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. 2021 Apr 30;16(4):e0250851. doi: 10.1371/journal.pone.0250851

Dynamic arm movements attenuate the perceptual distortion of visual vertical induced during prolonged whole-body tilt

Keisuke Tani 1,*, Shinji Yamamoto 2, Yasushi Kodaka 3, Keisuke Kushiro 4
Editor: Thomas A Stoffregen5
PMCID: PMC8087117  PMID: 33930085

Abstract

Concurrent body movements have been shown to enhance the accuracy of spatial judgment, but it remains unclear whether they also contribute to perceptual estimates of gravitational space not involving body movements. To address this, we evaluated the effects of static or dynamic arm movements during prolonged whole-body tilt on the subsequent perceptual estimates of visual or postural vertical. In Experiment 1, participants were asked to continuously perform static or dynamic arm movements during prolonged tilt, and we assessed their effects on the prolonged tilt-induced shifts of subjective visual vertical (SVV) at a tilted position (during-tilt session) or near upright (post-tilt session). In Experiment 2, we evaluated how static or dynamic arm movements during prolonged tilt subsequently affected the subjective postural vertical (SPV). In Experiment 1, we observed that the SVV was significantly shifted toward the direction of prolonged tilt in both sessions. The SVV shifts decreased when performing dynamic arm movements in the during-tilt session, but not in the post-tilt session. In Experiment 2, as well as SVV, the SPV was shifted toward the direction of prolonged tilt, but it was not significantly attenuated by the performance of static or dynamic arm movements. The results of the during-tilt session suggest that the central nervous system utilizes additional information generated by dynamic body movements for perceptual estimates of visual vertical.

Introduction

Knowledge of the gravitational direction is fundamental to our action and perception of the earth. The direction of gravity cannot be directly sensed; instead, it is estimated in the brain based on several types of sensory information. Numerous psychophysical studies have demonstrated the involvement of visual [1–3], somatosensory [4–6], and vestibular sensory signals [3, 7] in estimates of gravitational direction. Moreover, recent studies using computational modeling have shown that the central nervous system (CNS) weighs and combines these multisensory signals with prior knowledge and experience about the earth-vertical direction in a statistically optimal manner to resolve sensory ambiguity [7–9]. One typical way to evaluate internal estimates of the gravitational direction is the subjective visual vertical (SVV) adjustment, in which participants are asked to adjust a visual line to the perceived vertical [10]. Although the SVV closely coincides with the actual gravitational vertical in the upright position, the estimation error occurs when the head or body are tilted [11–14]. For instance, for a relatively small tilt angle (< 60°), the SVV typically shifts toward the opposite direction of body tilt [15]. Another method of assessing the perception of the gravitational direction is the subjective postural vertical (SPV) task, in which participants are asked to indicate their body’s vertical position while being inclined from one tilted side to the other [16]. It is known that although the estimation of postural vertical is relatively accurate, the SPV angle is affected by the direction and angle of the initial body tilt [16, 17].

The perception of gravitational direction is affected by maintaining the body in an inclined posture for a certain time, referred to as prolonged tilt. The SVV gradually shifts toward the tilted side during prolonged tilt [18–20] and remains deviated toward the previously tilted side even after a return to the upright position (i.e., after-effect) [19, 21–23]. Likewise, after prolonged tilt, the SPV biases toward the direction of prolonged tilt [24–27]. These time-dependent changes in SVV and SPV may be mainly attributable to sensory adaptation. Fernandez and Goldberg [28] showed that the otolith afferent firing rate in primates gradually decreased in the roll head-tilted position. Other studies suggest that somatosensory adaptation derived from trunk receptors may also contribute to the SVV shifts during prolonged tilt [11, 23]. The angles of the head and body relative to gravity would be sensed to be smaller due to vestibular and somatosensory adaptation, leading to shifts of the perceived direction of gravity toward the direction of prolonged tilt [29].

The present study aimed to investigate the effect of active arm movements on the perceptual estimates of gravitational direction. Performing arm movements against gravity generates additional information, such as proprioceptive feedback from muscle spindles, skin and joint receptors, and the Golgi tendon organ, as well as efferent copy [30], which would provide cues about the gravitational force on the arm. Moreover, the gravitational torque on the shoulder of an extended arm during arm lifting depends on the position of the arm relative to gravity [31]. Therefore, the gravitational cues generated by arm movements would play a role in estimating the gravitational direction. Previous studies have shown that the body tilt-induced errors in the judgment of the head-referenced eye level considerably decreased when accompanied by arm movements during judgment [32, 33]. This finding suggests that active body movements can improve the accuracy of spatial judgments, but it is unknown whether active body movements also influence the perceptual estimates of gravitational space not involving body movements. The CNS considers prior knowledge and experience as well as sensory signals to estimate the gravitational vertical [7–9], allowing us to hypothesize that additional cues generated by body movements may contribute to the subsequent perceptual estimates of the gravitational direction via prior knowledge and/or experience. To test this hypothesis, the present study evaluated whether static or dynamic arm movements during prolonged tilt influenced the perceptual judgments of visual vertical (Experiment 1) or postural vertical (Experiment 2). As mentioned above, the internal estimates of the gravitational direction are distorted during or after prolonged tilt, primarily due to sensory adaptation. We expected that these distorted estimates might be corrected based on additional cues generated by arm movements, resulting in the maintenance of SVV or SPV angles even after prolonged tilt.

Experiment 1

Materials and methods

Participants

Fifteen right-handed healthy volunteers (13 males and 2 females, aged 19–33 years) participated in this experiment after providing written informed consent. All participants had normal vision and no neurological, muscular, or cognitive disorders. This study was approved by the Ethics Committee of the Graduate School of Human and Environmental Studies, Kyoto University, and was conducted in accordance with the Declaration of Helsinki (2013).

Apparatus

The participants sat on a seat (RSR-7 KK100, RECARO Japan, Japan) mounted on a tilt table in a completely dark room. The head, trunk, and legs were firmly secured to the seat with bands and a four-point safety belt in a natural position (Fig 1). An axis under the tilt table was expanded or contracted via a servo motor, enabling the tilt table to be tilted in the roll plane around a rotation center located 18 cm underneath the bottom of the seat. The tilting velocity and initial acceleration were 0.44°/s and 0.09°/s2, respectively, which are below the rotational acceleration threshold [34]. Therefore, in the present study, the contribution of the semi-circular canal to the estimation of the visual vertical would be negligible.

Fig 1. Schematic illustration of the experimental setup.

Fig 1

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This figure illustrates a situation in which the participant was tilted leftward. The display portion was rotated in yaw, as denoted by a gray arrow.

A display (LTN097QL01, SAMSUNG, Korea; 19.6 cm × 14.7 cm) was placed 35 cm in front of the participant’s face. To prevent any spatial cues such as the edge of the display, a black-colored cylinder (26 cm in diameter) with one end covered by a plate with a hole (10 cm in diameter) in the center was placed between the face and the display. During the SVV adjustment, a white line (length, 4 cm; width, 0.1 cm) that was rotated via a digital controller (BSGP1204, iBUFFALO, Japan) was presented at the center of the display. An anti-aliasing mode was applied to the projection to avoid any orientational cues derived from the pixel alignment. The display was mounted on the tilt table via metal frames (Green Frame, SUS, Japan), maintaining identical display positions relative to the participants regardless of the body tilt angle. The center of a vertical frame positioned on the left side of the tilt table had a hinge structure, enabling the display portion to be rotated in the yaw plane independently of the tilting chair. Before the participants performed the task (see Task during prolonged tilt in detail), an experimenter rotated the display portion to the left side of the participants, preventing them from hitting their arm against the display or frames. An electric magnet was placed between the display portion and the horizontal frame positioned on the right side of the tilt table. The display portion and frames were firmly fixed via electrification of the electric magnet, enabling it to be set in front of the face. Prior to each experiment, the angle of the tilt table and the upper side of the display relative to the floor was calibrated at 0° using a digital inclinometer.

