Multiple interacting brain areas underlie successful spatiotemporal memory retrieval in humans.
- Authors
- Schedlbauer, Amber M; Copara, Milagros S; Watrous, Andrew J; Ekstrom, Arne D
- Year
- 2014
- Journal
- Scientific reports
- PMID
- 25234342
- DOI
- 10.1038/srep06431
- PMCID
- PMC4168271
Emerging evidence suggests that our memories for recent events depend on a dynamic interplay between multiple cortical brain regions, although previous research has also emphasized a primary role for the hippocampus in episodic memory. One challenge in determining the relative importance of interactions between multiple brain regions versus a specific brain region is a lack of analytic approaches to address this issue. Participants underwent neuroimaging while retrieving the spatial and temporal details of a recently experienced virtual reality environment; we then employed graph theory to analyze functional connectivity patterns across multiple lobes. Dense, large-scale increases in connectivity during successful memory retrieval typified network topology, with individual participant performance correlating positively with overall network density. Within this dense network, the hippocampus, prefrontal cortex, precuneus, and visual cortex served as "hubs" of high connectivity. Spatial and temporal retrieval were characterized by distinct but overlapping "subnetworks" with higher connectivity within posterior and anterior brain areas, respectively. Together, these findings provide new insight into the neural basis of episodic memory, suggesting that the interactions of multiple hubs characterize successful memory retrieval. Furthermore, distinct subnetworks represent components of spatial versus temporal retrieval, with the hippocampus acting as a hub integrating information between these two subnetworks.
Description of Experimental Design.(A) Participants (n = 16) navigated a virtual city where they picked up a passenger (depicted in the left panel) and delivered the person to a series of stores; they encoded the spatial layout of the city and the temporal order of deliveries. The middle panel provides an example of a store the participant visited. The right panel shows an aerial view of the virtual environment with the stores distributed unevenly around a circle. (B) After encoding, participants underwent functional imaging while performing the spatiotemporal retrieval task shown here. Participants were first presented with a single reference store and asked to indicate whether they saw this store before. After responding, they were subsequently presented with the spatiotemporal contextual retrieval question. Participants were shown two additional store pictures and asked to make a distance judgment regarding the spatial or temporal proximity to the reference store.
LLM interpretation
This figure is a schematic diagram illustrating an experimental design for a spatiotemporal memory study. Panel A shows the encoding phase, featuring a virtual city environment with a passenger, an example store, and an aerial map of store distribution. Panel B depicts the retrieval task timeline, where participants perform an item recognition question followed by either a temporal or spatial context proximity judgment between stores.
Increases in Network Connectivity during Successful Retrieval of Spatiotemporal Details.(A and B) Each ROI (colored circle) is plotted with significant connections (pink lines) between the nodes; network during correct context responses shown in A and during incorrect context responses in B. Both size and color indicate node degree; a larger radius and warmer colors represent a higher node degree, while a smaller radius and cooler colors represent a lower node degree. The ROIs are spatially distributed according to their x and y coordinates in standardized brain space but have been collapsed in the z coordinate direction. The right panel displays node hierarchy where anterior nodes (red) and posterior nodes (blue) are plotted in ascending order of node degree, with the highest node degree level at the top; nodes belonging to the same horizontal level have the same node degree. The abbreviations for the ROIs are as follows: SFG (Superior Frontal Gyrus); MFG (Middle Frontal Gyrus); IFOr (Inferior Frontal Gyrus, Orbitalis); IFTr (Inferior Frontal Gyrus, Triangularis); IFOp (Inferior Frontal Gyrus, Opercularis); PrCG (Precentral Gyrus); aHPC (Anterior Hippocampus); pHPC (Posterior Hippocampus); pPHG (Posterior Parahippocampal Gyrus); IPL (Inferior Parietal Lobule); SPL (Superior Parietal Lobule); PCN (Precuneus); Calc (Calcarine sulcus). (C) Left: The adjacency matrix (right of diagonal: correct – incorrect, left of diagonal: incorrect – correct) depicts the data to optimize viewing the intra-lobular connections. The colored boxes indicate intra-lobular connections in the frontal lobe and temporal lobe (blue, green, respectively). For successful retrieval, numerous connections exist within the MTL but many are found throughout the neocortex, compared to low levels of functional connectivity throughout the brain during unsuccessful retrieval. Right: Comparison of the total number of edges (significant functional connections) between conditions, with the correct – incorrect network containing significantly more edges. *p < 0.0001. (D) Bar graphs showing betweenness centrality for each ROI (collapsed across hemispheres). Asterisks indicate pcorrected < 0.05 significant differences using a chi-squared test on node connectivity between conditions (i.e. correct – incorrect and incorrect – correct).
