Opposite pattern of transcranial direct current stimulation effects in middle-aged and older adults: Behavioral and neurophysiological evidence

Abstract

Introduction: Episodic memory (EM) exhibits an age-related decline, with overall increased impairment after the age of 65. The application of transcranial direct current stimulation (tDCS) to ameliorate cognitive decline in ageing has been extensively investigated, but its efficacy has been reported with mixed results. In this study, we aimed to assess whether age contributes to interindividual variability in tDCS efficacy.

Methods: Thirty-eight healthy adults between 50 and 81 years old received anodal tDCS over the left prefrontal cortex during images encoding and then performed an EM recognition task while event-related potentials (ERPs) were recorded.

Results: Our results showed an opposite pattern of effect between middle-aged (50-64 years) and older (65-81 years) adults. Specifically, performance in the recognition task after tDCS was enhanced in older adults and was worsened in middle-aged adults. Moreover, ERPs acquired during the recognition task showed that two EM components related to familiarity and post-retrieval monitoring, i.e., Early Frontal and Late Frontal Old-New effects, respectively, were significantly reduced in middle-aged adults after anodal tDCS.

Discussion: These results support an age-dependent effect of prefrontal tDCS on EM processes and its underlying electrophysiological substrate, with opposing modulatory trajectories along the aging lifespan.

Keywords: aging; dorsolateral prefrontal cortex; episodic memory; event-related potentials; transcranial direct current stimulation.

Figure 1

Experimental procedures. (A) Anodal or sham tDCS was administered during the encoding phase of the episodic memory (EM) task. After a delay of 15 min, participants performed the recognition phase of the EM task during which EEG data were collected. (B) Trial procedure of the encoding phase of the EM task. In each trial, an image to be remembered is presented followed by two different semantic choices. The original task was performed in Italian. (C) Trial procedure of the recognition phase of the EM task. Participants are required to decide whether each image was old (already seen in the encoding phase) or new (not seen). The original task was performed in Italian.

Figure 2

Behavioral results. (A) Boxplots depicting the hit rate obtained during the recognition EM task in middle-aged (left) and older adults (right) after anodal and sham tDCS sessions; (B) Boxplots depicting the correct rejection rate obtained during the recognition EM task in middle-aged (left) and older adults (right) after anodal and sham tDCS sessions. For each boxplot, the rectangles represent the interquartile range from the 25th percentile (quartile 1, Q1; lower black bar) to the 75th percentile (quartile 3, Q3; upper black bar), with the horizontal bar inside representing the 50th percentile (quartile 2, Q2, median), and the horizontal bars depicting the largest (upper bar) and smallest (lower bar) values within 1.5 times the interquartile range above the 75th percentile and below the 25th percentile, respectively. * indicates a significant difference.

Figure 3

Grand-average ERP waveforms elicited by the old stimuli (hit) in the Anodal (red line) and Sham (black line) sessions for the middle-aged (upper panel) and older (lower panel) adults at the F3, Fz, F4, P3, Pz, and P4 electrodes. Vertical lines highlight the time window considered for the different ERP components. Black vertical lines with an asterisk indicate statistically significant differences between the anodal and sham conditions. EF, Early Frontal Old-New effect; LF, Late Frontal Old-New effect; P, Parietal Old-New effect. * indicates a significant difference.