Stimulating the hippocampal posterior-medial network enhances task-dependent connectivity and memory

  1. Kristen N Warren  Is a corresponding author
  2. Molly S Hermiller
  3. Aneesha S Nilakantan
  4. Joel L Voss
  1. Feinberg School of Medicine, Northwestern University, United States
5 figures and 5 additional files

Figures

Experiment Design.

(A) Subjects received five consecutive daily sessions of high-frequency (20 Hz) repetitive TMS delivered to a subject-specific parietal cortex location of the PMN selected based on high …

https://doi.org/10.7554/eLife.49458.002
Figure 2 with 1 supplement
Greater memory task-dependent connectivity increases due to PMN-targeted versus PFC-targeted control stimulation for the PMN.

(A) Stimulation effect on mean connectivity (all regions to all other regions) during memory retrieval relative to rest for the PMN (left) and the ATN (right). Error bars indicate subject-level …

https://doi.org/10.7554/eLife.49458.003
Figure 2—source data 1

PMN/ATN network-based analysis.

Subject: 1–16 = PMN targeted group, 17–32 = PFC targeted group. State: Autobiographical memory task (Retrieval) or resting-state (Rest). Condition: Full stimulation (Stim) or sham stimulation (Sham). Target: PMN-targeted (Par) or PFC-targeted (Ant). Order: Full stimulation first (1) or sham stimulation first (2). Connectivity: Average activity correlation between network regions for that scan. tSNR: Average whole-brain temporal signal to noise ratio for that scan. Network: Posterior-medial (PM) or anterior-temporal (AT).

https://doi.org/10.7554/eLife.49458.005
Figure 2—figure supplement 1
Network regions of interest.

Posterior medial network (PMN) and anterior temporal network (ATN) regions of interest (Ranganath and Ritchey, 2012): PMN (red), ATN (green).

https://doi.org/10.7554/eLife.49458.004
Figure 3 with 3 supplements
Greater memory task-dependent connectivity increases due to PMN-targeted versus prefrontal-control stimulation.

(A) Regions showing a significant interaction between condition, task, and group, with red coloration indicating stimulation increased connectivity more during retrieval than during rest in the …

https://doi.org/10.7554/eLife.49458.006
Figure 3—source data 1

Whole-brain analysis, full model.

Subject: 1–16 = PMN targeted group, 17–32 = PFC targeted group. State: Autobiographical memory task (Retrieval) or resting-state (Rest). Condition: Full stimulation (Stim) or sham stimulation (Sham). Target: PMN-targeted (Parietal) or PFC-targeted (Prefrontal). Cluster: Significant cluster identified via whole-brain analysis. Memory: Percent of memory trials with correct context recollection. Connectivity: Average global correlation within the cluster for that scan. tSNR: Average whole-brain temporal signal to noise ratio for that scan.

https://doi.org/10.7554/eLife.49458.010
Figure 3—figure supplement 1
Selective effects of stimulation on memory-specific connectivity.

All regions showing a significant three-way interaction between condition, demand, and group. Red coloration indicates supra-threshold voxels with positive differences (retrieval stimulation effect >…

https://doi.org/10.7554/eLife.49458.007
Figure 3—figure supplement 2
Increased fMRI connectivity during memory retrieval.

Regions showing a significant main effect of demand independent from stimulation condition or stimulation group. All showed greater connectivity during the retrieval demand relative to rest. Left = L…

https://doi.org/10.7554/eLife.49458.008
Figure 3—figure supplement 3
Common effects of stimulation across sites.

Regions showing a significant main effect of stimulation condition, regardless of demand or stimulation site. Left = Left. Red coloration indicates supra-threshold voxels with positive differences …

https://doi.org/10.7554/eLife.49458.009
Figure 4 with 2 supplements
Selective effects of PMN-targeted stimulation on memory-related connectivity.

(A) Regions showing significant interaction between stimulation condition and cognitive task following PMN-targeted stimulation, with red coloration indicating stimulation increased connectivity …

https://doi.org/10.7554/eLife.49458.011
Figure 4—source data 1

Whole-brain analysis, PMN-targeted group.

Subject: 1–16 = PMN targeted group, 17–32 = PFC targeted group. State: Autobiographical memory task (Retrieval) or resting-state (Rest). Condition: Full stimulation (Stim) or sham stimulation (Sham). Cluster: Significant cluster identified via whole-brain analysis. Memory: Percent of memory trials with correct context recollection. Connectivity: Average global correlation within the cluster for that scan. tSNR: Average whole-brain temporal signal to noise ratio for that scan.

https://doi.org/10.7554/eLife.49458.014
Figure 4—source data 2

Whole-brain analysis, PFC-targeted group.

Subject: 1-16=PMN-targeted group, 17-32=PFC-targeted group. State: Autobiographical memory task (Retrieval) or resting-state (Rest). Condition: Full stimulation (Stim) or sham stimulation (Sham). Cluster: Significant cluster identified via whole-brain analysis. Memory: Percent of memory trials with correct context recollection. Connectivity: Average global correlation within the cluster for that scan. tSNR: Average whole-brain temporal signal to noise ratio for that scan.

https://doi.org/10.7554/eLife.49458.015
Figure 4—figure supplement 1
Selective effects of stimulation on memory-specific connectivity.

All regions showing a significant interaction between condition and demand following PMN-targeted stimulation. Red coloration indicates supra-threshold voxels with positive differences (retrieval …

https://doi.org/10.7554/eLife.49458.012
Figure 4—figure supplement 2
Selective effects of stimulation on memory-specific connectivity.

All regions showing a significant interaction between condition and demand following PFC-targeted stimulation. Red coloration indicates supra-threshold voxels with positive differences (retrieval …

https://doi.org/10.7554/eLife.49458.013
Increased memory-dependent connectivity predicts episodic memory improvement.

(A) Episodic memory task design. Participants studied trial-unique objects paired with either scene or location contexts. After a delay, we assessed object recognition memory and contextual …

https://doi.org/10.7554/eLife.49458.016

Additional files

Supplementary file 1

Effect tables for the linear mixed models used to identify the demand-specific effects for PMN-targeted versus PFC-targeted control stimulation (Figure 1).

https://doi.org/10.7554/eLife.49458.017
Supplementary file 2

Expanded names for PMN and ATN region abbreviations used in Figure 2.

Region labels from Eickhoff-Zilles macro labels from N27 in MNI space. Note that ‘calcarine gyrus’ refers to the area surrounding the calcarine sulcus, including the precuneus and lingual gyrus.

https://doi.org/10.7554/eLife.49458.018
Supplementary file 3

18 supra-threshold regions identified via significant interaction between stimulation condition and demand (bolded), followed by their drivers—regions showing significant interaction between stimulation condition and demand in their seed-based connectivity to one of the 18 supra-threshold regions.

Region labels from Eickhoff-Zilles macro labels from N27 in MNI space. Note that ‘calcarine gyrus’ refers to the area surrounding the calcarine sulcus, including the precuneus and lingual gyrus.

https://doi.org/10.7554/eLife.49458.019
Supplementary file 4

15 supra-threshold regions identified via significant interaction between stimulation condition and demand (bolded), followed by their drivers—regions showing significant interaction between stimulation condition and demand in their seed-based connectivity to one of the 15 supra-threshold regions.

Region labels from Eickhoff-Zilles macro labels from N27 in MNI space. Note that ‘calcarine gyrus’ refers to the area surrounding the calcarine sulcus, including the precuneus and lingual gyrus.

https://doi.org/10.7554/eLife.49458.020
Transparent reporting form
https://doi.org/10.7554/eLife.49458.021

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