Differential Effects of Visual Feedback on Subjective Visual Vertical Accuracy and Precision

The brain constructs an internal estimate of the gravitational vertical by integrating multiple sensory signals. In darkness, systematic head-roll dependent errors in verticality estimates, as measured by the subjective visual vertical (SVV), occur. We hypothesized that visual feedback after each trial results in increased accuracy, as physiological adjustment errors (A−/E-effect) are likely based on central computational mechanisms and investigated whether such improvements were related to adaptational shifts of perceived vertical or to a higher cognitive strategy. We asked 12 healthy human subjects to adjust a luminous arrow to vertical in various head-roll positions (0 to 120deg right-ear down, 15deg steps). After each adjustment visual feedback was provided (lights on, display of previous adjustment and of an earth-vertical cross). Control trials consisted of SVV adjustments without feedback. At head-roll angles with the largest A-effect (90, 105, and 120deg), errors were reduced significantly (p<0.001) by visual feedback, i.e. roll under-compensation decreased, while precision of SVV was not significantly (p>0.05) influenced. In seven subjects an additional session with two consecutive blocks (first with, then without visual feedback) was completed at 90, 105 and 120deg head-roll. In these positions the error-reduction by the previous visual feedback block remained significant over the consecutive 18–24 min (post-feedback block), i.e., was still significantly (p<0.002) different from the control trials. Eleven out of 12 subjects reported having consciously added a bias to their perceived vertical based on visual feedback in order to minimize errors. We conclude that improvements of SVV accuracy by visual feedback, which remained effective after removal of feedback for ≥18 min, rather resulted from a cognitive strategy than by adapting the internal estimate of the gravitational vertical. The mechanisms behind the SVV therefore, remained stable, which is also supported by the fact that SVV precision – depending mostly on otolith input - was not affected by visual feedback.     

Disruption of Spatial Task Performance in Anorexia Nervosa

In anorexia nervosa (AN), body distortions have been associated with parietal cortex (PC) dysfunction. The PC is the anatomical substrate for a supramodal reference framework involved in spatial orientation constancy. Here, we sought to evaluate spatial orientation constancy and the perception of body orientation in AN patients. In the present study, we investigated the effect of passive lateral body inclination on the visual and tactile subjective vertical (SV) and body Z-axis in 25 AN patients and 25 healthy controls. Subjects performed visual- and tactile-spatial judgments of axis orientations in an upright position and tilted 90° clockwise or counterclockwise. We observed a significant deviation of the tactile and visual SV towards the body (an A-effect) under tilted conditions, suggesting a multisensory impairment in spatial orientation. Deviation of the Z-axis in the direction of the tilt was also observed in the AN group. The greater A-effect in AN patients may reflect reduced interoceptive awareness and thus inadequate consideration of gravitational inflow. Furthermore, marked body weight loss could decrease the somatosensory inputs required for spatial orientation. Our study results suggest that spatial references are impaired in AN. This may be due to particular integration of visual, tactile and gravitational information (e.g. vestibular and proprioceptive cues) in the PC.     

Polarity-Dependent Misperception of Subjective Visual Vertical during and after Transcranial Direct Current Stimulation (tDCS)

Pathologic tilt of subjective visual vertical (SVV) frequently has adverse functional consequences for patients with stroke and vestibular disorders. Repetitive transcranial magnetic stimulation (rTMS) of the supramarginal gyrus can produce a transitory tilt on SVV in healthy subjects. However, the effect of transcranial direct current stimulation (tDCS) on SVV has never been systematically studied. We investigated whether bilateral tDCS over the temporal-parietal region could result in both online and offline SVV misperception in healthy subjects. In a randomized, sham-controlled, single-blind crossover pilot study, thirteen healthy subjects performed tests of SVV before, during and after the tDCS applied over the temporal-parietal region in three conditions used on different days: right anode/left cathode; right cathode/left anode; and sham. Subjects were blind to the tDCS conditions. Montage-specific current flow patterns were investigated using computational models. SVV was significantly displaced towards the anode during both active stimulation conditions when compared to sham condition. Immediately after both active conditions, there were rebound effects. Longer lasting after-effects towards the anode occurred only in the right cathode/left anode condition. Current flow models predicted the stimulation of temporal-parietal regions under the electrodes and deep clusters in the posterior limb of the internal capsule. The present findings indicate that tDCS over the temporal-parietal region can significantly alter human SVV perception. This tDCS approach may be a potential clinical tool for the treatment of SVV misperception in neurological patients.     

