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Auditory cortical alpha/beta desynchronization prioritizes the representation of memory items during a retention period

  1. Nathan Weisz  Is a corresponding author
  2. Nadine Gabriele Kraft
  3. Gianpaolo Demarchi  Is a corresponding author
  1. Centre for Cognitive Neuroscience and Department of Psychology, Paris-Lodron Universität Salzburg, Austria
Research Article
Cite this article as: eLife 2020;9:e55508 doi: 10.7554/eLife.55508
6 figures, 1 data set and 1 additional file

Figures

Modified auditory Sternberg paradigm and cartoon depiction of analysis rationale.

(A) A sequence of four consonants spoken by a female voice was presented. After the retention period, either a strong (consonant spoken by a male voice) or a weak (scrambled consonant) distractor was presented (at 1 s). Distractor type was kept constant during a block. Subsequently, participants indicated by a button press whether the probe was part of the memory set (‘part’) or not (‘no part’). At an individual level, temporal decoding was performed on whether the probe was part of memory set or not. When the probe was part of the memory set, it should have been seen to share distinct neural patterns with those elicited by the items of the memory set, while this should not have been the case when the stimulus was not part of the memory set. By time-generalizing the classifiers trained on the probe to the period of the retention interval, we obtained a quantitative proxy for the strength of memorized information at the time of distractor presentation. The results were then statistically contrasted between weak and strong distractors across the group. (B) Alpha/Beta power in lSTG was calculated at a single trial level in a pre-distractor period and was used to bin high and low power trials. For a 0.5-s pre-distractor period, analysis analogous to (A) was performed to quantify the relationship between regionally specific alpha/beta power and strength of memorized information. A prioritization account would predict that lower ‘desynchronized’ states go along with relatively increased strength of memorized information. This pattern should be captured when contrasting the bins across the entire group and when taking into account the extent of modulation within single participants. An inhibition account would predict an opposing pattern.

Decoding of probe-related information.

(A) Results of the temporal decoding of MEG sensor-level activity after the probe presentation to classify whether it was part of the memory set or not (see also Figure 1A for rationale). Above-chance detection performance (AUC = area under the receiver operating characteristic [ROC] curve) was found commencing ~300 ms after the probe onset (at 2.0 s) and lasting at least until the response was prompted. Informative activity for this decoding as a function of time is shown on the right (green areas outlining the expanse of the cluster that results following a nonparametric permutation test for the 0.3–0.7-s post-probe onset interval). Within the relevant time interval (in blue-dotted box) informative activity emerges early in left STG and progressively spreads to further temporal, parietal and frontal areas. Data used for plotting the results of the temporal decoding at 10.17605/OSF.IO/753MK. (B) The time generalization result is shown separately for the strong and weak distractor conditions (left and middle panels). Trivially, the strongest classification results are obtained approximately at the onset of the probe (at 2 s). Relatively decreased decoding performance (AUC <0.5) was obtained prior to the onset of the strong distractor. Statistical comparison of strong vs weak distractor conditions revealed two peak effects at ~400 ms and ~200 ms preceding the distractor onset, although only the difference closer to distractor onset was significant (pcluster = 0.0156) at the cluster level (right panel). Data used for plotting the time generalized result at 10.17605/OSF.IO/4CV83.

Pre-distractor alpha power modulations in the left superior temporal gyrus.

(A) Time-frequency representations of the induced power show strong ongoing alpha/beta activity with a peak at ~10 Hz. No baseline normalization was applied. The vertical dots indicate a 500-ms period preceding the occurrence of the distractor. An alpha/beta power decrease in the strong vs the weak distractor condition can be seen (left and middle panel). The notion is supported by the outcome of a nonparametric permutation test leading to a significant difference at cluster level (marked by a black contour; pcluster = 0.0104) over an alpha to beta range with peak differences at ~12–13 and 21–22 Hz (right panel). For both ranges, the peak effects were observed at 0.7 s, that is, ~300 ms prior to the anticipated onset of the distractor. Data used for plotting induced power at 10.17605/OSF.IO/4WUYD. (B) Time-frequency representations of the evoked power. Post-distractor alpha enhancements are seen, but no prominent alpha preceded the distractor (left and middle panel). The nonparametric statistical test at cluster level showed no difference (right panel). Data used for plotting evoked power at 10.17605/OSF.IO/TYZC8.

Relationship between alpha and beta power modulation and strength of memorized information (operationalized via the time-generalized decoding approach; see Figure 1) in the 0.5-s pre-distractor period.

(A) Average strength of memorized information in the relevant period split between strong and weak power trials. At the group-level, significant modulation is seen only for the beta band, with relatively increased strength of memorized information for weak power trials. (B) Interindividual variation in the extent to which alpha power was modulated between high- and low-power trials within a participant (a higher value on the x-axis reflects a more extreme power difference between high- and low -power trials) was negatively correlated with the modulation of strength of memorized information (see main text). This effect was in large part driven by the strong power trials. (C) The same correlation analysis showed no effect in the beta band. Overall, power in the alpha range was more strongly modulated as compared to that in the beta range. Data used for plotting the relation between alpha power modulations and probe-related information is at 10.17605/OSF.IO/QG3KB.

Follow-up analysis to elucidate which frequency band drives decoding performance post-probe presentation (used as trained classifiers time-generalized to retention period).

(A) Results of temporal decoding on MEG sensor-level activity analogous to Figure 2A. (B) Average decoding performance for the relevant 0.4–0.7-s post-probe time period (used for results displayed in Figure 2B and Figure 4) shows that neither alpha nor beta band activity contains information with regards to the memorized item. As shown previously, above-chance decoding performance is seen for broadband activity and this effect appears to be driven strongly by activity in the theta range. Although amplitude information was sufficient for decoding above chance for broadband and theta activity, decoding performance was improved when the temporal fine-structure was maintained.

Author response image 1
The image on the left shows the (unthresholded) T-values averaged between in the.

5 to 1s period, i.e. the.5s window preceding the distractor. Separate (negative) peaks can be identified at 13 Hz and 22 Hz. Also when inspecting which frequencies contribute to the negative cluster (middle panel) it is clear that the cluster comprises two peaks at the respective frequencies. Displaying the temporal profiles for these frequencies (right panel) it can be seen that peaks are reached at ~.7s, i.e. ~.3s prior to the presentation of the distractor. Given these follow-up inspections of the cluster, in the original manuscript we focused on the lower-frequency contribution, i.e. multitaper FFT centred at 13Hz and.7s using reasonable parameters to estimate power.

Data availability

All the preprocessed, downsampled raw data and processing MATLAB and R scripts could be found at https://doi.org/10.17605/OSF.IO/PW9RD.

The following data sets were generated
  1. 1
    Open Science Framework
    1. N Weisz
    2. N Kraft
    3. G Demarchi
    (2020)
    Auditory cortical alpha / beta desynchronization prioritizes the representation of memory items during a retention period.
    https://doi.org/10.17605/OSF.IO/PW9RD

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