintained. There was no significant effect of category or the order of stimuli.

  • Figure 5.
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    Figure 5.

    Difference in the averaged probability of state transition matrix is reflected by the thickness of the arrows. The probabilities of all transitions were different between the R periods and ITIs. Red arrows show the transitions that occurred more often during the ITI than the R period, and blue arrows show the opposite situation. There was no difference between the probabilities of forward (1-2-3) and backward (3-2-1) transitions.

  • Figure 6.
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    Figure 6.

    Effect of replay of 170 ms representation on WM performance. A, B, The detail test (A) and for the order test (B) show the hit rate (%) with respect to whether the stimuli were not replayed (none), were replayed for a short duration (shorter than 1100 ms), or replayed for a long duration (longer than 1100 ms). Error bars show the SEM. *p < 0.05.

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    Figure 7.

    ERFs during encoding differentiate between PM stimuli in working memory and non-PM stimuli. A, The plots graph the F-statistics in channel by time topography, focusing on the significant clusters at 125 ms from the stimuli onset. The bottom plot shows the channel by channel topography of the effect (x-axis is from left to right, and y-axis is from posterior to anterior). The top plots are channel by time. The x-axis on the left plot shows channels from left to right, and the x-axis on the right plot shows the channels from anterior to posterior. The peaks are highlighted with shapes in A to D. B, The top plot is for the effect that peaked at 125 ms (p < 0.001) in a left lateral channel, and the bottom plot is for the ERF effect at 453 ms (p = 0.008) in a right lateral channel. The plots show the ERF effects in the peak of significant clusters, which are highlighted by shapes (A and B). The dashed boxes show the timing of the effects. C, The plots graph the F-statistics in channel by time (the same as in A), focusing on the significant effect that peaked at 287 ms (p = 0.002). The effect is highlighted by a diamond shape in C and D. D, The plot shows the ERF effect at 287 ms from the stimuli onset in middle frontal channels. E, The ERF effect at 125 ms (A and B) was source localized in the bilateral occipital cortex. F, The ERF effect at 287 ms (C and D) was source localized in the posterior inferior temporal areas. A to D, Dotted line shows the onset of the stimuli at encoding.

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Working Memory Replay Prioritizes Weakly Attended Events
Anna Jafarpour, Will Penny, Gareth Barnes, Robert T. Knight, Emrah Duzel
eNeuro 14 August 2017, 4 (4) ENEURO.0171-17.2017; DOI: 10.1523/ENEURO.0171-17.2017

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Working Memory Replay Prioritizes Weakly Attended Events
Anna Jafarpour, Will Penny, Gareth Barnes, Robert T. Knight, Emrah Duzel
eNeuro 14 August 2017, 4 (4) ENEURO.0171-17.2017; DOI: 10.1523/ENEURO.0171-17.2017
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Keywords

  • Decoding
  • magnetoencephalography
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  • Working memory

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