tDCS-induced episodic memory enhancement and its association with functional network coupling in older adults

Abstract

Transcranial direct current stimulation (tDCS) augments training-induced cognitive gains, an issue of particular relevance in the aging population. However, negative outcomes have been reported as well, and few studies so far have evaluated the impact of tDCS on episodic memory formation in elderly cohorts. The heterogeneity of previous findings highlights the importance of elucidating neuronal underpinnings of tDCS-induced modulations, and of determining individual predictors of a positive response. In the present study, we aimed to modulate episodic memory formation in 34 older adults with anodal tDCS (1 mA, 20 min) over left temporoparietal cortex. Participants were asked to learn novel associations between pictures and pseudowords, and episodic memory performance was subsequently assessed during immediate retrieval. Prior to experimental sessions, participants underwent resting-state functional magnetic resonance imaging. tDCS led to better retrieval performance and augmented learning curves. Hippocampo-temporoparietal functional connectivity was positively related to initial memory performance, and was positively associated with the magnitude of individual tDCS-induced enhancement. In sum, we provide evidence for brain stimulation-induced plasticity of episodic memory processes in older adults, corroborating and extending previous findings. Our results demonstrate that intrinsic network coupling may determine individual responsiveness to brain stimulation, and thus help to further explain variability of tDCS responsiveness in older adults.

Figure 1

Accuracy in the episodic memory task. (a) Percentage of correct responses in the five learning blocks (L1-L5) and the two retrieval blocks (R1, R2). Means and (one side of) two-sided 95%-CIs are shown. (b) Boxplots and individual data points for main outcome variable R1, created with BoxPlotR (http://boxplot.tyerslab.com/). *p < 0.05.

Figure 2

Reaction time in the memory task. Mean reaction time (in ms) during the five learning blocks (L1-L5) and the two retrieval blocks (R1, R2). Means and (one side of) two-sided 95%-CIs are shown.

Figure 3

Scatterplot of functional connectivity and memory performance. Functional connectivity between the left hippocampus and left temporoparietal cortex correlated with task performance at baseline (R, retrieval). The significant cluster that emerged from whole-brain seed-to-voxel analyses had peak coordinates of x = −40, y = −52, z = 18, T = 4.45, cluster size k = 232 mm², cluster-p-FDR = 0.040. The scatterplot illustrates the relationship (baseline performance is plotted over individual functional connectivity that was extracted from the significant cluster).

Figure 4

Partial regression plot (residuals) for the association between functional connectivity and individual responsiveness to tDCS (β = 0.31, p = 0.036). Linear regression included the difference in performance in anodal and sham stimulation condition as dependent variable and functional connectivity between hippocampus and angular gyrus as independent variable, adjusted for performance in sham stimulation condition, session order and age.