To temporarily restrict vision, the participants wore a mechanical shutter goggle controlled via a microcomputer (Arduino UNO, Arduino SRL, United States) during the experiment. They also wore earphones via which white noise was provided to avoid auditory cues from the environment.

Experimental procedure

This experiment consisted of two sessions: the during-tilt and post-tilt sessions. In the former, we evaluated how the SVV was influenced by arm movements at the tilted position. In the latter, we confirmed whether the effects of arm movements during prolonged body tilt influenced the SVV after returning to the near-upright positions (0° or ±4°). These angles were determined based on the fact that 4° is the threshold for the detection of body tilt in the roll plane [35]. The order of each session was randomized for each participant.

Fig 2A shows a sequence of experimental trials in the during-tilt session. After the shutter was closed, the tilt table was tilted to the left. One second after the tilt table came to the left-side-down (LSD) 16° position, the shutter opened again, and a white line was presented on the display. The participants were asked to adjust the line to the gravitational vertical via the controller (SVV adjustment). The initial angle of the line was set at ±45°, ±60°, or 90° relative to the body longitudinal axis in a pseudorandomized order. The participants performed five trials of the SVV adjustment within 40 seconds. The shutter then closed, and the display portion was moved leftward by the experimenter. The participants were asked to execute one of three tasks (see Task during prolonged tilt) at the tilted position. After the display portion was returned to the initial position (i.e., in front of the participant’s face), the shutter opened and the participants were asked to perform the SVV adjustments for five trials again. Each participant performed this sequence of experimental trials for each task condition, that is, 30 trials (three task conditions [No-movement, Static, Dynamic tasks] × 2 phases [before, after task] × 5 SVV adjustments) in total. A break of approximately 2 min was given between conditions. The order of the task conditions was pseudorandomized for each participant.

Fig 2.

Fig 2

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Schematic illustration of the experimental procedure in the during-tilt (A) and post-tilt sessions (B) and the Control condition (C). In both sessions, participants were asked to perform one of three tasks (No-movement, Static, or Dynamic task) during prolonged tilt in response to preparation (denoted as red) or action sounds (denoted as blue). As an example, the auditory cue for the dynamic task is shown in figures (A) and (B).

Fig 2B shows a sequence of experimental trials in the post-tilt session. After the participants were tilted to the LSD 16° position from upright with the shutter closed, the display portion was moved leftward by the experimenter, and the participants were asked to perform one of the three tasks during prolonged tilt. The display portion was then moved back to the original position, and the body was tilted to one of three final tilt positions: upright, right-side-down (RSD) 4°, or LSD 4°. The shutter was opened, and the participants were asked to repeat the SVV adjustments for five trials. After completing the task, the body was returned to the upright position via the RSD 16° position to avoid providing feedback about the final tilt position that could influence the subsequent performance on the SVV adjustment. In this session, the participants were not informed of the angles of the final tilt positions. Each participant performed this sequence of trials for each task condition in each final tilt position, that is, 45 trials (three task conditions [No-movement, Static, Dynamic tasks] × 3 final tilt positions [0°, ±4°] × 5 SVV adjustments) in total.

After all trials were completed, participants performed the SVV adjustments for five trials in each final tilt position (0° and ±4°) immediately after being tilted from an upright position (not via the LSD position), referred to as the Control condition (Fig 2C). Note that the effect of prolonged tilt (including the initial tilt) and arm movements at the LSD 16° position would not be reflected in the angle of SVV in the Control condition.

Task during prolonged tilt

The participants performed one of the three tasks during prolonged tilt as follows: no-movement, static, or dynamic tasks. For the no-movement task, neither preparation nor action sounds were presented, and the participants were asked to maintain their tilted posture. For the static task, a preparation sound was first presented via the earphones, prompting the participants to switch the controller to their left hand and to point to the front of the face using their right index finger with the right arm extended. The participants were instructed to maintain this posture until another preparation sound was presented. For the dynamic task, a preparation sound was first presented, and participants were asked to set the pointing posture as with the static tasks. Three seconds after the preparation sound, an action sound was presented every 3 s for a total of 10 times. The participants were asked to move their arm upward and then down parallel to their body’s longitudinal axis once per action sound with their arm extended. The length of the arm movement was set from the height of the eye to the navel. Then, another preparation sound was presented, prompting them to hold the controller again.

Prior to the beginning of the experiment, the participants practiced each task sufficiently. The duration of each action condition (i.e., duration of prolonged tilt) was identical across all conditions (34 s). The order of the tasks was pseudorandomized across the participants.

Data analysis

The SVV angle was calculated as the deviation between the subjective vertical and actual gravitational vertical for each trial. The median of five trials was applied as the representative value for each task condition for each participant. To determine the extent of SVV shifts induced by prolonged tilt and arm movements, the ΔSVV values were calculated by subtracting the SVV angle before the task from that after it for the during-tilt session, and by subtracting the SVV angle in the Control condition from the SVV angle in each task condition (No-movement, Static, Dynamic) for the post-tilt session. The results of Shapiro-Wisk test showed that the SVV angles and ΔSVV values were normally distributed across participants in all conditions for the during-tilt session (all p > 0.05), but not in some conditions for the post-tilt session (p < 0.05). Therefore, parametric statistical analyses were applied to the dataset in the during-tilt session, while non-parametric analyses were applied to the dataset in the post-tilt sessions. Specifically, the ΔSVV in each task condition were compared using one-way analysis of variance (ANOVA; three task conditions [No-movement, Static, Dynamic]) with repeated measures for the during-tilt session and Friedman tests (three task conditions [No-movement, Static, Dynamic]) for the dataset in each final tilt position (0, LSD, or RSD 4°) for the post-tilt session.

For the ANOVA, the degrees of freedom were corrected using Greenhouse-Geisser correction coefficient epsilon, and the p-value was recalculated if sphericity was violated with Mauchly’s sphericity test. The significance level for all comparisons was set at p < 0.05. Bonferroni correction was used for post-hoc multiple comparisons. All statistical analyses were conducted using R software version 3.5.3 (R Core Development Team, Austria).

Results

Prolonged tilt effect

We first checked whether prolonged tilt induced SVV shifts in the present experimental setup. Fig 3 shows the angular changes of the SVV in the No-movement condition for the during-tilt session and SVV angles in the Control and No-movement conditions for the post-tilt session. Positive and negative values correspond to rightward and leftward deviations, respectively. For the during-tilt session, a paired t-test revealed that the SVV angle after the no-movement task (1.3 ± 1.2°) significantly shifted leftward compared to that before the task (-0.4 ± 1.3°; t11 = 2.58; p < 0.05, Cohen’s d = 0.67). For the post-tilt session, the median SVV angles (1st, 3rd quartiles) in the Control and No-movement conditions were -1.0° (-1.5, 0.7) and -2.7° (-6.0, -0.4) for the LSD 4° position, -1.5° (-2.5, 0.5), and -3° (-5.6, -0.9) for the 0° position, and -3.5° (-6.5, -1.5) and -4.0° (-8.6, -1.8) for the 4° RSD position. The SVV angles for the Control condition were not significantly different between the final tilt positions (Friedman test; main effect χ2 = 2.07; p = 0.36). The results of Wilcoxon signed ranked test showed that the SVV angle in the No-movement condition significantly shifted leftward compared to the Control condition for LSD 4° (p < 0.001, effect size r = 0.86) and 0° positions (p < 0.05, effect size r = 0.78), but not for the RSD 4° position (p = 0.35, effect size r = 0.28).

Fig 3. The alteration of SVV angles during prolonged tilt without arm movements.

