Mismatch of Visual-Vestibular Information in Virtual Reality: Is Motion Sickness Part of the Brains Attempt to Reduce the Prediction Error?

Visually induced motion sickness (VIMS) is a relevant limiting factor in the use of virtual reality (VR) devices. Understanding the origin of this problem might help to develop strategies to circumvent this limitation. Previous studies have attributed VIMS to a mismatch between visual, and vestibular information, causing ambiguity of the position of the body in relation to its surrounding. Studies using EEG have shown a shift of the power spectrum to lower frequencies while VIMS is experienced. However, little is known about the relationship between the intensity of the VIMS and the changes in these power spectra. Moreover, the effect of different varieties of VIMS on the causal relationship between brain areas is largely unknown. Here, we used EEG to study 14 healthy subjects in a VR environment who were exposed to increasing levels of mismatch between vestibular and visual information. The frequency power and the bivariate transfer entropy as a measure for the information transfer were calculated. We found a direct association between increasing mismatch levels and subjective VIMS. With increasing VIMS, the proportion of slow EEG waves (especially 1–10 Hz) increases, especially in temporo-occipital regions. Furthermore, we found a general decrease in the information flow in most brain areas but especially in brain areas involved in the processing of vestibular signals and the detection of self-motion. We hypothesize that the general shift of frequency power and the decrease in information flow while experiencing high intensity VIMS represent a brain state of a reduced ability to receive, transmit and process information. We further hypothesize that the mechanism of reduced information flow is a general reaction of the brain to an unresolvable mismatch of information. This reaction aims on transforming a currently unstable model with a high prediction error into a stable model in an environment of minimal contradictory information.

Delineating neural responses and functional connectivity changes during vestibular and nociceptive stimulation reveal the uniqueness of cortical vestibular processing

Vestibular information is ubiquitous and often processed jointly with visual, somatosensory and proprioceptive information. Among the cortical brain regions associated with human vestibular processing, area OP2 in the parietal operculum has been proposed as vestibular core region. However, delineating responses uniquely to vestibular stimulation in this region using neuroimaging is challenging for several reasons: First, the parietal operculum is a cytoarchitectonically heterogeneous region responding to multisensory stimulation. Second, artificial vestibular stimulation evokes confounding somatosensory and nociceptive responses blurring responses contributing to vestibular perception. Furthermore, immediate effects of vestibular stimulation on the organization of functional networks have not been investigated in detail yet. Using high resolution neuroimaging in a task-based and functional connectivity approach, we compared two equally salient stimuli—unilateral galvanic vestibular (GVS) and galvanic nociceptive stimulation (GNS)—to disentangle the processing of both modalities in the parietal operculum and characterize their effects on functional network architecture. GNS and GVS gave joint responses in area OP1, 3, 4, and the anterior and middle insula, but not in area OP2. GVS gave stronger responses in the parietal operculum just adjacent to OP3 and OP4, whereas GNS evoked stronger responses in area OP1, 3 and 4. Our results underline the importance of considering this common pathway when interpreting vestibular neuroimaging experiments and underpin the role of area OP2 in central vestibular processing. Global network changes were found during GNS, but not during GVS. This lack of network reconfiguration despite the saliency of GVS may reflect the continuous processing of vestibular information in the awake human.

Vestibular-Evoked Cerebral Potentials

The human vestibular cortex has mostly been approached using functional magnetic resonance imaging and positron emission tomography combined with artificial stimulation of the vestibular receptors or nerve. Few studies have used electroencephalography and benefited from its high temporal resolution to describe the spatiotemporal dynamics of vestibular information processing from the first milliseconds following vestibular stimulation. Evoked potentials (EPs) are largely used to describe neural processing of other sensory signals, but they remain poorly developed and standardized in vestibular neuroscience and neuro-otology. Yet, vestibular EPs of brainstem, cerebellar, and cortical origin have been reported as early as the 1960s. This review article summarizes and compares results from studies that have used a large range of vestibular stimulation, including natural vestibular stimulation on rotating chairs and motion platforms, as well as artificial vestibular stimulation (e.g., sounds, impulsive acceleration stimulation, galvanic stimulation). These studies identified vestibular EPs with short latency (<20 ms), middle latency (from 20 to 50 ms), and late latency (>50 ms). Analysis of the generators (source analysis) of these responses offers new insights into the neuroimaging of the vestibular system. Generators were consistently found in the parieto-insular and temporo-parietal junction—the core of the vestibular cortex—as well as in the prefrontal and frontal areas, superior parietal, and temporal areas. We discuss the relevance of vestibular EPs for basic research and clinical neuroscience and highlight their limitations.

