Self-motion Perception Research Articles

Ventral and dorsal streams processing visual motion perception (FDG-PET study).

BackgroundEarlier functional imaging studies on visually induced self-motion perception (vection) disclosed a bilateral network of activations within primary and secondary visual cortex areas which was combined with signal decreases, i.e., deactivations, in multisensory vestibular cortex areas. This finding led to the concept of a reciprocal inhibitory interaction between the visual and vestibular systems. In order to define areas involved in special aspects of self-motion perception such as intensity and duration of the perceived circular vection (CV) or the amount of head tilt, correlation analyses of the regional cerebral glucose metabolism, rCGM (measured by fluorodeoxyglucose positron-emission tomography, FDG-PET) and these perceptual covariates were performed in 14 healthy volunteers. For analyses of the visual-vestibular interaction, the CV data were compared to a random dot motion stimulation condition (not inducing vection) and a control group at rest (no stimulation at all).ResultsGroup subtraction analyses showed that the visual-vestibular interaction was modified during CV, i.e., the activations within the cerebellar vermis and parieto-occipital areas were enhanced. The correlation analysis between the rCGM and the intensity of visually induced vection, experienced as body tilt, showed a relationship for areas of the multisensory vestibular cortical network (inferior parietal lobule bilaterally, anterior cingulate gyrus), the medial parieto-occipital cortex, the frontal eye fields and the cerebellar vermis. The “earlier” multisensory vestibular areas like the parieto-insular vestibular cortex and the superior temporal gyrus did not appear in the latter analysis. The duration of perceived vection after stimulus stop was positively correlated with rCGM in medial temporal lobe areas bilaterally, which included the (para-)hippocampus, known to be involved in various aspects of memory processing. The amount of head tilt was found to be positively correlated with the rCGM of bilateral basal ganglia regions responsible for the control of motor function of the head.ConclusionsOur data gave further insights into subfunctions within the complex cortical network involved in the processing of visual-vestibular interaction during CV. Specific areas of this cortical network could be attributed to the ventral stream (“what” pathway) responsible for the duration after stimulus stop and to the dorsal stream (“where/how” pathway) responsible for intensity aspects.

Tuning Self-Motion Perception in Virtual Reality with Visual Illusions

Motion perception in immersive virtual environments significantly differs from the real world. For example, previous work has shown that users tend to underestimate travel distances in virtual environments (VEs). As a solution to this problem, researchers proposed to scale the mapped virtual camera motion relative to the tracked real-world movement of a user until real and virtual motion are perceived as equal, i.e., real-world movements could be mapped with a larger gain to the VE in order to compensate for the underestimation. However, introducing discrepancies between real and virtual motion can become a problem, in particular, due to misalignments of both worlds and distorted space cognition. In this paper, we describe a different approach that introduces apparent self-motion illusions by manipulating optic flow fields during movements in VEs. These manipulations can affect self-motion perception in VEs, but omit a quantitative discrepancy between real and virtual motions. In particular, we consider to which regions of the virtual view these apparent self-motion illusions can be applied, i.e., the ground plane or peripheral vision. Therefore, we introduce four illusions and show in experiments that optic flow manipulation can significantly affect users' self-motion judgments. Furthermore, we show that with such manipulations of optic flow fields the underestimation of travel distances can be compensated.

Where is straight ahead to a patient with unilateral vestibular loss?

The vestibular system is classically associated with postural control, oculomotor reflexes and self-motion perception. The patients with vestibular loss are primarily concerned with balance and gait problems including head and trunk tilt and walking trajectory deviation to the lesioned side. These long-lasting postural and locomotor biases are thought to originate from changes in spatial perception of self. Indeed, we show here that vestibular cues are necessary for an accurate representation of body orientation. Patients with right (RVN; n=11) or left vestibular neurotomy (LVN; 9) as a treatment for Menière’s disease were compared with 10 healthy controls. The subjective straight ahead (SSA) was investigated using a method disentangling lateral shift and tilt components of error. In the horizontal plane, subjects were required to align a rod with their body midline. In the frontal plane, they were asked to align the rod with the midline of head or trunk. The analysis of SSA clearly showed distinct results according to the side of the lesion. The LVN patients had a contralesional lateral shift of SSA. In addition, they showed an ipsilesional tilt, more severe for the head than for the trunk. By contrast, in RVN patients, the representation of the body midline was fairly accurate in both the horizontal and frontal planes and did not differ from that of control subjects. The present study shows deviations in body orientation representation after unilateral vestibular loss. Deviations are observed in the horizontal as well as in the frontal planes. Interestingly, only patients with left vestibular loss were concerned with these changes in perception of self-orientation in space. These data support the hypothesis of an asymmetric vestibular function in healthy subjects and confirm the similarity of functional disorders in patients with vestibular deficits or spatial neglect. For the first time, this similarity is found at the level of body representation.

