Causal Contribution of Awake Post-encoding Processes to Episodic Memory Consolidation

Arielle Tambini, Mark D'Esposito, Arielle Tambini, Mark D'Esposito

Abstract

Stable representations of past experience are thought to depend on processes that unfold after events are initially encoded into memory. Post-encoding reactivation and hippocampal-cortical interactions are leading candidate mechanisms thought to support memory retention and stabilization across hippocampal-cortical networks. Although putative consolidation mechanisms have been observed during sleep and periods of awake rest, the direct causal contribution of awake consolidation mechanisms to later behavior is unclear, especially in humans. Moreover, it has been argued that observations of putative consolidation processes are epiphenomenal and not causally important, yet there are few tools to test the functional contribution of these mechanisms in humans. Here, we combined transcranial magnetic stimulation (TMS) and fMRI to test the role of awake consolidation processes by targeting hippocampal interactions with lateral occipital cortex (LOC). We applied theta-burst TMS to LOC (and a control site) to interfere with an extended window (approximately 30-50 min) after memory encoding. Behaviorally, post-encoding TMS to LOC selectively impaired associative memory retention compared to multiple control conditions. In the control TMS condition, we replicated prior reports of post-encoding reactivation and memory-related hippocampal-LOC interactions during periods of awake rest using fMRI. However, post-encoding LOC TMS reduced these processes, such that post-encoding reactivation in LOC and memory-related hippocampal-LOC functional connectivity were no longer present. By targeting and manipulating post-encoding neural processes, these findings highlight the direct contribution of awake time periods to episodic memory consolidation. This combined TMS-fMRI approach provides an opportunity for causal manipulations of human memory consolidation.

Keywords: awake rest; causal manipulations; fMRI-TMS; hippocampal-cortical interactions; hippocampus; lateral occipital cortex; memory consolidation; reactivation; resting state; transcranial magnetic stimulation.

Conflict of interest statement

Declaration of Interests The authors declare no competing interests.

Copyright © 2020 Elsevier Inc. All rights reserved.

Figures

Figure 1.. Experimental Design.
Figure 1.. Experimental Design.
(A) Participants completed a Baseline Session and Main TMS-fMRI Session. Theta-burst TMS was administered after the Immediate memory test. Participants returned approximately three and 24 hours after TMS for surprise Delayed memory tests. A unique subset of stimuli were tested in each memory test. Memory tests were performed outside of the MRI scanner. (B) TMS sites (LOC, blue; Control, black) are shown in MNI space.
Figure 2.. Memory retention (delayed divided by…
Figure 2.. Memory retention (delayed divided by immediate memory accuracy).
(A) Associative memory (associative hits minus associative false alarms) retention differed across groups, with reduced retention after LOC TMS. (B) No reliable influence of TMS was found on Item memory (item hits minus false alarms) retention. A significant TMS site by memory-type (associative versus item retention) interaction was found, indicated by the comparison across plots. Error bars show standard error of the mean. *P < .05, **P < .005. See also Figures S1, S2, Tables S1, S2.
Figure 3.. Post-encoding reactivation in LOC.
Figure 3.. Post-encoding reactivation in LOC.
(A) Analysis approach: object and face classifiers (yellow box) were trained in each participant (using data from functional localizer scans) and LOC patterns were extracted from volumes during rest and encoding were fed into the classifiers (depicted as vectors). Reactivation evidence was operationalized as an increase in the proportion of volumes classified as a face or object from Baseline to Post-Encoding Rest scans (increase in green squares). (B) As expected, a stimulus-evoked increase in classifier evidence (proportion of volumes classified as a face or object) was found during object-face encoding in both TMS groups (LOC, blue; Control, gray). Shaded region represents standard error of the mean across participants. (C) Reactivation evidence or change in the proportion of time-points classified as a face or object from Baseline to each Post-Encoding Rest scan. An increase was found in the Control TMS group (gray bars) but not the LOC TMS group, with a significant difference between TMS groups. *P < .05, **P < .005. See also Figures S3, S4.
Figure 4.. Post-encoding reactivation in the hippocampus.
Figure 4.. Post-encoding reactivation in the hippocampus.
(A) Analysis approach: denoised hippocampal encoding patterns were extracted (matrix on the left) and PCA was performed on each participant’s data, resulting in principal component (PC) encoding patterns (vectors on the right). Trial-triggered averages of the temporal projection of encoding PCs showing stimulus-evoked activity are displayed to the right of PC patterns. Shaded region depicts standard error of the mean across trials. (B) Reactivation evidence (change in the proportion of variance explained by each encoding PC from Baseline to Post-Encoding Rest) is shown for the top four PCs for each TMS group and scan (lightest bar = first Post-Encoding scan, second bar = second Post-Encoding scan, darkest bar = third Post-Encoding scan). Reactivation evidence is present in the Control TMS group, but not the LOC TMS group. (C) Correlation (Fisher Z-transformed) between the strength of each hippocampal encoding PC (eigenvalue) and its reactivation evidence (change in variance explained from Baseline to the average across Post-Encoding Rest scans) was assessed for each participant. A significant correlation is found in the Control TMS group, but not in the LOC TMS group. *P < .05
Figure 5.. Relationships between Post-Encoding measures and…
Figure 5.. Relationships between Post-Encoding measures and memory retention.
(A) Hippocampal ROI (right) defined from a subsequent associative memory contrast across all participants. Experience-dependent changes in hippocampal-LOC FC (from Baseline to the average across Post-Encoding Rest scans, Fisher Z-transformed) were related to same-day associative memory retention across participants in the Control TMS group (left), but not in the LOC TMS group (right). A significant difference was found between these correlations. Robust regression was used for all across-participant correlations. (B) The same as (A), using a hippocampal ROI defined from Control TMS participants. (C) The same as (A), using a hippocampal ROI defined from LOC TMS participants. (D) Summary score of reactivation measures was positively correlated with same-day associative memory retention in the Control TMS group, but not in the LOC TMS group. Summary reactivation score was derived from PCA on five measures: LOC reactivation (two measures), hippocampal reactivation (two measures), and changes in hippocampal-LOC FC. Vector below scatterplots depicts weighting of these measures to construct summary score (first PC). *P < .05
Figure 6.. Exploratory analyses of whole-brain changes…
Figure 6.. Exploratory analyses of whole-brain changes in hippocampal interactions related to next-day memory retention.
(A) Correlations between hippocampal (Figure 5A) FC changes across the whole brain and next-day associative memory retention (FWE-corrected using permutation testing). The only regions surviving FWE-correction are shown: retrosplenial cortex in the Control TMS group and right anterior temporal cortex in the LOC TMS group. Maps are shown on study-specific group-level template brain. (B) Patterns of correlations between hippocampal FC changes and next-day associative memory retention were repeatedly estimated for random subsets of each TMS group (left and middle) and a mixed set of participants across TMS groups (right) using subsampling. Plot shows similarity or correlation of these patterns across subsamples within each TMS group, within the mixed group, and the between-group similarity. Bars show mean Fisher Z-transformed correlation (similarity) and error bars show the standard deviation of Fisher Z-transformed correlations across iterations. *P < .001. See also Figure S5

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