Fig 3

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‘Con’ and ‘No-m’ refer to the Control and No-movement conditions, respectively. Grey bars denote the individual median data, and black bars denote the group-mean (during-tilt session) or -median data (post-tilt session). *: p < 0.05, **: p < 0.01.

During-tilt session

Fig 4A shows the group-mean ΔSVV value for each task condition. The results of one-way ANOVA revealed a significant main effect of task condition (F2, 28 = 4.77, p < 0.05, effect size η2 = 0.14). Results of post-hoc Bonferroni tests showed that the ΔSVV in the No-movement (-1.6 ± 0.6°) and Static conditions (-1.2 ± 0.4°) were smaller (i.e., shifted leftward) than in the Dynamic condition (0.2 ± 0.4°; vs No-movement, p < 0.05, effect size r = 0.60; vs Static, p < 0.05, effect size r = 0.54). No significant differences were noted between the Static and No-movement conditions (p = 0.46, effect size r = 0.19). These results indicate that the SVV shifts that occurred during prolonged tilt were attenuated when performing dynamic arm movements.

Fig 4.

Fig 4

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The group-mean ΔSVV values in the during-tilt (A) and post-tilt sessions (B). (A) Error bars denote standard error. (B) The horizontal line within each box and the lower and upper ends of each box represent the median and 1st and 3rd quartiles, respectively. *: p < 0.05

Post-tilt session

Fig 4B shows the group-median ΔSVV in each final tilt position for each action condition. The results of Friedman tests revealed a significant main effect of task condition for the LSD 4° position (χ2 = 8.40, p < 0.05), but not for 0° (χ2 = 2.53, p = 0.28) and RSD 4° (χ2 = 0.85, p = 0.65). For the LSD 4° position, however, the results of post hoc tests showed no significant differences in ΔSVV among different task conditions (No-movement vs Dynamic, p = 0.13, effect size r = 0.58; No-movement vs Static, p = 0.15, effect size r = 0.52; Static vs Dynamic, p = 0.44, effect size r = 0.38). These results indicate that the SVV shifts that occurred after prolonged tilt were not significantly influenced by either static or dynamic arm movements during prolonged tilt.

Experiment 2

Materials and methods

Participants

Twelve right-handed healthy volunteers (8 men and 4 women, aged 22–26 years) participated in this experiment after providing written informed consent. Similar to Experiment 1, this experiment was approved by the Ethics Committee of the Graduate School of Human and Environmental Studies, Kyoto University, and was conducted in accordance with the Declaration of Helsinki (2013).

Apparatus

As in Experiment 1, the participants sat on a tilting chair, and the head, trunk, and legs were firmly fastened to the seat. In this experiment, the velocities of the tilt table were different from those in Experiment 1. The velocity of the tilt-chair during the subjective postural vertical (SPV) task (see Experimental Procedure paragraph) was set at 1.0°/s (initial acceleration: 0.52°/s2) to avoid the stimulation of semi-circular canals [34]. The velocity of the chair from upright to LSD 16° (before the SPV task) and from RSD 16° to the upright position (after the SPV task) was relatively fast (8.0°/s). However, as a previous study [36] reported that the amplitude of post-rotatory nystagmus was small even after roll body tilt at a speed of 10°/s, the contribution of the semicircular canal to SPV estimations was negligible.

The participants held a custom-made controller with a press button to indicate the position of the perceived body vertical. The roll-tilt angle of the chair was monitored using an accelerometer module (KXM52-1050, Kionix, USA) mounted at the center of the tilt table. The signals from the accelerometer and controller were recorded using a data acquisition system (Power Lab 16sp, AD Instruments, Australia). The sampling frequency was set to 100 Hz.

During the experiment, the participants wore an eye-mask and were provided with white noise via earphones so as not to provide visual or auditory cues from the environment. To prevent the participants from being fatigued, a rest period of approximately 10 min was inserted per 10 SPV trials.

Experimental procedure

The blindfolded participants were first tilted to LSD 16°. In this position, they were presented with one of four task conditions (No-movement, Static, Dynamic, Control). Under the former three conditions, as in Experiment 1, they were asked to perform each task according to the preparation and action sounds (see Task during prolonged tilt), and then they were tilted to RSD 16°. While tilted from LSD 16° to RSD16°, they were asked to press the bottom of the controller when they felt that their body was upright (SPV task). In the Control condition, they were tilted to RSD 16° immediately after arriving at LSD 16° (i.e., without prolonged tilt) and performed the SPV task. After each SPV task, the participants were tilted back to the upright position. As in Experiment 1, the duration of each task was 34 s.

All the participants performed 7 trials of the SPV task for each of the four task conditions, that is, a total of 28 trials. The order of presentation of the task conditions was pseudorandomized for each participant.

Data analysis

The SPV angle was calculated as the deviation between the subjective vertical and actual gravitational vertical for each trial. The median was used as the representative value of the SPV angles for each task condition for each participant. Similar to SVV, the extent of SPV shifts (ΔSPV) induced by prolonged tilt and arm movements were quantified by subtracting the SPV angle in the Control condition from that in each task condition (No-movement, Static, and Dynamic). Since the SPV angles in each task condition were normally distributed across participants (Shapiro-Wisk tests, p > 0.05), a one-way ANOVA with repeated measures (three task conditions [No-movement, Static, Dynamic]) was conducted to compare ΔSPV values between task conditions. If sphericity was violated under Mauchly’s sphericity test, the degree of freedom was corrected using the Greenhouse-Geisser correction coefficient epsilon, and the p-value was recalculated.

Results

Fig 5A shows the mean SPV angles in the Control and No-movement conditions. The SPV angle significantly shifted leftward in the No-movement condition (-5.0 ± 0.9°), compared to the Control condition (-0.8°± 1.2°; t11 = 5.77, p < 0.001, Cohen’s d = 1.67). This result indicates significant SPV shifts induced by prolonged tilt.

Fig 5.

Fig 5

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The SPV angles in the Control and No-movement conditions (A) and group-mean ΔSPV value in each task condition (B). (A) Gray and black lines represent the individual median and group-mean values, respectively. (B) Error bars represent standard errors. ***: p < 0.001.

Fig 5B shows the group-mean ΔSPV values for each task condition. The mean (±SE) ΔSPV were -4.3 ± 0.7° for the No-movement condition, -3.5 ± 0.8° for the Static condition, and -3.9 ± 0.8° for the Dynamic condition, respectively. The result of one-way ANOVA revealed a non-significant main effect of task condition (F2, 22 = 2.54, p = 0.10) with a small effect size (η2 = 0.01). This result indicates that neither static nor dynamic arm movements significantly influenced the SPV shifts induced by prolonged tilt.

Discussion

The present study investigated how static or dynamic arm movements influenced changes in the SVV and SPV angles induced by prolonged tilt. In Experiment 1, we found that the performance of dynamic arm movements effectively attenuated the SVV shifts that occurred during prolonged tilt (during-tilt session), but not after prolonged tilt (post-tilt session). In Experiment 2, the SPV angles were not significantly affected by either static or dynamic arm movements.

Extending previous findings that the accuracy in spatial judgment at the tilted position was considerably improved by accompanying arm movements during judgment [32, 33], we hypothesized that active body movements could subsequently influence perceptual estimates of gravitational direction not involving body movements. Based on this hypothesis, we predicted that the perceptual distortion of the gravitational direction induced by prolonged tilt would decrease when active arm movements are performed in the tilted position. In support of our prediction, the results of the during-tilt session showed that the shifts of SVV toward the direction of prolonged tilt (Fig 3, left panel) were attenuated when the participants performed dynamic arm movements during prolonged tilt (Fig 4A). Prolonged tilt induces adaptive changes in the vestibular and body somatosensory systems [23, 28], leading to a decrease in the sensed angles of the head and/or body relative to gravity [29]. The performance of arm movements against gravity provides supplemental cues such as proprioceptive feedback or efferent copy [30] for estimating head and/or body orientation in space. The CNS would likely recalibrate the internal estimates of the gravitational direction based on these information, resulting in the stable perceptual judgment of visual vertical through prior knowledge/experience.

