High-definition transcranial direct current stimulation modulates performance and alpha/beta parieto-frontal connectivity serving fluid intelligence

Abstract

Fluid intelligence (Gƒ) includes logical reasoning abilities and is an essential component of normative cognition. Despite the broad consensus that parieto-prefrontal connectivity is critical for Gƒ (e.g. the parieto-frontal integration theory of intelligence, P-FIT), the dynamics of such functional connectivity during logical reasoning remains poorly understood. Further, given the known importance of these brain regions for Gƒ, numerous studies have targeted one or both of these areas with non-invasive stimulation with the goal of improving Gƒ, but to date there remains little consensus on the overall stimulation-related effects. To examine this, we applied high-definition direct current anodal stimulation to the left and right dorsolateral prefrontal cortex (DLPFC) of 24 healthy adults for 20 min in three separate sessions (sham, left, and right active). Following stimulation, participants completed a logical reasoning task during magnetoencephalography (MEG). Significant neural responses at the sensor-level were imaged using a beamformer, and peak task-induced activity was subjected to dynamic functional connectivity analyses to evaluate the impact of distinct stimulation montages on network activity. We found that participants responded faster following right DLPFC stimulation vs. sham. Moreover, our neural findings followed a similar trajectory of effects such that left parieto-frontal connectivity decreased following right and left DLPFC stimulation compared to sham, with connectivity following right stimulation being significantly correlated with the faster reaction times. Importantly, our findings are consistent with P-FIT, as well as the neural efficiency hypothesis (NEH) of intelligence. In sum, this study provides evidence for beneficial effects of right DLPFC stimulation on logical reasoning. KEY POINTS: Logical reasoning is an indispensable component of fluid intelligence and involves multispectral oscillatory activity in parietal and frontal regions. Parieto-frontal integration is well characterized in logical reasoning; however, its direct neural quantification and neuromodulation by brain stimulation remain poorly understood. High-definition transcranial direct current stimulation of dorsolateral prefrontal cortex (DLPFC) had modulatory effects on task performance and neural interactions serving logical reasoning, with right stimulation showing beneficial effects. Right DLPFC stimulation led to a decrease in the response time (i.e. better task performance) and left parieto-frontal connectivity with a marginal positive association between behavioural and neural metrics. Other modes of targeted stimulation of DLPFC (e.g. frequency-specific) can be employed in future studies.

Keywords: functional connectivity; logical reasoning; magnetoencephalography; phase coherence.

Figure 1.. Visit timeline, current density model and experimental paradigm.

Participants received 20 min of anodal and sham HD-tDCS over the left and right DLPFC. Stimulation montages were pseudorandomized across three visits, each separated by at least a week. Current distribution modeling using our HD-tDCS montage revealed focal stimulation of the left and right DLPFC (left). Following HD-tDCS participants completed a logical reasoning paradigm during MEG recording (right). The total visit time from the beginning of stimulation to the end of the MEG task was approximately 89 min.

Figure 2.. Behavioral performance on the logical reasoning task.

Stimulation montage (i.e., left and right active stimulation conditions and sham) is denoted at the bottom with the mean reaction time displayed on the y-axis. Each plot includes the individual data points, median (horizontal line), first and third quartile (box), and local minima and maxima (whiskers). Following right DLPFC stimulation, participants responded faster on the task compared to the sham condition. Error bars show the SEM. *p < 0.05.

Figure 3.. Neural responses to the logical reasoning task.

(Left): Grand-averaged time–frequency spectrograms of MEG sensors exhibiting one or more significant responses, with gamma activity at the top, alpha/beta middle, and theta at the bottom. In each spectrogram, frequency (Hz) is shown on the y-axis and time (ms) on the x-axis and. All signal power data are expressed as percent difference from baseline, with color legends shown to the right of the spectrograms. Dashed lines indicate the time–frequency windows that were subjected to beamforming. (Right): Grand-averaged beamformer images (pseudo-t) across all participants and HD-tDCS montages for each time–frequency component, with theta at the bottom, alpha/beta in the middle, and gamma at the top. Separate color scale bars are shown for each.

Figure 4.. Differential modulation of parieto-frontal connectivity by stimulation montages.

(Left) Phase locking value (PLV) is represented on the y-axes. Each plot includes the individual data points, median (horizontal line), first and third quartile (box), and local minima and maxima (whiskers). Weaker alpha/beta phase coherence was observed between left DLPFC and left parietal cortex following right and left stimulation relative to sham. Glass brains to the right show the pathway corresponding to the data on the left. Error bars reflect the SEM. *p < 0.05, **p < 0.01.