Understanding Vestibular Information Processing in Velocity-Storage Circuit and Application to Interpreting Clinical Manifestation of Vestibular Disorders

The velocity-storage circuit comprised of bilateral vestibular nucleus complexes, commissural fiber, and nodulus and uvula functions in refining the raw vestibular signal to estimate rotational velocity, gravity direction, and inertia. In this review, we pursued the functional significance of this velocity-storage circuit and how this physiologic knowledge could help us understand the clinical symptoms and signs of patients with vestibular disorders.

Effects of vestibular stimulation on gait stability and variability

Vestibular information modulates muscle activity during gait, presumably to contribute stability, because noisy electrical vestibular stimulation perturbs gait stability. An important mechanism to stabilize gait in the mediolateral direction is to coordinate foot placement based on a sensory estimate of the trunk center of mass state, to which vestibular information appears to contribute. We, therefore expected that noisy vestibular stimulation would decrease the correlation between foot placement and trunk center of mass state. Moreover, as vestibular modulation of muscle activity during gait depends on step width, we expected stronger effects for narrow-base than normal walking, and smaller effects for wide-base walking. In eleven healthy subjects we measured the kinematics of the trunk (as a proxy of the center of mass), and feet, while they walked on a treadmill in six conditions, including three different step widths: control (preferred step width), narrow-base (steps smaller than hip width), and wide-base (with steps greater than hip width). The three conditions were conducted with and without a bipolar electrical stimulus, applied behind the ears (5 mA). Walking with EVS reduced gait stability but increased the foot placement to center of mass correlation in different step width conditions. The narrow-base walking was the most stable condition and showed a stronger correlation between foot placement and center of mass state. We argue that EVS destabilized gait, but that this was partially compensated for by tightened control over foot placement, which would require successful use of other than vestibular sensory inputs, to estimate center of mass movement.

Rate of infant carrying impacts infant spontaneous motor tempo

Rhythm production is a critical component of human interaction, not least forming the basis of our musicality. Infants demonstrate a spontaneous motor tempo (SMT), or natural rate of rhythmic movement. Here, we ask whether infant SMT is influenced by the rate of locomotion infants experience when being carried. Ten-month-old, non-walking infants were tested using a free drumming procedure before and after 10 min of being carried by an experimenter walking at a slower (98 BPM) or faster (138 BPM) than average tempo. We find that infant SMT is differentially impacted by carrying experience dependent on the tempo at which they were carried: infants in the slow-walked group exhibited a slower SMT from pre-test to post-test, while infants in the fast-walked group showed a faster SMT from pre-test to post-test. Heart rate data suggest that this effect is not due to a general change in the state of arousal. We argue that being carried during caregiver locomotion is a predominant experience for infants throughout the first years of life, and as a source of regular, vestibular, information, may at least partially form the basis of their sense of rhythm.

Overcoming navigational challenges: A novel approach to the study and assessment of topographical orientation

Several studies investigating environmental navigation require participants to navigate in virtual environments, in which the proprioceptive and vestibular components present during real environmental navigation are lost. Here, we aimed to provide a novel computerized ecological navigational battery, investigating whether the absence of proprioceptive and vestibular inputs yields a representation of the navigational space comparable to that acquired ecologically. In Study 1, 38 participants underwent two sets of tasks, one performed in a laboratory-based setting (LBS) and the other in an ecological environment (EE), with both including evaluation of route, landmark, and survey knowledge and a landmark ordering task. All tasks, except the route task, significantly correlated between EE and LBS. In LBS, performance in the landmark ordering task was predicted by that in the survey task, but not by those in the route and landmark tasks. Results of Study 1 were replicated in Study 2, in which 44 participants completed a modified and shorter online version of LBS tests. Reliability of the online LBS tests was also tested and showed a moderate-to-high internal consistency. Overall, results show that the conditions in which tasks are performed affect the acquisition of route knowledge, likely due to the lack of proprioceptive and vestibular information in LBS. However, LBS tasks presented here provide a standard battery of tests that can overcome the replicability problems encountered by ecological navigation tests, while taking into consideration all the complexities of navigational processes in terms of the use of landmark, route, and survey strategies.