In contrast to dynamic arm movements, we observed no significant effects of static arm movements on SVV in the during-tilt session, even though the gravitational force on the arm, dependent on the body’s tilt angle, is generated by both types of arm movements. The lack of an effect of static arm movements may imply that the dynamic property of arm movements is important for estimating the visual vertical. The gravitational force on the arm during arm movements can be perceived as a sense of heaviness based on the afferent information about muscle tension from the Golgi tendon organ (GTO) located at the muscle-tendon junction [37, 38]. Psychophysical studies have shown that estimation of the heaviness of an object with concurrent dynamic movements, such as lifting or wielding, is more accurate than estimation with static holding [39, 40]. In addition, a physiological study has demonstrated that when constant tension is persistently applied to a muscle, the firing rate and sensitivity of the GTO to the force gradually deteriorate [41]. These findings lead us to speculate that information about the gravitational force on the arm might be conveyed to the CNS more accurately while performing dynamic than static arm movements, leading to effective attenuation of the prolonged-induced SVV shifts.

In the post-tilt session, the significant SVV shifts after prolonged tilt were observed in the final tilt positions of LSD 4° and 0° (Fig 3, right panel). However, in contrast to the during-tilt session, dynamic arm movements did not significantly attenuate these SVV shifts (Fig 4B). One possible explanation for this difference between the sessions is the interval between the arm movement task and SVV adjustment. In the during-tilt session, the participants performed the SVV adjustments immediately after the arm movement task. On the other hand, in the post-tilt session, they performed the SVV adjustments after slowly tilting back toward each final tilt position; thus, the interval between dynamic arm movements and SVV adjustments was relatively long (at least 20s). The contribution of the additional cues derived from dynamic arm movements to visual vertical estimates likely diminished over time after the task, thereby resulting in no clear effects of dynamic arm movements on SVV in the post-tilt session. In favor of this assumption, the attenuation effect of dynamic arm movements on SVV shifts appears to be greater at positions closer to the initial tilt position, where the interval between the action task and SVV adjustment was shorter.

The prolonged tilt-induced SPV shifts were not significantly influenced by either static or dynamic arm movements (Fig 5). Due to the relatively long time between the estimation of postural vertical and the arm movement task, as well as the post-tilt session, the lack of significant effect of arm movements on the SPV may also be attributed to the temporal decay of the arm movement effects. In contrast, a previous study showed that detection of self-body tilt was not improved even immediately after dynamic arm movements [42]. Given this, the present result in SPV may indicate that the arm movement-related gravitational cues are less utilized for the estimation of body orientation relative to gravity.

Although the results of the during-tilt session suggest the role of active body movements in the conscious perception of the gravitational direction, it remains unclear whether or how they influence the control of body orientation. Previous studies have shown an inconsistency between perceived and achieved body orientations when actively controlling body orientation [43, 44]. This suggests that dynamic body movements may have different effects on the perception of gravitational direction and control of body orientation. On the other hand, some recent studies have demonstrated the contribution of dynamic somatosensory cues to active postural control [45, 46]. Future research directly assessing the influence of dynamic arm movements on the achieved body orientation would be helpful for a better understanding of the mechanisms underlying the perception and control of body orientation in space.

Three limitations must be noted when interpreting our findings. First, the sample size was relatively small. In particular, at the LSD 4° position in the post-tilt session, no significant differences were noted between the No-movement condition and the Static or Dynamic conditions despite the large effect size (r > 0.50), which is likely a result of the small sample size. Therefore, our findings need to be confirmed by studies that include a larger sample size. Second, we used a static whole-tilt for the SVV assessment in which the gravitational and gravitoinertial force (GIF) vectors were the same; therefore, it remains unknown whether participants responded to either force vectors. Since the otolith system responds to both gravitational and inertial forces [28], the visual vertical estimation reflects a response to the GIF. However, a previous study has shown that the estimation of the earth-horizontal direction is differently influenced by whole-body tilt and body centrifugation, even though the GIF vector relative to the head was identical [33]. This implies that the gravitational force may specifically affect the perception of gravitational direction. To address this, further studies are needed to dissociate the gravitational and GIF vectors. Third, the arms were not restrained to the body during prolonged tilt. In such a situation, gravity would have pulled the arms to the side, providing a static cue for the perception of the gravitational direction even when the arm movements were not performed (i.e., No-movement condition). This methodological limitation may be partially responsible for the lack of a significant difference in the SVV angles between the No-movement and Static conditions.

Conclusion

The present study shows that dynamic arm movements can attenuate the perceptual distortion of the visual vertical induced by prolonged tilt. This finding suggests that the supplementary information generated by dynamic body movements plays an important role in the perceptual estimates of gravitational direction as well as vestibular and body somatosensory signals. To provide a comprehensive understanding of the relationship between action and the perception of the gravitational space, we need to further examine how performance in the estimation of the gravitational direction is influenced by the manipulation of temporal (e.g., arm movement velocity, interval between arm movements and perceptual tasks) and spatial properties (e.g., direction and angle of arm movements or body tilt).

Data Availability

All individual dataset are available from Open Source Framework (OSF) at https://doi.org/10.17605/OSF.IO/BUFTG.

Funding Statement

The present study was funded by Japan society for the promotion of science (JSPS) KAKENHI No. 17J07245 and No. 20K19305 (to KT), and No. 16K01595 and No. 19K11621 (to KK). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Decision Letter 0

Thomas A Stoffregen

22 Jan 2021

PONE-D-20-40610

Dynamic arm movements attenuate perceptual distortion of visual vertical induced during prolonged whole-body tilt

PLOS ONE

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Reviewer #1: Restrained subjects were passively tilted to a fixed angle in the coronal plane. The subject’s task was to adjust a display (a line) to align with the “gravitational vertical”. These subjective reports were made before and after arm movements, and after the completion of passive body tilt. In Experiment 2, passive body tilt was ongoing, and subjects were asked to indicate when they felt their body to be aligned with “gravitational vertical”. The results replicated common findings that the subjective vertical can be influenced by passive body tilt. The main finding was that perceived orientation was influenced by arm movements.

The authors claim that “no experimental evidence” exists relating active body movement to perception of “gravitational space”. This claim seems odd, given that the authors have cited the work of Bringoux, who studied exactly this topic. In addition, other studies have examined the role of active movement on perception of orientation, in general, and the vertical in particular. Perhaps the closest, with respect to the present study, is the work of Fouque et al. (1999), in which active arm movements were related to whole body tilt in the perception of orientation. In revising, I think the authors should explain how their hypotheses, design, results, and interpretation differ from Fouque et al. In addition, please revise to indicate that the present study provides information only about perception during passive tilt, as contrasted with studies in which body tilt has been actively controlled (e.g., Panic et al., 2015; Riccio et al., 1992). It would be specially helpful, in the Discussion, to consider how future research might help us understand relations between perceived orientation during passive versus active tilt. Achieved orientation can differ from subjective orientation; moreover, outside the laboratory, conscious awareness of orientation is uncommon, whereas (successful) control of orientation is nearly continuous.

It is widely assumed that the body is controlled relative to the direction of gravity, but this view is not universal. In fact, it has come under sustained criticism, mainly because body movement is not constrained directly (or solely) by the gravitational vector but, rather, by the sum of gravitational and inertial forces—the gravitoinertial force vector (e.g., Stoffregen & Riccio, 1988). In the present experiments, the gravitational and gravitorinertial force vectors were the same, and so the results cannot tell us whether participants were responding to one or the other. This limitation of the design should be noted in the Discussion. Similarly, clinical data from stroke patients do not permit the scientist to know which vector is detected.

