Deterioration of postural control due to the increase of similarity between center of pressure and smooth-pursuit eye movements during standing on one leg

Abstract

Upright postural control is regulated by afferent and efferent/reafferent visual mechanisms. There are two types of efferent and conjugate eye movements: saccades and smooth pursuits. Although postural control is improved by saccades, the effects of smooth pursuits on postural control are still debated, because the difficulties of postural and visual tasks differ in the previous research. Additionally, the mechanisms that interfere with postural control and smooth pursuit are not fully understood. To address these issues, we examined the effects of different patterns of smooth-pursuit eye movement on the path length of the center of pressure (COP) displacement under bipedal and unipedal standing conditions. The relative frequency and amplitude of the COP displacement were remarkably increased when uniform linear visual targets were presented during unipedal standing. In addition, dynamic time warping analysis demonstrated that the similarity between the displacement of the COP and eye movements was increased by the presentation of uniform linear visual targets with orientation selectivity during unipedal standing but not during bipedal standing. In contrast, the attenuation of similarity between the displacement of the COP and eye movements significantly decreased the path length, relative frequency, and amplitude of the COP displacement. Our results indicate that postural stability is deteriorated by the increase of similarity between the displacement of the COP and smooth-pursuit eye movements under unstable conditions.

Fig 1. Schematic representation of the COP movement and gaze point measurement.

(A) The measurement system of the COP movement and gaze point. Participants stood at the center of the stabilometer and had a handheld keyboard. The monitor was set 60 cm in front of a stabilometer at eye level. (B-E) The visual targets were presented on the monitor. A 3 × 3 grid were continuously presented on the monitor. In the case of WO, there were no moving signals for 60 s (B). In the case of RM, a blue square was presented at one of the 3 × 3 grid for 0.9 s. After the blank phase for 1.6 s, a blue square was represented at one of the 3 × 3 grid for 0.9 s. The flushing presentation of the blue square was repeated 24 times. The order of presented areas of blue squares was randomized (C). In the case of SH, the movement of blue square was linear at 12.6 °/s along the x-axis. A New blue square appeared from the right edge after the complete disappearance to left. A total of 24 blue squares were presented (D). In the case of EL, a small blue square (1 pixel × 1 pixel) was presented at the center of the monitor; it was enlarged into 1080 pixels × 1080 pixels for 2.5 s. A total of 24 small blue squares were presented and enlarged (E).

Fig 2. Smooth-pursuit eye movement affected the path length of the COP displacement.

(A-D) Representative trajectories of the COP during bipedal (BP) standing under the presentation of no moving signals (WO, A), random flushing squares (RM, B), squares that shift from right to left (SH, C), and enlarged squares (EL, D). (E-H) Representative trajectories of the COP during unipedal (UP) standing under the presentation of the WO- (E), RM- (F), SH- (G), and EL-type (H) visual targets. (I) The total distances of COP movement under the presentation of the WO-, RM-, SH-, and EL-type visual targets during BP (orange) and UP (green) standing. (J) The distances of COP movement in the anteroposterior (AP) direction under the presentation of the WO-, RM-, SH-, and EL-type visual targets during BP (orange) and UP (green) standing. (K) The distances of COP movement in the mediolateral (ML) direction under the presentation of the WO-, RM-, SH-, and EL-type visual targets during BP (orange) and UP (green) standing. The box plots represent the median, first and third quartiles (boxes), and fifth and 95^th percentiles (whiskers). The number of participants: n = 14. Statistical differences were analyzed using Friedman’s analysis of variance followed by multiple Wilcoxon’s signed-rank test with Bonferroni correction. Abbreviations: AP, anteroposterior; BP, bipedal; ML, mediolateral; UP, unipedal. Statistical significance is indicated by asterisks: * P < 0.00833, ** P < 0.00167.

Fig 3. Changes in the relative proportion and amplitude of three frequency bandwidths of the COP displacement by smooth-pursuit eye movement.

