Research ArticleNEUROSCIENCE

Rehearsal initiates systems memory consolidation, sleep makes it last

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Science Advances  24 Apr 2019:
Vol. 5, no. 4, eaav1695
DOI: 10.1126/sciadv.aav1695
  • Fig. 1 General design.

    Participants visited the laboratory twice and spent the 12-hour interval in between either awake during the day (wake group, n = 16) or went to bed normally (sleep group, n = 15). Each session consisted of seven encoding repetitions (E) of a word list of 28 concrete German nouns. Every repetition was followed by a self-paced free recall (R) of all remembered words. We refer to the encoding-recall repetition as rehearsal. During the second session, the word list consisted of 14 words known from the first session (dark blue) and 14 new words (light blue). Words were presented in each repetition one at a time in randomized order.

  • Fig. 2 Fast transition of memory systems contributions over repeated rehearsal.

    (A) The hippocampus (left) and the mPFC (right) showed decreasing activity between the first and the last learning repetition of the first session. (B) The β values within these clusters show a significant linear decline over all learning repetitions. (C) Single-subject regression slopes based on all learning repetitions confirm the decrease in activity within hippocampal and mPFC voxels. Each panel shows a histogram of regression slopes over all participants (left) and individual regression slopes plotted as regression lines over the seven learning repetitions (right, gray) and the average regression slope (right, black). (D) Activity in the precuneus (left) and in the IPL (right) showed significant increases between the first and the last learning repetition. (E) The β estimates based on the precuneus and the IPL clusters, respectively, show significant linear increases over all learning repetitions. (F) Single-subject regression slopes based on all learning repetitions confirm the increase in activity within the precuneus and the IPL clusters. Results are displayed as in (C). All T maps in (A) and (D) are displayed at a whole-brain family-wise error (FWE)–corrected threshold of PFWE ≤ 0.05 for clusters exceeding 20 voxels and are not masked. Error bars in (B) and (E) indicate SEM.

  • Fig. 3 Increasing precuneus activity over recall repetitions.

    (A) The right precuneus showed increasing activity between the first and the last recall repetition of the first session. Further regions displaying significant increases at whole-brain FWE-corrected threshold of PFWE ≤ 0.05 are given in table S3. T maps are displayed at a whole-brain FWE-corrected threshold of PFWE ≤ 0.05 (B) The β estimates from the precuneus cluster. Single-subject regression statistics indicated a linear increase in the precuneus β estimates over recall repetitions (t30 = 4.385, P < 0.001, mean r = 0.469).

  • Fig. 4 Fast transition of memory systems contributions over repeated rehearsal of new words in the second session.

    (A) The hippocampus (left) and the mPFC (right) showed decreasing activity between the first and the last learning repetition of the first session. The bottom panels show the mean β estimates within the left hippocampus and the mPFC for the seven repetitions. (B) Activity in the precuneus (left) and in the IPL (right) showed significant increases between the first and the last learning repetition. The bottom panels show the mean β estimates within the precuneus and the IPL for the seven learning repetitions. Because the number of stimuli was half that of session 1, only the hippocampus showed a whole-brain FWE-corrected effect. All T maps are displayed at P ≤ 0.001 for clusters exceeding 20 voxels and are not masked.

  • Fig. 5 Parietal long-term memory representations.

    Both the precuneus and the IPL showed an increased BOLD response to the first presentation of old words compared to new words 12 hours after the initial learning (small-volume FWE corrected at PSVC ≤ 0.05, ROI based on all significant whole-brain–corrected voxels that decrease over learning repetitions in the first session; Fig. 2). T maps are displayed at P ≤ 0.001 for clusters exceeding 20 voxels.

  • Fig. 6 Stabilization of hippocampal signaling over sleep.

    Sleep following repeated rehearsal alters hippocampal involvement during the memory task on the next day (sleep/wake × old/new × learning repetitions). This contrast was calculated for the mean β estimates in the left hippocampus (structural mask; left). The β estimates within the hippocampus showed a stabilization of the hippocampal response to old words after sleep: Initial activity in the sleep group is low and does not decrease significantly over repetitions. For new words in the sleep group, hippocampal activity mirrors that of the first session: Initial activity is high and decreases over repeated rehearsal. Similar activity decreases were observed for old words in the wake group but only showed a trend for new words (P = 0.075). Error bars indicate SEM, *P ≤ 0.05, t indicates P ≤ 0.1, n.s., not significant.

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/5/4/eaav1695/DC1

    Fig. S1. Memory performance.

    Table S1. List of regions with decreasing activity over repeated learning (session 1).

    Table S2. List of regions with increasing activity over repeated learning (session 1).

    Table S3. List of regions with activity changes over repeated recall (session 1).

    Table S4. List of regions with decreasing activity over repeated learning of new words (session 2).

    Table S5. List of regions with increasing activity over repeated learning of new words (session 2).

    Table S6. List of regions with a stronger response to old compared to new words (session 2).

    Table S7. List of regions with a stronger response to new compared to old words (session 2).

  • Supplementary Materials

    This PDF file includes:

    • Fig. S1. Memory performance.
    • Table S1. List of regions with decreasing activity over repeated learning (session 1).
    • Table S2. List of regions with increasing activity over repeated learning (session 1).
    • Table S3. List of regions with activity changes over repeated recall (session 1).
    • Table S4. List of regions with decreasing activity over repeated learning of new words (session 2).
    • Table S5. List of regions with increasing activity over repeated learning of new words (session 2).
    • Table S6. List of regions with a stronger response to old compared to new words (session 2).
    • Table S7. List of regions with a stronger response to new compared to old words (session 2).

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