Transcranial magnetic stimulation to the angular gyrus modulates the temporal dynamics of the hippocampus and entorhinal cortex

Abstract

Transcranial magnetic stimulation (TMS) delivered to the angular gyrus (AG) affects hippocampal function and associated behaviors (Thakral PP, Madore KP, Kalinowski SE, Schacter DL. Modulation of hippocampal brain networks produces changes in episodic simulation and divergent thinking. 2020a. Proc Natl Acad Sci U S A. 117:12729–12740). Here, we examine if functional magnetic resonance imaging (fMRI)-guided TMS disrupts the gradient organization of temporal signal properties, known as the temporal organization, in the hippocampus (HPC) and entorhinal cortex (ERC). For each of 2 TMS sessions, TMS was applied to either a control site (vertex) or to a left AG target region (N = 18; 14 females). Behavioral measures were then administered, and resting-state scans were acquired. Temporal dynamics were measured by tracking change in the fMRI signal (i) “within” single voxels over time, termed single-voxel autocorrelation and (ii) “between” different voxels over time, termed intervoxel similarity. TMS reduced AG connectivity with the hippocampal target and induced more rapid shifting of activity in single voxels between successive time points, lowering the single-voxel autocorrelation, within the left anteromedial HPC and posteromedial ERC. Intervoxel similarity was only marginally affected by TMS. Our findings suggest that hippocampal-targeted TMS disrupts the functional properties of the target site along the anterior/posterior axis. Further studies should examine the consequences of altering the temporal dynamics of these medial temporal areas to the successful processing of episodic information under task demand.

Single voxel autocorrelation reflects hippocampal function in temporal lobe epilepsy

“…Consistent with findings from our previous work (Bouffard, Golestani et al, 2023; Coughlan et al, 2023), we found that data-driven clustering of the signal voxel autocorrelation in TLE patients and controls resulted in three distinct clusters. Our clustering approach does not use a predefined number of clusters, and visual examinations of the cluster maps revealed that there were no differences in number of clusters between patients and controls, nor was there a difference between healthy and epileptogenic hemispheres.…”

“…In this study we examined single voxel autocorrelation and clusters of single voxel autocorrelation in patients with unilateral left and right TLE to investigate how hippocampal damage present in TLE affects the temporal signal dynamics in the hippocampus. Here, we replicated our past work (Bouffard, Golestani et al, 2023; Coughlan et al, 2023) and found that all groups demonstrated a pattern of high autocorrelation values clustered in the anterior-medial hippocampus and low autocorrelation values clustered in the posterior-lateral. There were two major findings in the TLE groups, both selective to the anterior-medial cluster.…”

“…In the healthy hippocampus, single voxel autocorrelation follows a gradient from high-to-low along the anterior-posterior and medial-lateral axes Coughlan et al, 2023;Raut et al, 2020). These continuous gradients can be segmented into distinct clusters based on the autocorrelation of individual voxels and result in three segments: an anterior-medial cluster of high autocorrelation voxels, an intermediate cluster, and a posterior-lateral cluster of low autocorrelation voxels (Bouffard, Golestani et al, 2023;Coughlan et al, 2023). Our past work used a datadriven clustering approach and found that changes in single voxel autocorrelation, specifically in the anterior-medial cluster, were related to changes in navigation difficulty.…”

“…Recently our lab has developed an fMRI analytic technique that allows us to measure dynamics in the BOLD signal over time in single voxels. Single voxel autocorrelation is the lagged autocorrelation of individual voxels, a measure of how similar a voxel’s activity is to itself over time (Bouffard, Golestani et al, 2023; Coughlan et al, 2023). In healthy populations, single voxel autocorrelation is thought to reflect underlying neuronal dynamics, where high autocorrelation indicates slow fluctuations in neural activity and low autocorrelation indicates rapid fluctuations in neural activity.…”

Causal role of the angular gyrus in insight-driven memory reconfiguration

“…One promising candidate that may contribute to insight-driven memory reconfiguration is the angular gyrus. The angular gyrus has extensive structural and functional connections to many other brain regions (Petit et al, 2023), including the hippocampus (Coughlan et al, 2023; Uddin et al, 2010). Accordingly, previous studies have shown that stimulation of the angular gyrus resulted in altered hippocampal activity (Thakral et al, 2020; Wang et al, 2014).…”