Cathodal Transcranial Direct Current Stimulation Over the Right Temporoparietal Junction Suppresses Its Functional Connectivity and Reduces Contralateral Spatial and Temporal Perception

Abstract

The temporoparietal junction plays key roles in vestibular function, motor-sensory ability, and attitude stability. Conventional approaches to studying the temporoparietal junction have drawbacks, and previous studies have focused on self-motion rather than on vestibular spatial perception. Using transcranial direct current stimulation, we explored the temporoparietal junction's effects on vestibular-guided orientation for self-motion and vestibular spatial perception. Twenty participants underwent position, motion, and time tasks, as well as functional magnetic resonance imaging scans. In the position task, cathodal transcranial direct current stimulation yielded a significantly lower response in the -6, -7, -8, -9, -10, -11, and -12 stimulus conditions for leftward rotations (P < 0.05). In the time task, the temporal bias for real transcranial direct current stimulation significantly differed from that for sham stimulation (P < 0.01). Functional magnetic resonance imaging showed that cathodal transcranial direct current stimulation suppressed functional connectivity between the temporoparietal junction, right insular cortex, and right supplementary motor area. Moreover, the change in connectivity between the right temporoparietal junction seed and the right insular cortex was positively correlated with temporal bias under stimulation. The above mentioned results show that cathodal transcranial direct current stimulation induces immediate and extended vestibular effects, which could suppress the functional connectivity of the temporoparietal junction and in turn reduce contralateral spatial and temporal perception. The consistent variation in temporal and spatial bias suggested that the temporoparietal junction may be the cortical temporal integrator for the internal model. Moreover, transcranial direct current stimulation could modulate the integration process and may thus have potential clinical applications in vestibular disorders caused by temporoparietal junction dysfunction.

Keywords: functional connectivity; internal model; self-motion; spatial perception; temporoparietal junction; transcranial direct current stimulation; vestibular nerve.

FIGURE 1

Transcranial direct current stimulation montage. Saline-soaked cathodal sponge electrodes (5 cm × 5 cm) were applied over the right P4 region, according to the International 10/20 electroencephalogram (EEG) system, and a larger anodal electrode (5 cm × 7 cm) was placed on the right shoulder deltoideus triangularis.

FIGURE 2

Task protocols. (A) Position task. Participants were instructed to sit on a rotational vestibular chair; the inner face of the chair enclosure was marked with 12 numbers. First, the participant faced number 12. Then, the participant was randomly rotated to the left or right. The participants were asked to estimate the number they were facing without providing them with any visual cues. The light was then switched on to reveal that number and the participants returned to the initial position. This process was repeated to involve all orientation directions, velocities, and angle amplitudes. (B) Motion task. Participants sat holding a control panel with two buttons. The chair rotated to the left or right randomly from rest with the acceleration increasing by 0.5 deg/s² every 3 s, and rotation-induced vestibular nystagmus was recorded. When the participants felt they were rotating, they pressed the corresponding button. (C) Time task. Each time task comprised two rotations with equal duration and opposite direction, in random order. After the two rotations, the participant was instructed to press the button corresponding to the rotation with the longer duration.

FIGURE 3

Experimental procedures. The whole experiment consisted of four sessions, i.e., a position task session, motion task session, time task session, and fMRI scan session. Each session was separated from the previous one by 3 days to eliminate aftereffects and included two tasks or scans, also separated by 3 days. Immediately before both tasks or scans, sham and real stimulation were delivered, in random order.

FIGURE 4

Position task and position bias results. (A) Position task results. The blue circle and inverted blue triangle represent the sham transcranial direct current stimulation (tDCS) condition for the leftward and rightward rotations, respectively. Correspondingly, for the real tDCS condition, a red square and red triangle represent the responses of the two stimulus directions. The linear regression lines for the real and sham tDCS condition are also denoted by blue and red lines, respectively. Asterisks are used to indicate significant differences between the real and sham tDCS conditions in the specific stimulus position. (B) Slopes of the regression lines for the four conditions. The slopes of the regression lines for the left real, left sham, right real, and right sham condition were calculated for each participant. The mean values and standard deviations of the four slopes are shown, and the vertical lines represent standard errors of the mean.

FIGURE 5

Motion task results. (A) Vestibular-ocular reflex (VOR) thresholds. There was no significance difference in performance under the real transcranial direct current stimulation (tDCS) and sham conditions for VOR thresholds in leftward or rightward rotation. (B) Motion perception thresholds. Compared with the perceptual thresholds under sham conditions, the motion perception thresholds under real tDCS showed no marked difference in either direction.

FIGURE 6

Time task results. (A) Temporal bias results. Temporal bias was defined as the proportion of participants indicating that the duration of the right rotation was longer when the rotations in opposite directions were in fact equal. Asterisks indicate significant differences between real and sham transcranial direct current stimulation (tDCS) conditions (P < 0.01). (B) Correlation between position bias and temporal bias. Correlation between position bias in position task performance and temporal bias in time task performance across all participants under the real tDCS condition. The coefficient of determination denoted R² in the figure is the proportion of temporal bias that can be predicted from position bias.

FIGURE 7

Correlation results. FC change between the right TPJ and the right IC was correlated with temporal bias across all subjects under the real tDCS condition. The coefficient of determination, denoted R² in the figure, is the proportion of temporal bias that can be predicted from FC variation. FC, functional connectivity; rTPJ, right temporoparietal junction; rIC, right insular cortex.