Perceived object stability depends on multisensory estimates of gravity

Background

How does the brain estimate object stability? Objects fall over when the gravity-projected centre-of-mass lies outside the point or area of support. To estimate an object''s stability visually, the brain must integrate information across the shape and compare its orientation to gravity. When observers lie on their sides, gravity is perceived as tilted toward body orientation, consistent with a representation of gravity derived from multisensory information. We exploited this to test whether vestibular and kinesthetic information affect this visual task or whether the brain estimates object stability solely from visual information.

Methodology/Principal Findings

In three body orientations, participants viewed images of objects close to a table edge. We measured the critical angle at which each object appeared equally likely to fall over or right itself. Perceived gravity was measured using the subjective visual vertical. The results show that the perceived critical angle was significantly biased in the same direction as the subjective visual vertical (i.e., towards the multisensory estimate of gravity).

Conclusions/Significance

Our results rule out a general explanation that the brain depends solely on visual heuristics and assumptions about object stability. Instead, they suggest that multisensory estimates of gravity govern the perceived stability of objects, resulting in objects appearing more stable than they are when the head is tilted in the same direction in which they fall.     

Interaction between Visual and Proprioceptive Analyzers in Vertical Posture Control

The CNS can precisely assess the spatial position of the human body only by simultaneously processing and integrating the visual, proprioceptive, and vestibular inputs. Postural stability data make it possible to estimate changes taking place in the function of analyzers involved in the maintenance of the upright posture. The vertical posture stability was assessed in healthy children and children with spastic diplegic cerebral palsy from their postural responses to the presentation of single optokinetic or somatosensory stimuli. The visual analyzer was found to play a significant role in maintaining the upright position under natural gravity conditions in healthy children. A single exposure of the proprioceptive system to variable forces directed with the gravity of the earth (vertical) decreased the contribution of the visual analyzer. Healthy children maintained the upright position relying on the direction of movement of the optokinetic stimuli, which, however, produced no effect on the maintenance of posture in the patients. A hypothesis is proposed that prenatal or early postnatal CNS lesions decrease the contribution of phylogenetically newer brain structures to the regulation of upright posture.     

Modulation of Internal Estimates of Gravity during and after Prolonged Roll-Tilts

Perceived direction of gravity, as assessed by the subjective visual vertical (SVV), shows roll-angle dependent errors that drift over time and a bias upon return to upright. According to Bayesian observer theory, the estimated direction of gravity is derived from the posterior probability distribution by combining sensory input and prior knowledge about earth-vertical in a statistically optimal fashion. Here we aimed to further characterize the stability of SVV during and after prolonged roll-tilts. Specifically we asked whether the post-tilt bias is related to the drift pattern while roll-tilted. Twenty-nine healthy human subjects (23-56yo) repetitively adjusted a luminous arrow to the SVV over periods of 5min while upright, roll-tilted (±45°, ±90°), and immediately after returning to upright. Significant (p<0.05) drifts (median absolute drift-amplitude: 10°/5min) were found in 71% (±45°) and 78% (±90°) of runs. At ±90° roll-tilt significant increases in absolute adjustment errors were more likely (76%), whereas significant increases (56%) and decreases (44%) were about equally frequent at ±45°. When returning to upright, an initial bias towards the previous roll-position followed by significant exponential decay (median time-constant: 71sec) was noted in 47% of all runs (all subjects pooled). No significant correlations were found between the drift pattern during and immediately after prolonged roll-tilt. We conclude that the SVV is not stable during and after prolonged roll-tilt and that the direction and magnitude of drift are individually distinct and roll-angle-dependent. Likely sensory and central adaptation and random-walk processes contribute to drift while roll-tilted. Lack of correlation between the drift and the post-tilt bias suggests that it is not the inaccuracy of the SVV estimate while tilted that determines post-tilt bias, but rather the previous head-roll orientation relative to gravity. We therefore favor central adaptation, most likely a shift in prior knowledge towards the previous roll orientation, to explain the post-tilt bias.     