Is Vestibular Self-Motion Perception Controlled by the Velocity Storage? Insights from Patients with Chronic Degeneration of the Vestibulo-Cerebellum

BackgroundThe rotational vestibulo-ocular reflex (rVOR) generates compensatory eye movements in response to rotational head accelerations. The velocity-storage mechanism (VSM), which is controlled by the vestibulo-cerebellar nodulus and uvula, determines the rVOR time constant. In healthy subjects, it has been suggested that self-motion perception in response to earth-vertical axis rotations depends on the VSM in a similar way as reflexive eye movements. We aimed at further investigating this hypothesis and speculated that if the rVOR and rotational self-motion perception share a common VSM, alteration in the latter, such as those occurring after a loss of the regulatory control by vestibulo-cerebellar structures, would result in similar reflexive and perceptual response changes. We therefore set out to explore both responses in patients with vestibulo-cerebellar degeneration.Methodology/Principal FindingsReflexive eye movements and perceived rotational velocity were simultaneously recorded in 14 patients with chronic vestibulo-cerebellar degeneration (28–81yrs) and 12 age-matched healthy subjects (30–72yrs) after the sudden deceleration (90°/s2) from constant-velocity (90°/s) rotations about the earth-vertical yaw and pitch axes. rVOR and perceived rotational velocity data were analyzed using a two-exponential model with a direct pathway, representing semicircular canal activity, and an indirect pathway, implementing the VSM. We found that VSM time constants of rVOR and perceived rotational velocity co-varied in cerebellar patients and in healthy controls (Pearson correlation coefficient for yaw 0.95; for pitch 0.93, p<0.01). When constraining model parameters to use the same VSM time constant for rVOR and perceived rotational velocity, moreover, no significant deterioration of the quality of fit was found for both populations (variance-accounted-for >0.8).Conclusions/SignificanceOur results confirm that self-motion perception in response to rotational velocity-steps may be controlled by the same velocity storage network that controls reflexive eye movements and that no additional, e.g. cortical, mechanisms are required to explain perceptual dynamics.

Effect of Haptic Supplementation Provided by a Fixed or Mobile Stick on Postural Stabilization in Elderly People

Background: Haptic supplementation by a light touch with the index finger on a stable surface has been widely shown to increase postural stability. With a view to a potential application in the domain of mobility aids, it should, however, be demonstrated that haptic supplementation is effective even if provided by a mobile support. Objective: The present experiment aimed at determining whether haptic supplementation was effective in elderly people when provided by a light grip on an unstable stick support. Methods: Ten young and 11 older adults were tested in an upright position in 6 experimental conditions, in which the mobility of the stick support and its resistance to body sway were manipulated. Classical center-of-pressure (COP) variables (i.e. root mean square variability, range and area) were computed together with power spectral analysis and stabilogram diffusion analysis (SDA) variables of COP. Results: The results suggest that the stabilizing effect of haptic supplementation is independent of age and the nature of the support (fixed or mobile) when transient sway-related contact forces at the fingertip and proprioceptive cues are of sufficient magnitude. The results also indicate that haptic supplementation attenuates the age-related increase in energy consumption during the postural task even in the mobile support condition on a low-resistance surface. The results of SDA suggest that the availability of sway-related haptic cues reduces reliance on increased muscle activity around the ankle over short time intervals of postural control. After some time, haptic supplementation eventually leads to well-coordinated postural corrections. Conclusions: In summary, haptic supplementation improves postural control mechanisms independent of age due to enhanced perception of self-motion through sensory interaction with the environment.