LLM interpretation
This figure consists of network diagrams, an adjacency matrix, and bar graphs comparing brain connectivity during correct versus incorrect spatiotemporal retrieval. Panels A and B show that correct responses are associated with a significantly denser network of functional connections (pink lines) and higher node degrees (larger, warmer-colored circles) across various ROIs compared to incorrect responses. Panel C includes an adjacency matrix and a bar chart showing a significantly higher total edge count for the "Correct-Incorrect" condition (*p < 0.0001). Panel D uses bar graphs to show significantly higher betweenness centrality for the anterior hippocampus, posterior hippocampus, calcarine sulcus, and inferior frontal gyrus (orbitalis) during correct versus incorrect retrieval (pcorrected < 0.05).
Individual Patterns of Network Connectivity Predict Memory Performance.The scatter plot shows a significant linear relationship between total connectivity and individual participant behavioral performance (p < 0.05). To determine which ROIs were driving this correlation, each node's contribution to overall network density was regressed against individual performance using a multiple linear regression. The initial model in the stepwise regression consisted of the nodes labeled with asterisks, and a final more parsimonious model resulted in the nodes highlighted in red (MFG, HPC, PCN, and IFG). The beta coefficients from the linear regression and stepwise regression are presented on a line next to the independent variables. For example, the network density resulted in a coefficient of 0.20 for the linear regression.
LLM interpretation
This figure consists of a scatter plot and a corresponding list of brain regions (ROIs) used in regression analyses. The scatter plot shows a positive linear relationship between "Percent Connectivity" (x-axis) and "Percent Correct" behavioral performance (y-axis). To the left, a list of ROIs includes beta coefficients and markers (asterisks and red text) identifying specific nodes, such as MFG_L and PCN_R, that contributed to the predictive models.
Differential Spatial and Temporal Network Connectivity.Panels A, B, and C are arranged similarly to Fig. 2 but show the spatial – temporal and temporal – spatial retrieval networks. (A, B) Connectivity plots, using standardized brain space (left plot) or hierarchical arrangement based on node degree (right plot), for spatial and temporal networks. (C) Left: Adjacency matrix where right of diagonal are significant nodes during spatial retrieval and left of diagonal are significant nodes during temporal order retrieval. Middle: Bar graphs comparing the number of edges for anterior versus posterior brain regions for the two conditions. Anterior brain regions showed higher connectivity during temporal retrieval while posterior brain regions showed higher connectivity during spatial retrieval. Right: Bar graph showing no difference in the total number of edges present in each network. (D and E) The MTL (aHPC, pHPC, pPHG) regions displayed high betweenness centrality values but no differences between condition. The SPL and calcarine ROIs showed significantly greater betweenness centrality for the spatial – temporal network, while IFG and MFG showed greater betweenness centrality in the temporal – spatial network. *pcorrected < 0.05.
LLM interpretation
This figure presents network connectivity analysis comparing spatial-temporal and temporal-spatial retrieval. Panels A and B show connectivity plots in brain space and by node degree, while Panel C includes an adjacency matrix and bar graphs showing higher edge counts in posterior regions for spatial-temporal and anterior regions for temporal-spatial networks, with no difference in total edge counts. Panels D and E use bar charts to show betweenness centrality, indicating significantly higher values for the SPL and calcarine ROIs in the spatial-temporal network and for the IFG and MFG in the temporal-spatial network (*p < 0.05).
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