Long-Lasting Enhancement of Visual Perception with Repetitive Noninvasive Transcranial Direct Current Stimulation

Abstract

Understanding processes performed by an intact visual cortex as the basis for developing methods that enhance or restore visual perception is of great interest to both researchers and medical practitioners. Here, we explore whether contrast sensitivity, a main function of the primary visual cortex (V1), can be improved in healthy subjects by repetitive, noninvasive anodal transcranial direct current stimulation (tDCS). Contrast perception was measured via threshold perimetry directly before and after intervention (tDCS or sham stimulation) on each day over 5 consecutive days (24 subjects, double-blind study). tDCS improved contrast sensitivity from the second day onwards, with significant effects lasting 24 h. After the last stimulation on day 5, the anodal group showed a significantly greater improvement in contrast perception than the sham group (23 vs. 5%). We found significant long-term effects in only the central 2-4° of the visual field 4 weeks after the last stimulation. We suspect a combination of two factors contributes to these lasting effects. First, the V1 area that represents the central retina was located closer to the polarization electrode, resulting in higher current density. Second, the central visual field is represented by a larger cortical area relative to the peripheral visual field (cortical magnification). This is the first study showing that tDCS over V1 enhances contrast perception in healthy subjects for several weeks. This study contributes to the investigation of the causal relationship between the external modulation of neuronal membrane potential and behavior (in our case, visual perception). Because the vast majority of human studies only show temporary effects after single tDCS sessions targeting the visual system, our study underpins the potential for lasting effects of repetitive tDCS-induced modulation of neuronal excitability.

Keywords: contrast sensitivity; noninvasive brain stimulation; plasticity; primary visual cortex; transcranial direct current stimulation; visual perceptual learning.

Figure 1

Site of stimulation and experimental design. (A, B) Determination of the position of the polarization electrode: An anatomical magnetic resonance image (MRI) was aligned to the surface using the Nexstim system for MRI-guided brain stimulation. (A) The target region for anodal stimulation was the left-hemispherical striate area (V1, blue arrow). (B) The polarization electrode (E) was placed over the target region and between two anatomical structures (see yellow depth markers): laterally, the inter-hemispherical fissure, and caudally, the boundary between the occipital cortex and the cerebellum (cerebellar tentorium). (C) Experimental design: Pre-test before the experiment (0). Stimulation phase: Over five consecutive days (days 1–5), subjects received brain stimulation (S) via anodal transcranial direct current stimulation (tDCS) or sham stimulation and participated in computerized threshold perimetry tests before and after stimulation. Follow-up measurements: Computerized threshold perimetry measurements were taken 2 and 4 weeks (days 19 and 33, respectively) after the final stimulation. N = 24 healthy subjects (12 sham group, 12 anodal group).

Figure 2

Effects of anodal and sham tDCS on 5 consecutive days. Contrast perception improved across both groups and was not significant in the control group (rectangle line; within-subject effect time: F = 2.782, P = 0.066). Effects were greater for the anodal group (diamond line; interaction of within-subject effect intervention and between-subject effect stimulation: F = 6.456, P = 0.019), with a significantly greater average increase in performance over time (days 1–5, interaction of within-subject effect time and between-subject effect stimulation: F = 2.237, P = 0.037). ^*P < 0.05, error bars show standard error of the mean (SEM). N = 24 healthy subjects (12 sham group, 12 anodal group).

Figure 3

Effects of anodal and sham tDCS at 5 consecutive days after stimulation. Compared to the control group (rectangle line), effects of stimulation were greater for the anodal group at days 2–5 compared to baseline (ANOVA days 1–33, days 19 and 33 are not shown) diamond line; contrasts of within-subject effect time and between-subject effect stimulation: day 2: F = 4.659, P = 0.042; day 3: F = 9.293, P = 0.006; day 4: F = 6.972, P = 0.015; day 5: F = 6.332, P = 0.020). ^*P < 0.05, error bars show standard error of the mean (SEM). N = 24 healthy subjects (12 sham group, 12 anodal group).

Figure 4

Immediate, overnight, and total effects. The average difference between performance immediately after stimulation and right before simulation (immediate, dnpost compared to dnpre, left bars), were greater in the anodal group (gray bars; P = 0.015). In contrast, effects between days (overnight, dnpre compared to d(n−1)post, central bars) were greater in the sham group (white bars; P = 0.034). Total enhancement of contrast perception (total, right bars) at day 5 (post), compared to baseline was superior on average (P = 0.047) in the anodal group than in sham. ^*P < 0.05; error bars show SEM. N = 24 healthy subjects (12 sham group, 12 anodal group).

Figure 5

tDCS effects at follow-up dates. The enhancement in contrast perception at the follow-up measurements compared to baseline was not significant regarding the whole visual field (degrees 2–10) across all subjects (within-subject effect time: F = 1.798; P = 0.156) or between groups (between-subject effect stimulation: F = 1.073, P = 0.312). Over the study period and compared to the sham group (rectangle line), the anodal group (diamond line) showed no significant improvement of contrast sensitivity (interaction of within-subject effect time and between-subject effect stimulation: F = 2.390; P = 0.076). Compared to sham, tDCS-induced significant enhancement of contrast sensitivity (day 5 post) did not lead to a sharper decline on follow-up dates (t = 5, 19, 33; between-subject effect stimulation: F = 0.089, P = 0.768, within-subject effects time: F = 1.972, P = 0.151 and interaction time × stimulation: F = 0.244, P = 0.797). Baseline levels are the dotted (anodal) and dashed (sham) lines. Error bars show SEM. N = 24 healthy subjects (12 sham group, 12 anodal group).

Figure 6

Significant lasting effect in the central visual field. Contrast sensitivity in the central visual field was significantly higher than peripheral sensitivity in both groups (within-subject effect eccentricity: F = 262.494, P < 0.001). Contrast perception on follow-up dates revealed that tDCS-induced enhancement of contrast perception was solely significant within the central visual field (anodal 2–4°; diamond line) on day 19 compared to baseline (degrees 2–4; eccentricity × stimulation × time day 19 to baseline: F = 7.338, P = 0.013) and day 33 compared to baseline (F = 6.144, P = 0.021), whereas there was no significant effect regarding the visual field as a whole (stimulation × time day 19 to baseline: F = 2.558, P = 0.124, and day 33 to baseline: F = 2.325, P = 0.140). ^*P < 0.05; error bars show SEM. N = 24 healthy subjects (12 sham group, 12 anodal group).