The entorhinal-DG/CA3 pathway in the medial temporal lobe retains visual working memory of a simple surface feature

  1. Weizhen Xie  Is a corresponding author
  2. Marcus Cappiello
  3. Michael A Yassa
  4. Edward Ester
  5. Kareem A Zaghloul
  6. Weiwei Zhang  Is a corresponding author
  1. Surgical Neurology Branch, National Institute of Neurological Disorders and Stroke, United States
  2. Department of Psychology, University of California, Riverside, United States
  3. Department of Psychology, University of Maryland, United States
  4. Center for the Neurobiology of Learning and Memory, School of Biological Sciences, University of California, Irvine, United States
  5. Department of Psychology, University of Nevada, United States
5 figures and 2 additional files

Figures

Figure 1 with 1 supplement
Visual WM task and participants’ task performance.

(A) During fMRI scanning, participants were directed to retain the orientation of a cued grating stimulus from two sequentially presented grating stimuli (item 1 vs 2). After a short retention …

Figure 1—figure supplement 1
Behavioral task design and data in the current study across participants.

(A) The cued and uncued items were randomly chosen from the feature space with a constraint that the chosen items on each trial were >20 degrees apart. As a result, the absolute angular distance …

Figure 2 with 2 supplements
The MTL retains item-specific WM information revealed by stimulus-based representational similarity analysis.

(A) MTL ROIs are parcellated based on previous research (Montchal et al., 2019; Reagh et al., 2017). The amygdala is chosen as an adjacent control region. (B) For each ROI, we examined the extent to …

Figure 2—figure supplement 1
Voxel responses in an example ROI (aLEC) for different remembered stimuli from one example subject.

We sorted these voxels based on the magnitude of BOLD response to different orientation stimuli. This analysis only serves illustrative purposes. The reliability of these multi-voxel patterns can be …

Figure 2—figure supplement 2
Across-region neural similarity analysis using the combined aLEC-DG/CA3 as an MTL seed region, the superior parietal lobule (SPL) ROI as a benchmark region, and the amygdala as a control region.

(A) Trial-by-trial neural similarity pattern at each TR can be calculated to reflect the representational pattern within a given ROI. The similarity of these neural representational patterns between …

Figure 3 with 6 supplements
The MTL retains item-specific WM information revealed by Inverted Encoding Modeling (IEM).

(A) The IEM method assumes that each voxel response in the multi-voxel pattern reflects a weighted summation of different ideal stimulus information channels (C). The weights (W) of these …

Figure 3—figure supplement 1
Example channel responses before and after shifting to the cued orientation for aLEC (A) and the amygdala (B).

Based on a level-one-block-out cross-validation approach, we reconstructed the assumed neural channel response model reported in Figure 3B. Before shifting individual channel responses to the cued …

Figure 3—figure supplement 2
Distributed brain regions retain information about the cued item during WM.

A roving searchlight procedure was combined with the inverted encoding modeling (IEM) to identify brain regions containing item-specific WM content for the cued item (Ester et al., 2015). This …

Figure 3—figure supplement 3
Stimulus-based representational similarity analysis (RSA) and inverted encoding model (IEM) reveal shared item-related variance in the observed neural data.

In both the aLEC and DG/CA3 ROIs, the association between the patterns of the task stimuli and neural responses (RSA) was highly correlated with IEM decoding performance across participants (aLEC: r=…

Figure 3—figure supplement 4
Analyses based on the whole hippocampus, as compared with a benchmark sphere ROI in the posterior parietal cortex (e.g., superior parietal lobule, SPL) and the hippocampal DG/CA3 subfield.

(A) As the posterior parietal cortex has consistently implicated to support visual WM representations (Bettencourt and Xu, 2016; Ester et al., 2015), we identified the local peaks of the bilateral …

Figure 3—figure supplement 5
Time-varying IEM analysis shows that mid-delay period activity in aLEC-DG/CA3 contains item-specific information that could not be attributed to perceptual processing alone.

(A) We performed a time-varying IEM analysis for the combined aLEC-DG/CA3 ROI based on raw BOLD signals weighted by adjacent TRs, with a moving window in steps of 1 TR. This analysis was done …

Figure 3—figure supplement 6
Modeling results of the hippocampal subfields based on FreeSurfer labels.

In addition to the in-house subfield parcellation, we verified our findings based on the hippocampal subfield labels extracted from each participant’s MRI scan using FreeSurfer 6.0 (https://surfer.nm…

The quality of WM information retained in the aLEC-DG/CA3 pathway is associated with later recall fidelity.

(A) Participants’ performance in the visual WM task is high with most of absolute recall errors falling within the 3 SD of the aggregated recall error distribution. As the angular resolution of the …

Author response image 1
IEM reconstruction based on precise and imprecise recall trials separately for aLEC (top row) and DG/CA3 (bottom row).

Additional files

Supplementary file 1

Supporting data tables.

(A) Tests of statistical significance in the neural similarity across trials captured by the similarity of the cued item. (B) Tests of statistical significance in IEM results for the cued item. (C) The number of voxels included for each bilateral ROI in each subject.

https://cdn.elifesciences.org/articles/83365/elife-83365-supp1-v2.docx
MDAR checklist
https://cdn.elifesciences.org/articles/83365/elife-83365-mdarchecklist1-v2.pdf

Download links