The Introduction should be revised to state explicitly the hypotheses that were tested in the study. What testable predictions did the authors make? Similarly, the Discussion should be revised to re-state the predictions indicating, in each case, whether each prediction was (or was not) confirmed. The pattern of confirmed (vs. not confirmed) predictions should structure data interpretation.

Please revise so that the Results of Experiment 1 are presented before the Method of Experiment 2. That is, completely present Experiment 1, and then completely present Experiment 2.

Fouque, F., Bardy, B. G., Stoffregen, T. A., & Bootsma, R. B. (1999). Intermodal perception of orientation during goal-directed action. Ecological Psychology, 11, 45-79.

Panic, H., Panic, A. S., DiZio, P. & Lackner, J. R. (2015). Direction of balance and perception of the upright are perceptually dissociable. Journal of Neurophysiology, 113, 3600-3609.

Riccio, G. E., Martin, E. J., & Stoffregen, T. A. (1992). The role of balance dynamics in the active perception of orientation. Journal of Experimental Psychology: Human Perception & Performance, 18, 624-644.

Stoffregen, T. A., & Riccio, G. E. (1988). An ecological theory of orientation and the vestibular system. Psychological Review, 95, 3-14.

Reviewer #2: This interesting paper investigates dynamic arm movements as a new variable in the long search for the sensory determinants of the subjective vertical. The 'During Tilt' portion of Experiment 1 first re-demonstrates the known ability of prolonged tilt to bias the subjective visual vertical (SVV) towards the tilt, and then shows (as a new finding) that a series of dynamic arm movements during the tilt reduces this bias. The 'Post Tilt' portion of Experiment 1 shows that this bias reduction does not occur if the SVV is estimated after the participant is moved to a different tilt angle. This may be due to the timing between the prolonged tilt and the SVV estimation (as mentioned by the authors) but could also be due to the new tilt angle 'overwriting' the participant's sense of orientation. Experiment 2 shows that a subjective postural vertical estimation is not affected by the dynamic arm movements in the same manner as the SVV estimation is. The sample sizes are on the small side, as noted by the authors themselves, but the data analysis appears to be well done. I recommend some revisions as follows:

Lines 46-92

The introduction is not as thorough as I would expect in an otherwise well-written paper. Many of the references are grouped together with somewhat superficial descriptions, such as in Lines 49-51. There are very few references from the past 10 years, despite considerable recent research from several labs on the use of dynamic and movement cues on balance. The paper would benefit from a more substantive introduction, which could then be used to deepen the discussion of the results.

Lines 104-106

Was there a reason not to secure the participants’ arms by some mechanism that could be loosened/removed at the same time as the display frame was rotated to the left? If the arms were left unsecured then they will necessarily be pulled to the side by gravity when in a static roll, and this would provide an extra, potentially confounding sensory cue. This may have been a reason why the no-movement and static conditions did not significantly differ (Fig 4).

Lines 142-165, Lines 242-253

The term ‘trial’ appears to be used for two different types of event: a single instance of the participant setting the white line for SVV (as in line 148), as well as a set of ‘tilt, SVV, task, SVV’ (as in line 153). The explanation of the procedure would be clarified if two different terms were used.

Line 159

What was the rationale for selecting to test at 4 degrees left, 0 degrees, and 4 degrees right? Would a larger tilt be expected to produce a larger effect?

Lines 160-162

It was not clear to me why the 'Post Tilt' experimental procedure ends with moving the participant to 16 degrees right and then to the start position. These tilts happen after the SVV estimations are made, so are they necessary? If they are necessary for the 'Post Tilt' procedure, why are they not done at the end of the 'During Tilt' procedure?

Lines 378-382

The lack of effect of dynamic arm movements on SVV estimation in the 4 degree Right position for the ‘Post Tilt’ procedure is explained as a result of a small sample size. This may be true, but it may also represent an effect of always using a prolonged left tilt at the start of the experiment. What would happen if the initial tilt was to the right instead?

Figure 1:

This figure appears to be added to show how the display rotates in yaw away from the participant. I found it confusing at first, because I was expecting an image showing the roll rotation used in the experiment. Perhaps the figure could be updated to show both of these features.

Figure 3:

Why is the SVV angle for the control in the +4 RSD group so different from the controls in the +4 LSD and 0 degrees groups? I would think that all three groups would have very similar values on the control.

Figure 3:

Why is the variability so much larger for the +4 RSD group, compared to the +4 LSD and 0 degrees groups?

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PLoS One. 2021 Apr 30;16(4):e0250851. doi: 10.1371/journal.pone.0250851.r002

Author response to Decision Letter 0

29 Mar 2021

Reviewer #1

Comment 1

Restrained subjects were passively tilted to a fixed angle in the coronal plane. The subject’s task was to adjust a display (a line) to align with the “gravitational vertical”. These subjective reports were made before and after arm movements, and after the completion of passive body tilt. In Experiment 2, passive body tilt was ongoing, and subjects were asked to indicate when they felt their body to be aligned with “gravitational vertical”. The results replicated common findings that the subjective vertical can be influenced by passive body tilt. The main finding was that perceived orientation was influenced by arm movements.

Responses;

We appreciate the constructive comments from the reviewers. We have carefully read the comments and corrected our manuscript accordingly.

Comment 2

The authors claim that “no experimental evidence” exists relating active body movement to perception of “gravitational space”. This claim seems odd, given that the authors have cited the work of Bringoux, who studied exactly this topic. In addition, other studies have examined the role of active movement on perception of orientation, in general, and the vertical in particular. Perhaps the closest, with respect to the present study, is the work of Fouque et al. (1999), in which active arm movements were related to whole body tilt in the perception of orientation. In revising, I think the authors should explain how their hypotheses, design, results, and interpretation differ from Fouque et al. In addition, please revise to indicate that the present study provides information only about perception during passive tilt, as contrasted with studies in which body tilt has been actively controlled (e.g., Panic et al., 2015; Riccio et al., 1992). It would be specially helpful, in the Discussion, to consider how future research might help us understand relations between perceived orientation during passive versus active tilt. Achieved orientation can differ from subjective orientation; moreover, outside the laboratory, conscious awareness of orientation is uncommon, whereas (successful) control of orientation is nearly continuous.

Responses;

As pointed out by the reviewer, our description was inappropriate because other papers (Bringoux et al. 2004, 2007; Scotto Di Cesare et al. 2014) have shown the influence of arm movements on spatial judgments even though these results were not positive. Thus, we have removed the description “no experimental evidence” from the manuscript, and accordingly, we have modified the abstract.

Fouque et al. (1999) showed that concurrent arm movements improved accuracy in judgments of the head-referenced eye level, proposing that action promotes spatial judgment. However, this finding cannot tell us whether action also influences the perceptual judgment of gravitational space, not involving body movements. As the CNS would estimate the gravitational vertical by integrating not only sensory inputs but also prior knowledge/experience (Clemens et al. 2011), active body movements may also influence the subsequent perceptual estimates of the gravitational direction via prior knowledge/experience. To assess this hypothesis, we evaluated whether or how active arm movements during prolonged tilt subsequently influenced the perceptual judgments of gravitational direction (SVV or SPV). The results of the during-tilt session showed a significant attenuation of SVV shifts by dynamic arm movements (Fig. 4), at least partially supporting our hypothesis. This result extends Fouque et al.’s finding and suggests that action contributes to perceptual estimates of gravitational space, even without accompanying body movements. We have modified the text (Introduction and Discussion) to emphasize the differences between our study and theirs.