Haptic awareness changes when lying down

Accurate localization of touch requires the integration of two reference frames—an internal (e.g., anatomical) and an external (e.g., spatial). Using a tactile temporal order judgement task with the hands crossed over the midline, we investigated the integration of these two reference frames. We manipulated the reliability of the visual and vestibular information, both of which contribute to the external reference frame. Visual information was manipulated between experiments (Experiment 1 was done with full vision and Experiment 2 was done while wearing a blindfold). Vestibular information was manipulated in both experiments by having the two groups of participants complete the task in both an upright posture and one where they were lying down on their side. Using a Bayesian hierarchical model, we estimated the perceptual weight applied to these reference frames. Lying participants on their side reduced the weight applied to the external reference frame and produced a smaller deficit; blindfolding resulted in similar reductions. These findings reinforce the importance of the visual system when weighting tactile reference frames, and highlight the importance of the vestibular system in this integration.

Delineating Neural Responses and Functional Connectivity Changes During Vestibular and Nociceptive Stimulation Reveal the Uniqueness of Cortical Vestibular Processing

Vestibular information is ubiquitous and often processed jointly with visual, somatosensory and proprioceptive information. Among the cortical brain regions associated with human vestibular processing, area OP2 in the parietal operculum has been proposed as vestibular core region. However, delineating responses uniquely to vestibular stimulation in this region using neuroimaging is challenging for several reasons: Firstly, the parietal operculum is a cytoarchitectonically heterogeneous region responding to multisensory stimulation. Secondly, artificial vestibular stimulation evokes confounding somatosensory and nociceptive responses blurring responses contributing to vestibular perception. Furthermore, immediate effects of vestibular stimulation on the organization of functional networks have not been investigated in detail yet.Here, we compared two equally salient stimuli - galvanic vestibular stimulation (GVS) and galvanic nociceptive stimulation (GNS)- to disentangle the processing of both modalities in the parietal operculum and characterize their effects on functional network architecture. GNS and GVS gave joint responses in area OP1,3,4, and the anterior and middle insula, but not in area OP2. Contrasting both stimulation modalities resulted in stronger responses in parts of the parietal operculum adjacent to OP3 and OP4 during GVS, whereas GNS evoked stronger responses in area OP1,3 and 4. Our results underline the importance of considering this common multisensory trunk when interpreting vestibular neuroimaging experiments and further underpin the role of area OP2 in central vestibular processing. Global network changes were found during GNS, but not during GVS. This lack of network reconfiguration despite the saliency of GVS may reflect the continuous processing of vestibular information in the awake human.

Effects of Linear Visual-Vestibular Conflict on Presence, Perceived Scene Stability and Cybersickness in the Oculus Go and Oculus Quest

Humans rely on multiple senses to perceive their self-motion in the real world. For example, a sideways linear head translation can be sensed either by lamellar optic flow of the visual scene projected on the retina of the eye or by stimulation of vestibular hair cell receptors found in the otolith macula of the inner ear. Mismatches in visual and vestibular information can induce cybersickness during head-mounted display (HMD) based virtual reality (VR). In this pilot study, participants were immersed in a virtual environment using two recent consumer-grade HMDs: the Oculus Go (3DOF angular only head tracking) and the Oculus Quest (6DOF angular and linear head tracking). On each trial they generated horizontal linear head oscillations along the interaural axis at a rate of 0.5 Hz. This head movement should generate greater sensory conflict when viewing the virtual environment on the Oculus Go (compared to the Quest) due to the absence of linear tracking. We found that perceived scene instability always increased with the degree of linear visual-vestibular conflict. However, cybersickness was not experienced by 7/14 participants, but was experienced by the remaining participants in at least one of the stereoscopic viewing conditions (six of whom also reported cybersickness in monoscopic viewing conditions). No statistical difference in spatial presence was found across conditions, suggesting that participants could tolerate considerable scene instability while retaining the feeling of being there in the virtual environment. Levels of perceived scene instability, spatial presence and cybersickness were found to be similar between the Oculus Go and the Oculus Quest with linear tracking disabled. The limited effect of linear coupling on cybersickness, compared with its strong effect on perceived scene instability, suggests that perceived scene instability may not always be associated with cybersickness. However, perceived scene instability does appear to provide explanatory power over the cybersickness observed in stereoscopic viewing conditions.