Neural correlates of oddball detection in self-motion heading: A high-density event-related potential study of vestibular integration

The perception of self-motion is a product of the integration of information from both visual and non-visual cues, to which the vestibular system is a central contributor. It is well documented that vestibular dysfunction leads to impaired movement and balance, dizziness and falls, and yet our knowledge of the neuronal processing of vestibular signals remains relatively sparse. In this study, high-density electroencephalographic recordings were deployed to investigate the neural processes associated with vestibular detection of changes in heading. To this end, a self-motion oddball paradigm was designed. Participants were translated linearly 7.8 cm on a motion platform using a one second motion profile, at a 45° angle leftward or rightward of straight ahead. These headings were presented with a stimulus probability of 80-20 %. Participants responded when they detected the infrequent direction change via button-press. Event-related potentials (ERPs) were calculated in response to the standard (80 %) and target (20 %) movement directions. Statistical parametric mapping showed that ERPs to standard and target movements differed significantly from 490 to 950 ms post-stimulus. Topographic analysis showed that this difference had a typical P3 topography. Individual participant bootstrap analysis revealed that 93.3 % of participants exhibited a clear P3 component. These results indicate that a perceived change in vestibular heading can readily elicit a P3 response, wholly similar to that evoked by oddball stimuli presented in other sensory modalities. This vestibular-evoked P3 response may provide a readily and robustly detectable objective measure for the evaluation of vestibular integrity in various disease models.

Characteristics and classification of hippocampal theta rhythm induced by passive translational displacement

Theta rhythms in the hippocampus are believed to be the “metric” relating to various behavior patterns for free roaming rats. In this study, the theta rhythms were studied while rats either walked or were passively translated by a toy car on a linear track (referred to as WALK and TRANS respectively). For the similar running speeds in WALK and TRANS conditions, theta frequency and amplitude were both reduced during TRANS. Theta modulation of pyramidal cells during TRANS was reduced compared to that during WALK. Theta frequency was positively correlated with translation speed during TRANS. Theta rhythm remained apparent during TRANS and WALK after large dose of atropine sulfate (blocking the cholinergic pathway) was injected compared to still states. The present study demonstrated the patterns of theta rhythm induced by passive translation in rats and suggested that the Type I theta rhythm could occur during non-voluntary locomotion. We further argued that the perception of actual self-motion may be the underlying mechanism that initiates and modulates type I theta.

Directional Asymmetries and Age Effects in Human Self-Motion Perception

Directional asymmetries in vestibular reflexes have aided the diagnosis of vestibular lesions; however, potential asymmetries in vestibular perception have not been well defined. This investigation sought to measure potential asymmetries in human vestibular perception. Vestibular perception thresholds were measured in 24 healthy human subjects between the ages of 21 and 68 years. Stimuli consisted of a single cycle of sinusoidal acceleration in a single direction lasting 1 or 2 s (1 or 0.5 Hz), delivered in sway (left-right), surge (forward-backward), heave (up-down), or yaw rotation. Subject identified self-motion directions were analyzed using a forced choice technique, which permitted thresholds to be independently determined for each direction. Non-motion stimuli were presented to measure possible response bias. A significant directional asymmetry in the dynamic response occurred in 27% of conditions tested within subjects, and in at least one type of motion in 92% of subjects. Directional asymmetries were usually consistent when retested in the same subject but did not occur consistently in one direction across the population with the exception of heave at 0.5 Hz. Responses during null stimuli presentation suggested that asymmetries were not due to biased guessing. Multiple models were applied and compared to determine if sensitivities were direction specific. Using Akaike information criterion, it was found that the model with direction specific sensitivities better described the data in 86% of runs when compared with a model that used the same sensitivity for both directions. Mean thresholds for yaw were 1.3±0.9°/s at 0.5 Hz and 0.9±0.7°/s at 1 Hz and were independent of age. Thresholds for surge and sway were 1.7±0.8 cm/s at 0.5 Hz and 0.7±0.3 cm/s at 1.0 Hz for subjects <50 and were significantly higher in subjects >50 years old. Heave thresholds were higher and were independent of age.

Human discrimination of translational accelerations

Human perception of self-motion is the result of combining information from many sensory systems such as visual, vestibular, and proprioceptive systems. Research on vestibular thresholds has mainly focused on estimating absolute thresholds for translational and rotational motions and estimating difference thresholds for rotational velocities. In this study, psychophysical methods are used to determine the ability of normal subjects to discriminate among sinusoidal accelerations in the horizontal plane. Difference thresholds were estimated using four different acceleration amplitudes ranging from peak amplitude of 0.5-2.0 m/s2 and three different frequencies ranging from 0.25 to 0.6 Hz. Difference thresholds ranged from 0.05 m/s2 for a sinusoidal acceleration with peak amplitude of 0.5 to 0.13 m/s2 for a sinusoidal acceleration with peak amplitude of 2.0 m/s2. The relationship between difference threshold estimates and peak accelerations is found to compare favorably to Weber's law, which is often used to represent changes in threshold values in other sensory systems. Moreover, the threshold estimates tend to decrease as frequency increases. The effect of visual condition on thresholds was also investigated. It was shown that when the visual scene is stationary with respect to the subject, there are no significant differences between threshold estimates based on closed-eye and open-eye scenarios.