As the reviewer indicates, the body orientation continuously achieved in our daily life would not always be consistent with the conscious and perceived orientation of vertical. Panic et al. (2015) showed that the dissociation of the direction of balance (DOB) from the gravitational vertical influences the achieved body upright during active tilt, but not perceived upright. Unfortunately, since our study used only passive body tilt, it remains unknown whether or how prolonged tilt influences the achieved orientation when actively controlling the body, and whether it is modulated by arm movements. We have described the importance of directly assessing the effects of active body movements on the control of body orientation in future research.

Changes;

Abstract

Lines 24-28

Concurrent body movements have been shown to enhance the accuracy of spatial judgment, but it remains unclear whether they also contribute to perceptual estimates of gravitational space not involving body movements. To address this, we evaluated the effects of static or dynamic arm movements during prolonged whole-body tilt on the subsequent perceptual estimates of visual or postural vertical.

Introduction

Lines 80-94

Previous studies have shown that the body tilt-induced errors in the judgment of the head-referenced eye level considerably decreased when accompanied by arm movements during judgment [32,33]. This finding suggests that active body movements can improve the accuracy of spatial judgments, but it is unknown whether active body movements also influence the perceptual estimates of gravitational space not involving body movements. The CNS considers prior knowledge and experience as well as sensory signals to estimate the gravitational vertical [7-9], allowing us to hypothesize that additional cues generated by body movements may contribute to the subsequent perceptual estimates of the gravitational direction via prior knowledge and/or experience. To test this hypothesis, the present study evaluated whether static or dynamic arm movements during prolonged tilt influenced the perceptual judgments of visual vertical (Experiment 1) or postural vertical (Experiment 2). As mentioned above, the internal estimates of the gravitational direction are distorted during or after prolonged tilt, primarily due to sensory adaptation. We expected that these distorted estimates might be corrected based on additional cues generated by arm movements, resulting in the maintenance of SVV or SPV angles even after prolonged tilt.

Discussion

Lines 350-363

Extending previous findings that the accuracy in spatial judgment at the tilted position was considerably improved by accompanying arm movements during judgment [32,33], we hypothesized that active body movements could subsequently influence perceptual estimates of gravitational direction not involving body movements. Based on this hypothesis, we predicted that the perceptual distortion of the gravitational direction induced by prolonged tilt would decrease when active arm movements are performed in the tilt position. In support of our prediction, the results of the during-tilt session showed that the shifts of SVV toward the direction of prolonged tilt (Fig. 3, left panel) were attenuated when the participants performed dynamic arm movements during prolonged tilt (Fig. 4A). Prolonged tilt induces adaptive changes in the vestibular and body somatosensory systems [23,28], leading to a decrease in the sensed angles of the head and/or body relative to gravity [29]. The performance of arm movements against gravity provides supplemental cues such as proprioceptive feedback or efferent copy [30] for estimating head and/or body orientation in space. The CNS would likely recalibrate the internal estimates of the gravitational direction based on these information, resulting in the stable perceptual judgment of visual vertical through prior knowledge/experience.

Lines 399-408

Although the results of the during-tilt session suggest the role of active body movements in the conscious perception of the gravitational direction, it remains unclear whether or how they influence the control of body orientation. Previous studies have shown an inconsistency between perceived and achieved body orientations when actively controlling body orientation [43,44]. This suggests that dynamic body movements may have different effects on the perception of gravitational direction and control of body orientation. On the other hand, some recent studies have demonstrated the contribution of dynamic somatosensory cues to active postural control (Misiaszek et al. 2016, 2017). Future research directly assessing the influence of dynamic arm movements on the achieved body orientation would be helpful for a better understanding of the mechanisms underlying the perception and control of body orientation in space.

Comment 3

It is widely assumed that the body is controlled relative to the direction of gravity, but this view is not universal. In fact, it has come under sustained criticism, mainly because body movement is not constrained directly (or solely) by the gravitational vector but, rather, by the sum of gravitational and inertial forces—the gravitoinertial force vector (e.g., Stoffregen & Riccio, 1988). In the present experiments, the gravitational and gravitorinertial force vectors were the same, and so the results cannot tell us whether participants were responding to one or the other. This limitation of the design should be noted in the Discussion. Similarly, clinical data from stroke patients do not permit the scientist to know which vector is detected.

Responses;

As the reviewer indicates, we used only a static tilt for SVV adjustments, and thus could not dissociate the gravitational and gravitoinertial force (GIF) vectors. Therefore, we cannot conclude whether the perceptual judgments of the gravitational vertical (SVV and SPV) resulted from the responses to either vector. This is a limitation of the present study. As suggested by a number of studies (e.g., Stoffregen & Riccio, 1988), the otolith system responds to the GIF but not solely to the gravitational force; the performance on SVV adjustments would be mainly derived from GIF. On the other hand, a previous study has demonstrated that the estimation of the earth-horizontal direction is influenced differently by whole-body tilt and body centrifugation, even though the GIF vector relative to the head was identical (Carriot et al., 2006). This finding suggests that gravitational force may specifically affect the perception of the gravitational direction. To address this, further studies are needed to dissociate the gravitational and GIF vectors. We have added this description to the text as a limitation of this study. Additionally, we have deleted the description of the relationship between postural control and perception of gravitational vertical in stroke patients from the introduction, since this assumption would not be definitive.

Changes;

Discussion

Lines 413-421

Second, we used a static whole-tilt for the SVV assessment in which the gravitational and gravitoinertial force (GIF) vectors were the same; therefore, it remains unknown whether participants responded to either force vectors. Since the otolith system responds to both gravitational and inertial forces [28], the visual vertical estimation reflects a response to the GIF. However, a previous study has shown that the estimation of the earth-horizontal direction is differently influenced by whole-body tilt and body centrifugation, even though the GIF vector relative to the head was identical [33]. This implies that the gravitational force may specifically affect the perception of gravitational direction. To address this, further studies are needed to dissociate the gravitational and GIF vectors.

Comment 4

The Introduction should be revised to state explicitly the hypotheses that were tested in the study. What testable predictions did the authors make? Similarly, the Discussion should be revised to re-state the predictions indicating, in each case, whether each prediction was (or was not) confirmed. The pattern of confirmed (vs. not confirmed) predictions should structure data interpretation.

Responses;

We agree with these comments. We had to explicitly state our hypotheses. As we have responded above (please see Comment 2), our hypothesis was that active body movements might also influence the subsequent perceptual estimates of the gravitational direction without body movements. To test this hypothesis, we evaluated whether static or dynamic arm movements during prolonged tilt influenced the perceptual judgments of visual or postural vertical. We predicted that the distorted estimate of the gravitational direction induced by prolonged tilt might be corrected based on additional cues generated by arm movements. Supporting our prediction, in the during-tilt session, the shifts of SVV were significantly attenuated by dynamic arm movements. We have revised the introduction and discussion sections for the readers’ better understanding of the aims and hypotheses of this study and our interpretation of the results.

Changes;

Introduction

Lines 80-94

Previous studies have shown that the body tilt-induced errors in the judgment of the head-referenced eye level considerably decreased when accompanied by arm movements during judgment [32,33]. This finding suggests that active body movements can improve the accuracy of spatial judgments, but it is unknown whether active body movements also influence the perceptual estimates of gravitational space not involving body movements. The CNS considers prior knowledge and experience as well as sensory signals to estimate the gravitational vertical [7-9], allowing us to hypothesize that additional cues generated by body movements may contribute to the subsequent perceptual estimates of the gravitational direction via prior knowledge and/or experience. To test this hypothesis, the present study evaluated whether static or dynamic arm movements during prolonged tilt influenced the perceptual judgments of visual vertical (Experiment 1) or postural vertical (Experiment 2). As mentioned above, the internal estimates of the gravitational direction are distorted during or after prolonged tilt, primarily due to sensory adaptation. We expected that these distorted estimates might be corrected based on additional cues generated by arm movements, resulting in the maintenance of SVV or SPV angles even after prolonged tilt.

