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Research Articles, Behavioral/Cognitive

Transformed Neural Pattern Reinstatement during Episodic Memory Retrieval

Xiaoqian Xiao, Qi Dong, Jiahong Gao, Weiwei Men, Russell A. Poldrack and Gui Xue
Journal of Neuroscience 15 March 2017, 37 (11) 2986-2998; https://doi.org/10.1523/JNEUROSCI.2324-16.2017
Xiaoqian Xiao
1State Key Laboratory of Cognitive Neuroscience and Learning and IDG/McGovern Institute of Brain Research, Beijing Normal University, Beijing 100875, PR China,
2Center for Collaboration and Innovation in Brain and Learning Sciences, Beijing Normal University, Beijing 100875, PR China,
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Qi Dong
1State Key Laboratory of Cognitive Neuroscience and Learning and IDG/McGovern Institute of Brain Research, Beijing Normal University, Beijing 100875, PR China,
2Center for Collaboration and Innovation in Brain and Learning Sciences, Beijing Normal University, Beijing 100875, PR China,
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Jiahong Gao
3Center for MRI Research and Beijing City Key Laboratory for Medical Physics and Engineering, School of Physics and McGovern Institute for Brain Research, Peking University, Beijing 100871, PR China, and
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Weiwei Men
3Center for MRI Research and Beijing City Key Laboratory for Medical Physics and Engineering, School of Physics and McGovern Institute for Brain Research, Peking University, Beijing 100871, PR China, and
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Russell A. Poldrack
4Department of Psychology, Stanford University, Stanford, California 94305
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Gui Xue
1State Key Laboratory of Cognitive Neuroscience and Learning and IDG/McGovern Institute of Brain Research, Beijing Normal University, Beijing 100875, PR China,
2Center for Collaboration and Innovation in Brain and Learning Sciences, Beijing Normal University, Beijing 100875, PR China,
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  • Figure 1.
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    Figure 1.

    Experiment paradigm. A, Slow event-related design (16 s for each trial) was used to better estimate brain responses associated with single items. Self-spaced orientation judgment task applied during 8 s intertrial interval to prevent further encoding of the word cue-picture association. B, The arrangement of scanning runs. There were four encoding-retrieval sessions in total. C, Strategies to examine item-specific encoding (left), retrieval (middle), and ERS (right). The item specificity was obtained by comparing similarities between different cues-same picture (C−P+) pairs with different cues-different picture pairs (C−P−; matched with C−P+ pair in memory performance, category, and lag). The words used as cues were actually presented in Chinese.

  • Figure 2.
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    Figure 2.

    ROI results for item-specific encoding, retrieval, and ERS. A, The location of the pre-defined anatomic ROIs. B, ROI results for item-specific encoding. C, ROI results for item-specific retrieval. D, ROI results for item-specific ERS. Error bars indicate within-subject error. After Bonferroni correction for 14 ROIs (p < 0.0036), effect of item-specific encoding survived in bilateral VVC, item-specific retrieval survived in bilateral AG, MFG, LSMG, and LIFG. ***p < 0.001/14. **p < 0.01/14. *p < 0.05/14.

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    Figure 3.

    Time-resolved ERS between encoding and retrieval. The BOLD responses for each of the 3 TRs after stimulus onset during encoding and retrieval (with 4 s delay to account for the slow BOLD response) were extracted, and the ERS was calculated between representation at each of the TRs during encoding and that during retrieval. Values in the heat maps are the mean item-specific ERS [ERS(C−P+) − ERS(C−P−)] across subjects.

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    Figure 4.

    Whole-brain searchlight results. Item-specific representation for encoding and retrieval, their direct comparisons, and ERS were rendered onto a population-averaged surface atlas (Xia et al., 2013). All activations were thresholded using cluster detection statistics, with a height threshold of z > 3.1 and a cluster probability of p < 0.05, corrected for whole-brain multiple comparisons using Gaussian Random Field Theory.

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    Figure 5.

    Item-specific representation in the MTL subregions. A, The segmentation of the MTL from one sample subject. There are five subregions of hippocampus: CA1, CA2, DG, CA3, and subiculum. CA2 and CA3 were not included in further analysis considering their relatively limited voxels. The anterior portion of parahippocampus was divided into two parts: PRc (which further divided into BA35 and BA36) and ERc. B, Item-specific representation in these regions for encoding (left), retrieval (middle), and ERS (right). Error bars indicate within-subject error. *p < 0.05, uncorrected.

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    Figure 6.

    Feature selection results. Left, Feature selection results in the VVC. Right, Feature selection results in the FPC. Error bars indicate within-subject error. EE, Item-specific encoding in voxels selected based on encoding data; ER, item-specific retrieval in voxels selected based on encoding data; RE, item-specific encoding in voxels selected based on retrieval data; RR, item-specific retrieval in voxels selected based on retrieval data.

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    Figure 7.

    Cross-region pattern reinstatement. Representational similarity matrix for encoding (A) and retrieval phase (B). Data are from one ROI (i.e., LVVC) of one participant (Subject 3). For each of the 48 pictures, the representational similarity matrix was obtained by calculating the pairwise Pearson correlation of activation pattern between each of the 48 pictures and the other 23 pictures from different run (the same picture pairs were removed), separately for encoding and retrieval phase. C, Heat-map for group-averaged encoding-retrieval representational connectivity within and across brain regions. D, Bar graphs of within-region encoding-retrieval representational connectivity (i.e., within-region reinstatement). E, F, Bar graphs of across-region encoding-retrieval representational connectivity (i.e., cross-region reinstatement) for the left and right VVC, respectively. Error bars indicate within-subject error.

Tables

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    Table 1.