Social, societal, and economic burden of mal de debarquement syndrome

Mal de debarquement syndrome (MdDS) is a disorder of phantom perception of self-motion of unknown cause. The purpose of this work was to describe the quality of life (QOL) of patients with MdDS and to estimate the economic costs associated with this disorder. A modified version of a QOL survey used for another neurological disease (multiple sclerosis; MSQOL-54) was used to assess the impact of MdDS on QOL in 101 patients. The estimated economic costs were based on self-reported direct and indirect costs of individuals living in the United States using Medicare reimbursement payment rates for 2011 in 79 patients. Patients with MdDS reported a poor overall QOL as indicated by a mean composite QOL score of 59.26 ± 1.89 (out of 100). The subcategories having the lowest QOL rating were role limitations due to physical problems (18.32 ± 3.20), energy (34.24 ± 1.47), and emotional problems (36.30 ± 4.00). The overall physical health composite score including balance was 49.40 ± 1.69, and the overall mental health composite score was 52.40 ± 1.83. The cost to obtain a diagnosis was $2,997 ± 337, which included requiring an average of 19 physician visits per patient. The direct cost of MdDS medical care was $826 ± 140 per patient per year, which mainly included diagnostic imaging and physician visits. The indirect costs (i.e., lost wages) were $9,781 ± 2,347 per patient per year. Among 65 patients who were gainfully employed when they acquired MdDS, the indirect costs were $11,888 ± 2,786 per patient per year. Thus, the total annual cost of the disorder ranged from $11,493 ± 2,341 to $13,561 ± 2,778 per patient per year depending on employment status prior to developing MdDS. MdDS negatively and dramatically impacts QOL, and also imposes a substantial economic burden on MdDS patients. These findings underscore the need for further basic and clinical research on MdDS.

The structure of self-experience during visuo–tactile stimulation of a virtual and the physical body

The simultaneous visuo–tactile stimulation of an individual’s body and a virtual body (avatar) is an experimental method used to investigate the mechanisms of self-experience. Studies incorporating this method found that it elicits the experience of bodily ownership over the avatar. Moreover, as part of our own research we found that it also has an effect on the experience of agency, spatial presence, as well as on the perception of self-motion, and thus on self-localization. However, it has so far not been investigated whether these effects represent distinct categories within conscious experience. We stroked the back of 21 male participants for three minutes while they watched an avatar getting synchronously stroked within a virtual city in a head-mounted display setup. Subsequently, we assessed their avatar and their spatial presence experience with 23 questionnaire items. The analysis of the responses to all items by means of nonmetric multidimensional scaling resulted in a two-dimensional map (stress = 0.151) on which three distinct categories of items could be identified: a cluster (Cronbach’s alpha = 0.89) consisting of all presence items, a cluster (Cronbach’s alpha = 0.88) consisting of agency-related items, and a cluster (Cronbach’s alpha = 0.93) consisting of items related to body ownership as well as self-localization. The reason that spatial presence formed a distinct category could be that body ownership, self-localization and agency are not reported in relation to space. Body ownership and self-localization belonged to the same category which we named identification phenomena. Hence, we propose the following three higher-order categories of self-experience: identification, agency, and spatial presence.

Linear Path Integration Deficits in Patients with Abnormal Vestibular Afference

Effective navigation requires the ability to keep track of one's location and maintain orientation during linear and angular displacements. Path integration is the process of updating the representation of body position by integrating internally-generated self-motion signals over time (e.g., walking in the dark). One major source of input to path integration is vestibular afference. We tested patients with reduced vestibular function (unilateral vestibular hypofunction, UVH), patients with aberrant vestibular function (benign paroxysmal positional vertigo, BPPV), and healthy participants (controls) on two linear path integration tasks: experimenter-guided walking and target-directed walking. The experimenter-guided walking task revealed a systematic underestimation of self-motion signals in UVH patients compared to the other groups. However, we did not find any difference in the distance walked between the UVH group and the control group for the target-directed walking task. Results from neuropsychological testing and clinical balance measures suggest that the errors in experimenter-guided walking were not attributable to cognitive and/or balance impairments. We conclude that impairment in linear path integration in UVH patients stem from deficits in self-motion perception. Importantly, our results also suggest that patients with a UVH deficit do not lose their ability to walk accurately without vision to a memorized target location.