(A, B) Alterations in the relative proportions of postural sway in low- (0.1–0.3 Hz, magenta), middle- (0.3–1.0 Hz, green), and high- (1.0–3.0 Hz, cyan) frequency bandwidths in the anteroposterior (AP) direction under the presentation of no moving signals (WO), random flushing squares (RM), squares which shift from right to left (SH), and enlarged squares (EL) during bipedal (BP, A) and unipedal (UP, B) standing. (C-E) Alterations in the amplitudes of postural sway in low- (C), middle- (D), and high- (E) frequency bandwidths in the AP direction under the presentation of the WO-, RM-, SH-, and EL-type visual targets during BP standing. (F-H) Alterations in the amplitudes of postural sway in low- (F), middle- (G), and high- (H) frequency bandwidths in the AP direction under the presentation of the WO-, RM-, SH-, and EL-type visual targets during UP standing. (I, J) Alterations in the relative proportions of postural sway in low-, middle-, and high-frequency bandwidths in the mediolateral (ML) direction under the presentation of the WO-, RM-, SH-, and EL-type visual targets during BP (I) and UP (J) standing. (K-M) Alterations in the relative proportions of postural sway in low- (K), middle- (L), and high- (M) frequency bandwidths in the mediolateral (ML) direction under the presentation of the WO-, RM-, SH-, and EL-type visual targets during BP standing. (N-P) Alterations in the amplitudes of postural sway in low- (N), middle- (O), and high- (P) frequency bandwidths in the ML direction under the presentation of the WO-, RM-, SH-, and EL-type visual targets during UP standing. The box plots represent the median, first and third quartiles (boxes), and fifth and 95^th percentiles (whiskers). The number of participants: n = 14. Statistical differences were analyzed using Friedman’s analysis of variance followed by multiple Wilcoxon’s signed-rank test with Bonferroni correction. Abbreviations: AP, anteroposterior; BP, bipedal; ML, mediolateral; UP, unipedal. Statistical significance is indicated by asterisks: * P < 0.00833, ** P < 0.00167.

Fig 4. The similarity between the displacement of the center of pressure (COP) and gaze point.

(A₁) Temporal displacement of the COP in the anteroposterior (AP, green) and mediolateral (ML, purple) directions under the presentation of the WO-type visual target during unipedal (UP) standing. (A₂) Temporal displacement of the gaze point in x- (purple) and y-axes (green) of the monitor under the presentation of the WO-type visual target during UP standing. (B₁) Temporal displacement of the COP in the AP and ML directions under the presentation of the RM-type visual target during UP standing. (B₂) Temporal displacement of the gaze point in the x- and y-axes of the monitor under the presentation of the RM-type visual target. (C₁) Temporal displacement of the COP in the AP and ML directions under the presentation of the SH-type visual target during UP standing. (C₂) Temporal displacement of the gaze point in the x- and y-axes of the monitor under the presentation of the SH-type visual target during UP standing. (D₁) Temporal displacement of the COP in the AP and ML directions under the presentation of the EL-type visual target during UP standing. (D₂) Temporal displacement of the gaze point in the x- and y-axes of the monitor under the presentation of the EL-type visual target during UP standing. (E) Representative warping alignment between temporal displacements of the COP in the ML direction (red) and the gaze point in the x-axis (blue) under the presentation of the SH-type visual target. (F, G) The nearest warping distance between the standardized plots of the COP and the gaze under the presentation of the WO- (cyan), RM- (green), SH- (magenta), and EL-type (yellow) visual targets during BP (F) and UP (G) standing. (H) The ratio of nearest warping distance (SH/WO) during UP standing. The box plots represent the median, first and third quartiles (boxes), and fifth and 95^th percentiles (whiskers). The number of participants: n = 14. Statistical differences were analyzed using Friedman’s analysis of variance followed by multiple Wilcoxon’s signed-rank test with Bonferroni correction. Abbreviations: AP, anteroposterior; BP, bipedal; DTW, dynamic time warping; ML, mediolateral; UP, unipedal. Statistical significance is indicated by asterisks: * P < 0.00833, ** P < 0.00167.

Fig 5. The decrease of similarity between the displacement of the center of pressure (COP) and the gaze point inhibited the displacement of the COP.

(A) The temporal coordinates of predictable SH-type (SH) visual object (A₁) and gaze point (A₂) in the x- (purple) and y- (green) axes respectively. (B) The temporal coordinates of unpredictable SH-type (ulSH) visual object (B₁) and gaze point (B₂) in the x- and y-axes respectively. (C) The change in the total distance of gaze point under the presentation of the SH- and ulSH-type visual targets. (D) The nearest warping distance between the standardized plots of the COP and the gaze under the presentation of the SH- and ulSH-type visual targets. (E) The relative ratio of nearest warping distance (ulSH/SH) during UP standing. (F) The total distance of COP movement under the presentation of the SH- and ulSH-type visual targets. (G, H) The distance of COP movement in the anteroposterior (AP, G) and mediolateral (ML, H) directions under the presentation of the SH- and ulSH-type visual targets. (I, J) The relative percentage of middle-frequency bandwidth of postural sway in the AP (I) and ML (J) directions under the presentation of the SH- and ulSH-type visual targets. (K, L) The amplitude of postural sway in middle-frequency bandwidths in the AP (K) and ML (L) directions under the presentation of the SH- and ulSH-type visual targets during UP standing. The box plots represent the median, first and third quartiles (boxes), and fifth and 95^th percentiles (whiskers). The number of participants: n = 14. Statistical differences were analyzed using Wilcoxon’s signed-rank test. Abbreviations: AP, anteroposterior; BP, bipedal; DTW, dynamic time warping; ML, mediolateral; UP, unipedal. Statistical significance is indicated by asterisks: * P < 0.05, ** P < 0.01.