Discussion

Lines 350-363

Extending previous findings that the accuracy in spatial judgment at the tilted position was considerably improved by accompanying arm movements during judgment [32,33], we hypothesized that active body movements could subsequently influence perceptual estimates of gravitational direction not involving body movements. Based on this hypothesis, we predicted that the perceptual distortion of the gravitational direction induced by prolonged tilt would decrease when active arm movements are performed in the tilt position. In support of our prediction, the results of the during-tilt session showed that the shifts of SVV toward the direction of prolonged tilt (Fig. 3, left panel) were attenuated when the participants performed dynamic arm movements during prolonged tilt (Fig. 4A). Prolonged tilt induces adaptive changes in the vestibular and body somatosensory systems [23,28], leading to a decrease in the sensed angles of the head and/or body relative to gravity [29]. The performance of arm movements against gravity provides supplemental cues such as proprioceptive feedback or efferent copy [30] for estimating head and/or body orientation in space. The CNS would likely recalibrate the internal estimates of the gravitational direction based on these information, resulting in the stable perceptual judgment of visual vertical through prior knowledge/experience.

Comment 5

Please revise so that the Results of Experiment 1 are presented before the Method of Experiment 2. That is, completely present Experiment 1, and then completely present Experiment 2.

Responses;

According to the reviewer’s suggestion, we have revised the text.

 

Reviewer #2

Comment 1

This interesting paper investigates dynamic arm movements as a new variable in the long search for the sensory determinants of the subjective vertical. The 'During Tilt' portion of Experiment 1 first re-demonstrates the known ability of prolonged tilt to bias the subjective visual vertical (SVV) towards the tilt, and then shows (as a new finding) that a series of dynamic arm movements during the tilt reduces this bias. The 'Post Tilt' portion of Experiment 1 shows that this bias reduction does not occur if the SVV is estimated after the participant is moved to a different tilt angle. This may be due to the timing between the prolonged tilt and the SVV estimation (as mentioned by the authors) but could also be due to the new tilt angle 'overwriting' the participant's sense of orientation. Experiment 2 shows that a subjective postural vertical estimation is not affected by the dynamic arm movements in the same manner as the SVV estimation is. The sample sizes are on the small side, as noted by the authors themselves, but the data analysis appears to be well done. I recommend some revisions as follows:

Responses;

We are deeply thankful for the reviewer’s helpful comments and advice. We have responded to all the comments and modified the text accordingly.

Comment 2

Lines 46-92

The introduction is not as thorough as I would expect in an otherwise well-written paper. Many of the references are grouped together with somewhat superficial descriptions, such as in Lines 49-51. There are very few references from the past 10 years, despite considerable recent research from several labs on the use of dynamic and movement cues on balance. The paper would benefit from a more substantive introduction, which could then be used to deepen the discussion of the results.

Responses;

Several recent studies have shown the involvement of dynamic cues in postural control (e.g., Misiaszerk et al. 2016). However, the purpose of our study was to clarify the mechanism underlying the perception of gravitational direction rather than postural control. As the other reviewer points out (please see #Reviewer 1 Comment 2), the achieved body direction when actively controlling the posture can differ from the perceived orientation. Given this, we have avoided describing the findings of postural control in the Introduction. On the other hand, as the reviewer indicated, our description in the Introduction was too superficial. Therefore, in the new version of the manuscript, we have described the underlying mechanism of the perception of the gravitational direction in more detail based on recent findings, and more explicitly stated our hypothesis in the Introduction. Moreover, we have mentioned the possible effect of arm movements on the control of body orientation based on the findings that dynamic somatosensory cues influence postural control in the Discussion.

Changes;

Introduction

Lines 46-52

Knowledge of the gravitational direction is fundamental to our action and perception of the earth. The direction of gravity cannot be directly sensed; instead, it is estimated in the brain based on several types of sensory information. Numerous psychophysical studies have demonstrated the involvement of visual [1-3], somatosensory [4-6], and vestibular sensory signals [3,7] in estimates of gravitational direction. Moreover, recent studies using computational modeling have shown that the central nervous system (CNS) weighs and combines these multisensory signals with prior knowledge and experience about the earth-vertical direction in a statistically optimal manner to resolve sensory ambiguity [7-9].

Lines 80-94

Previous studies have shown that the body tilt-induced errors in the judgment of the head-referenced eye level considerably decreased when accompanied by arm movements during judgment [32,33]. This finding suggests that active body movements can improve the accuracy of spatial judgments, but it is unknown whether active body movements also influence the perceptual estimates of gravitational space not involving body movements. The CNS considers prior knowledge and experience as well as sensory signals to estimate the gravitational vertical [7-9], allowing us to hypothesize that additional cues generated by body movements may contribute to the subsequent perceptual estimates of the gravitational direction via prior knowledge and/or experience. To test this hypothesis, the present study evaluated whether static or dynamic arm movements during prolonged tilt influenced the perceptual judgments of visual vertical (Experiment 1) or postural vertical (Experiment 2). As mentioned above, the internal estimates of the gravitational direction are distorted during or after prolonged tilt, primarily due to sensory adaptation. We expected that these distorted estimates might be corrected based on additional cues generated by arm movements, resulting in the maintenance of SVV or SPV angles even after prolonged tilt.

Discussion

Lines 399-408

Although the results of the during-tilt session suggest the role of active body movements in the conscious perception of the gravitational direction, it remains unclear whether or how they influence the control of body orientation. Previous studies have shown an inconsistency between perceived and achieved body orientations when actively controlling body orientation [43,44]. This suggests that dynamic body movements may have different effects on the perception of gravitational direction and control of body orientation. On the other hand, some recent studies have demonstrated the contribution of dynamic somatosensory cues to active postural control (Misiaszek et al. 2016, 2017). Future research directly assessing the influence of dynamic arm movements on the achieved body orientation would be helpful for a better understanding of the mechanisms underlying the perception and control of body orientation in space.

Comment 3

Lines 104-106

Was there a reason not to secure the participants’ arms by some mechanism that could be loosened/removed at the same time as the display frame was rotated to the left? If the arms were left unsecured then they will necessarily be pulled to the side by gravity when in a static roll, and this would provide an extra, potentially confounding sensory cue. This may have been a reason why the no-movement and static conditions did not significantly differ (Fig 4).

Responses;

Although the participants’ arms should have been restrained, we could not do this methodologically. As indicated by the reviewer, gravity would pull the arms to the side during prolonged tilt, which might provide a cue for the estimation of the gravitational direction. This is another limitation of the present study. We have described this as a limitation in the Discussion section.

Changes;

Discussion

lines 421-425

Third, the arms were not restrained to the body during prolonged tilt. In such a situation, gravity would have pulled the arms to the side, providing a static cue for the perception of the gravitational direction even when the arm movements were not performed (i.e., No-movement condition). This methodological limitation may be partially responsible for the lack of a significant difference in the SVV angles between the No-movement and Static conditions.

Comment 3

Lines 142-165, Lines 242-253

The term ‘trial’ appears to be used for two different types of event: a single instance of the participant setting the white line for SVV (as in line 148), as well as a set of ‘tilt, SVV, task, SVV’ (as in line 153). The explanation of the procedure would be clarified if two different terms were used.

Reponses;

We apologize for the inappropriate writing. To avoid confusion, we have applied the trial “trial” for a single SVV adjustment, and “sequence of experiment trials” for a set of trials in each condition in the new version of the manuscript.

Changes;

Materials and Methods

Lines 148

Figure 2A shows a sequence of experimental trials during the during-tilt session.

Lines 153-154

The participants performed five trials of the SVV adjustment within 40 seconds.