    ROI-based results for item-specific encoding, retrieval, and ERSa

    EncodingRetrievalERS
    F(1,19)pF(1,19)pF(1,19)p
    LVVC40.0690.0000*4.9820.03791.7120.2064
    RVVC53.0180.0000*8.8980.00760.5270.4767
    LAG1.2960.269126.7790.0001*9.0480.0072
    RAG2.1500.158912.5870.0021*1.4340.2458
    LSMG1.1040.306624.0180.0001*8.4330.0091
    RSMG0.2900.59646.4190.02031.8470.1901
    LIFG4.6390.044319.3770.0003*4.1620.0555
    RIFG1.7660.19964.9270.03880.5760.4571
    LMFG2.3670.140420.9150.0002*8.5620.0087
    RMFG1.6830.210014.3000.0013*1.0590.3164
    LSFG0.0130.910810.3570.00452.1320.1606
    RSFG0.0450.83476.4880.01970.6870.4176
    mPFC0.0010.97994.6280.04451.0750.3129
    PCC1.4840.238012.6650.0021*8.7380.0081
    • ↵aThe numbers in the table indicate the comparison results between pattern similarities of different cues-same picture (C−P+) pairs and that of different cues-different pictures pairs (C−P−; matched with the C−P+ pairs in memory performance, stimulus category, and lag).

    • ↵*Significant results after Bonferroni correction across 14 ROIs (p < 0.05/14).

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    Table 2.

    Searchlight results for item-specific encoding, retrieval, and ERSa

    RegionxyzMaximum z
    EncodingLLOC−24−80364.65
    RLOC18−84−86.43
    RetrievalLLOC−26−66−504.33
    LIFG/LMFG−5610225.35
    RIFG/RMFG5012445.07
    LIPL−50−48465.15
    LTOF−20−52−165.10
    Encoding > retrievalLvLOC/LOFUS−14−96−64.32
    RvLOC/ROFUS20−88−105.24
    ERS (C−P+)LOC−24−68524.9
    RdLOC32−68564.07
    • ↵aWhole brain corrected (z = 3.1, p < 0.05).

    • View popup
    Table 3.

    Correlations between hippocampal subregion activity and cortical item-specific representationsa

    RegionERS encodingERS retrievalEncodingRetrieval
    CA1DGCA1DGCA1DGCA1DG
    LVVC0.5970.8810.1300.1690.000*0.001*0.0030.006
    RVVC0.4530.9990.4171.0000.0070.0030.0140.016
    LIFG0.2290.3690.5220.3410.1490.1110.0150.003
    RIFG0.3400.3140.7640.8571.0000.4930.0540.049
    LMFG0.1990.2780.8600.5770.1260.3880.0210.029
    RMFG0.4340.1540.4550.3410.2040.5740.1910.050
    LAG0.3220.4660.6510.3260.3140.5820.2580.379
    RAG0.5430.2360.0640.0690.5500.6140.2070.174
    LSMG0.1890.4660.4140.1510.9340.7980.1541.000
    RSMG0.4520.4270.1920.2410.7470.3450.3230.383
    • ↵aThe numbers in the table indicate the p value of the mixed-effects model. ERS encoding, Hippocampal encoding activities correlated with ERS; ERS retrieval, hippocampal retrieval activities correlated with ERS; Encoding, hippocampal encoding activities correlated with item-specific representation during encoding; Retrieval, hippocampal retrieval activities correlated with item-specific representation during retrieval.

    • ↵*Significant after Bonferroni correction across 20 models (p < 0.05/20).

    • View popup
    Table 4.

    Within-region reinstatement of representational structure

    ROItp
    LVVC3.2260.0022*
    LAG0.0370.4852
    LSMG−0.4280.6632
    LIFG4.7450.0001*
    LMFG3.6670.0008*
    RVVC5.3260.0000*
    RAG3.7090.0007*
    RSMG1.9850.0309
    RIFG2.9660.0040*
    RMFG4.7580.0001*
    • ↵*Significant results after Bonferroni correction across 10 ROIs (p < 0.05/10).

    • View popup
    Table 5.

    Cross-regions reinstatement (from VVC to frontoparietal cortex) of representational structure

    Encoding retrievalLVVCRVVC
    tptp
    LAG1.5830.06491.4590.0804
    LSMG2.9260.00431.1580.1306
    LIFG4.4270.0001*2.7100.0069
    LMFG4.4200.0001*4.4690.0001*
    RAG2.6670.00764.2790.0002*
    RSMG3.3370.0017*4.4310.0001*
    RIFG3.7450.0007*3.4730.0013*
    RMFG4.3150.0002*5.9950.0000*
    • ↵*Significant results after Bonferroni correction for 16 comparisons (p < 0.05/16).

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The Journal of Neuroscience: 37 (11)
Journal of Neuroscience
Vol. 37, Issue 11
15 Mar 2017
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Transformed Neural Pattern Reinstatement during Episodic Memory Retrieval
Xiaoqian Xiao, Qi Dong, Jiahong Gao, Weiwei Men, Russell A. Poldrack, Gui Xue
Journal of Neuroscience 15 March 2017, 37 (11) 2986-2998; DOI: 10.1523/JNEUROSCI.2324-16.2017

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Transformed Neural Pattern Reinstatement during Episodic Memory Retrieval
Xiaoqian Xiao, Qi Dong, Jiahong Gao, Weiwei Men, Russell A. Poldrack, Gui Xue
Journal of Neuroscience 15 March 2017, 37 (11) 2986-2998; DOI: 10.1523/JNEUROSCI.2324-16.2017
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Keywords

  • episodic memory
  • reinstatement
  • representational pattern similarity

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