Emotional Sounds Influence Vertical Vection

While viewing a large vertically moving sinusoidal luminance grating, the perception of upward self-motion (vection) was modulated by positive sounds (e.g., a baby's laughter). This may be because positive emotion and the spatial metaphor of vertical directions were unified in the mind.

Perceptually Plausible Sounds Facilitate Visually Induced Self-Motion Perception (Vection)

We examined whether and how sounds influence visually induced illusory self-motion (vection). Visual stimuli were presented for 40 s. They were made radially, expanding or contracting visual motion field and luminance-defined gratings drifting in a vertical or horizontal direction. Auditory stimuli were presented with the visual stimuli in most conditions; we employed sounds that increased or decreased in intensity, or ascended or descended in frequency. As a result, the sound which increased in intensity facilitated forward vection, and the sound which ascended/descended in frequency facilitated upward/downward vection. The perceptual plausibility of the sound for the corresponding self-motion seemed an important factor of enhancing vection.

More Rapid and Stronger Vection in Elementary School Children Compared with Adults

We compared vection (visually induced illusory self-motion perception) among elementary school children and adults by measuring latency to onset, cumulative duration, and estimated strength of vection. Significantly stronger vection with shorter latency was observed in children compared with adults. Several possible causes (eg size-difference of the effective visual field) of the age-related differences are discussed.

Directionless Vection: A New Illusory Self-Motion Perception

We report a new visual illusion, “directionless vection.” When expanding and contracting optic flows are simultaneously presented in the same depth plane, observers can perceive illusory self-motion (vection) without direction.

The effect of self-motion perception on horizontal sound localization in front and rear spaces

The effect of self-motion perception on horizontal sound localization in front and rear spaces

Mathematical requirements of visual–vestibular integration

This article addresses the intersection between perceptual estimates of head motion based on purely vestibular and purely visual sensation, by considering how nonvisual (e.g. vestibular and proprioceptive) sensory signals for head and eye motion can be combined with visual signals available from a single landmark to generate a complete perception of self-motion. In order to do this, mathematical dimensions of sensory signals and perceptual parameterizations of self-motion are evaluated, and equations for the sensory-to-perceptual transition are derived. With constant velocity translation and vision of a single point, it is shown that visual sensation allows only for the externalization, to the frame of reference given by the landmark, of an inertial self-motion estimate from nonvisual signals. However, it is also shown that, with nonzero translational acceleration, use of simple visual signals provides a biologically plausible strategy for integration of inertial acceleration sensation, to recover translational velocity. A dimension argument proves similar results for horizontal flow of any number of discrete visible points. The results provide insight into the convergence of visual and vestibular sensory signals for self-motion and indicate perceptual algorithms by which primitive visual and vestibular signals may be integrated for self-motion perception.

Perceived Direction of Self-Motion from Orthogonally Directed Visual and Vestibular Stimulation in Passive and Active Observation

Perceiving the direction of self-motion is typically a multisensory process. The most effective cue to detect the observer's heading direction is the visual optic-flow pattern. In the initial period of body movement, however, the vestibular sense is another effective cue to detect the direction in which one's body started to move. Here I report our recent research on the perception of self-motion, 1) when observers are passively experiencing their real somatic motion in different body posture, and 2) when observers are actively moving their bodies forward and backward. Previously, we reported that when upright observers passively experience real linear oscillatory somatic motion (leftward/rightward or forward/backward) while viewing orthogonal visual optic flow patterns (translating or expanding/contracting), their perceived body motion direction is intermediate to those specified by visual and vestibular information individually (Sakurai et al., 2002, ACV; 2003, ECVP; Sakurai et al., 2010, VSS; Kubodera ...

Integration of Visual, Vestibular and Somatosensory Information for the Perception of Gravitational Vertical and Forward Self-Motion

We investigated how human perceives forward self-motion from the information produced by the vestibular, somatosensory and visual systems. In the experiments, we manipulated vestibular and somatosensory information by changing the direction of the subject's body. The subject sat in a drum which was tilted about the pitch axis of the subject. We also manipulated the visual information by presenting optic flow of dots on the display in front of the subject. In Exp.1, the pitch of subject was fixed at a certain angle for each trial. In Exp.2, the pitch angle was changed temporally, and the acceleration of the optic flow was synchronized with the angle to simulate the flow produced by the forward self-motion of the acceleration. During the trials, the subject continuously responded the gravitational vertical. In the condition of fixed pitch angle (Exp.1), subjects' responses of the gravitational vertical almost corresponded to the real direction and were not affected by the visual stimulus. In the condition o...