Lines 156-160

After the display portion was returned to the initial position (i.e., in front of the participant’s face), the shutter opened and the participants were asked to perform the SVV adjustments for five trials again. Each participant performed this sequence of experimental trials for each task condition, that is, 30 trials (three task conditions [No-movement, Static, Dynamic tasks] × 2 phases [before, after task] × 5 SVV adjustments) in total.

Lines 167-168

The shutter opened and the participants were asked to repeat the SVV adjustments for 5 trials.

Lines 171-173

Each participant performed this sequence of trials for each task condition in each final tilt position, i.e. 45 trials [3 task conditions (No-movement, Static, Dynamic tasks) × 3 final tilt positions (0°, ±4°) × 5 SVV adjustments] in total.

Comment 4

Line 159

What was the rationale for selecting to test at 4 degrees left, 0 degrees, and 4 degrees right? Would a larger tilt be expected to produce a larger effect?

Responses;

We apologize for this inadequate explanation. Our interest in the post-tilt session was to evaluate how arm movements during prolonged tilt attenuated the after-effect of prolonged tilt on SVV angles near upright. Based on a previous finding showing that approximately 4°is the threshold for the detection of body tilt relative to gravity (Bringoux et al. 2002, Neuropsychologia), we assumed that participants could recognize a body tilt at 4°, and used these angles. We have added the reason for the application of such small tilt angles to the text.

The results of the post-tilt session showed that the effect of dynamic arm movements on the SVV shifts tended to be larger (i.e., SVV shifts were more strongly attenuated) at a position closer to the initial tilt position (Fig. 5), probably due to the duration between the SVV and action tasks (as described in line 380-388). Given this, we expect to observe a greater effect of dynamic arm movements at a position (e.g., LSD 8°) closer to the prolonged tilt position.

Changes;

Materials and Methods

Lines 145-146

These angles were determined based on the fact that 4° is the threshold for the detection of body tilt in the roll plane [35].

Comment 5

Lines 160-162

It was not clear to me why the 'Post Tilt' experimental procedure ends with moving the participant to 16 degrees right and then to the start position. These tilts happen after the SVV estimations are made, so are they necessary? If they are necessary for the 'Post Tilt' procedure, why are they not done at the end of the 'During Tilt' procedure?

Responses;

In the post-tilt session, we set three final tilt positions. If the participants were tilted back to the upright position directly from each position after the SVV task, the tilt motion would provide a cue about the final tilt position, which could affect the performance in subsequent trials. To prevent this as much as possible, the participants were returned to the upright position via the RSD 16° position. In the during-tilt session, only one body tilt angle was used; therefore, we did not specifically consider this feedback. If multiple tilt directions and angles were used in the during-tilt session, we inserted a tilt position before returning to upright, as in the post-tilt session. To convey this point more clearly, we have corrected the description of the reason for using RSD 16°in the text.

Changes;

Materials and Methods

Lines 168-170

After completing the task, the body was returned to the upright position via the RSD 16° position to avoid providing feedback about the final tilt position that could influence the subsequent performance on the SVV adjustment.

Comment 6

Lines 378-382

The lack of effect of dynamic arm movements on SVV estimation in the 4 degree Right position for the ‘Post Tilt’ procedure is explained as a result of a small sample size. This may be true, but it may also represent an effect of always using a prolonged left tilt at the start of the experiment. What would happen if the initial tilt was to the right instead?

Responses;

The results in the post-tilt session show a lack of significant effect of dynamic arm movements, not for only RSD 4°, but also for LSD 4° and 0° (please see Fig. 5). However, the effect of arm movements tended to be smaller for the RSD 4° position than for the other positions (although not statistically significant). As indicated by the reviewer, the tilt direction used for prolonged tilt would have contributed to this. The involvement of the additional information generated by arm movements in the internal estimates of the gravitational direction presumably decays with time (as described in lines 380-388). Because the time duration between the SVV and action tasks was longer in RSD 4° than in LSD 4°, the effect of dynamic arm movements may have been less observed in RSD 4° position. We speculate that if the side of prolonged tilt was right, the effect of dynamic arm movements would be larger in RSD 4° than in LSD 4°. We have not specifically stated this because it is speculative. Instead, we have mentioned that the dependency of the effect of dynamic arm movements on final tilt positions may be due to the duration between the SVV and action tasks. In conclusion, we have stated the necessity of evaluating the effect of dynamic arm movements using different tilt directions and angles in the future.

Changes;

Discussion

Lines 388-390

In favor of this assumption, the attenuation effect of dynamic arm movements on SVV shifts appears to be greater at positions closer to the initial tilt position, where the interval between the action task and SVV adjustment was shorter.

Conclusion

Lines 433-438

To provide a comprehensive understanding of the relationship between action and the perception of the gravitational space, we need to further examine how performance in the estimation of the gravitational direction is influenced by the manipulation of temporal (e.g., arm movement velocity, interval between arm movements, and perceptual task) and spatial properties (e.g., direction and angle of arm movements or body tilt).

Comment 7

Figure 1:

This figure appears to be added to show how the display rotates in yaw away from the participant. I found it confusing at first, because I was expecting an image showing the roll rotation used in the experiment. Perhaps the figure could be updated to show both of these features.

Responses;

We apologize for the confusing depictions. We have modified the figure to better depict our experimental setup and added a sentence to the figure caption.

Changes;

Figure caption (Fig.1)

This figure illustrates a situation in which the participants were tilted leftward. The display portion was rotated in yaw, as denoted by a gray arrow.

Comment 8

Figure 3:

Why is the SVV angle for the control in the +4 RSD group so different from the controls in the +4 LSD and 0 degrees groups? I would think that all three groups would have very similar values on the control.

Responses;

As pointed out by the reviewer, SVV angles for the Control condition appear to be larger at RSD 4° than at LSD 4° and 0°. However, since our additional analysis showed no significant difference in SVV angles for the Control condition between these positions, we cannot conclude the larger SVV errors specifically for the RSD 4° position. Although we cannot exactly explain the reason for the tendency (not statistically significant), this may reflect the structural and functional properties of otolith organs given that the CNS would weigh more heavily on otolith signals for the SVV adjustments near upright than somatosensory signals (Clemens et al. 2011). Since this assumption is speculative, we have not specifically described this in the text. Instead, we have added the statistical results showing no significant difference in the angle of SVV for the control condition between the final tilt positions.

Changes;

Discussion

Lines 232-237

For the post-tilt session, the median SVV angles (1st, 3rd quartiles) in the Control and No-movement conditions were -1.0° (-1.5, 0.7) and -2.7° (-6.0, -0.4) for the LSD 4° position, -1.5° (-2.5, 0.5), and -3° (-5.6, -0.9) for the 0° position, and -3.5° (-6.5, -1.5) and -4.0° (-8.6, -1.8) for the 4° RSD position. The SVV angles for the Control condition were not significantly different between the final tilt positions (Friedman test; main effect χ2 = 2.07; p = 0.36).

Comment 9

Figure 3:

Why is the variability so much larger for the +4 RSD group, compared to the +4 LSD and 0 degrees groups?

Responses;

The inter-individual variability in the SVV angles appeared to be larger for the RSD 4°position than for the other positions. Unfortunately, as with Comment 7, we cannot explain the reason for this based on our data. The characteristics of the otolith function may also contribute to this. We have not specifically stated this in the text because it is too speculative. We need to address this issue in future studies.

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Decision Letter 1

Thomas A Stoffregen

15 Apr 2021

Dynamic arm movements attenuate the perceptual distortion of visual vertical induced during prolonged whole-body tilt

PONE-D-20-40610R1

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Acceptance letter

Thomas A Stoffregen

22 Apr 2021

PONE-D-20-40610R1

Dynamic arm movements attenuate the perceptual distortion of visual vertical induced during prolonged whole-body tilt

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