Leg orientation as a clinical sign for pusher syndrome

Background  

Effective control of (upright) body posture requires a proper representation of body orientation. Stroke patients with pusher syndrome were shown to suffer from severely disturbed perception of own body orientation. They experience their body as oriented 'upright' when actually tilted by nearly 20° to the ipsilesional side. Thus, it can be expected that postural control mechanisms are impaired accordingly in these patients. Our aim was to investigate pusher patients' spontaneous postural responses of the non-paretic leg and of the head during passive body tilt.     

Subjective Visual Vertical and Postural Capability in Children Born Prematurely

Purpose

We compared postural stability and subjective visual vertical performance in a group of very preterm-born children aged 3-4 years and in a group of age-matched full-term children.

Materials and Methods

A platform (from TechnoConcept) was used to measure postural control in children. Perception of subjective visual vertical was also recorded with posture while the child had to adjust the vertical in the dark or with visual perturbation. Two other conditions (control conditions) were also recorded while the child was on the platform: for a fixation of the vertical bar, and in eyes closed condition.

Results

Postural performance was poor in preterm-born children compared to that of age-matched full-term children: the surface area, the length in medio-lateral direction and the mean speed of the center of pressure (CoP) were significantly larger in the preterm-born children group (p < 0.04, p < 0.01, and p < 0.04, respectively). Dual task in both groups of children significantly affected postural control. The subjective visual vertical (SVV) values were more variable and less precise in preterm-born children.

Discussion-Conclusions

We suggest that poor postural control as well as perception of verticality observed in preterm-born children could be due to immaturity of the cortical processes involved in the motor control and in the treatment of perception and orientation of verticality.     

Internal reference frame for representation and storage of visual information during standing

The participation of different afferent systems in organization of internal reference frame was studied. For this was chosen the task of visual comparison that executed in different experimental conditions: in upright standing, with inclined body or head in frontal plane and availability or non-availability visual information about external environment. Results showed that dominant orientation of referent stimulus (minimal value of mean error and minimal variability of responses) was connected with body position, mainly head position but not with gravity and visual vertical even when visual environment was available. It means that for creating the internal representing of vertical CNS mainly uses proprioceptive information about longitudinal axis of body.     

Perfusion Imaging in Pusher Syndrome to Investigate the Neural Substrates Involved in Controlling Upright Body Position

Brain damage may induce a dysfunction of upright body position termed “pusher syndrome”. Patients with such disorder suffer from an alteration of their sense of body verticality. They experience their body as oriented upright when actually tilted nearly 20 degrees to the ipsilesional side. Pusher syndrome typically is associated with posterior thalamic stroke; less frequently with extra-thalamic lesions. This argued for a fundamental role of these structures in our control of upright body posture. Here we investigated whether such patients may show additional functional or metabolic abnormalities outside the areas of brain lesion. We investigated 19 stroke patients with thalamic or with extra-thalamic lesions showing versus not showing misperception of body orientation. We measured fluid-attenuated inversion-recovery (FLAIR) imaging, diffusion-weighted imaging (DWI), and perfusion-weighted imaging (PWI). This allowed us to determine the structural damage as well as to identify the malperfused but structural intact tissue. Pusher patients with thalamic lesions did not show dysfunctional brain areas in addition to the ones found to be structurally damaged. In the pusher patients with extra-thalamic lesions, the thalamus was neither structurally damaged nor malperfused. Rather, these patients showed small regions of abnormal perfusion in the structurally intact inferior frontal gyrus, middle temporal gyrus, inferior parietal lobule, and parietal white matter. The results indicate that these extra-thalamic brain areas contribute to the network controlling upright body posture. The data also suggest that damage of the neural tissue in the posterior thalamus itself rather than additional malperfusion in distant cortical areas is associated with pusher syndrome. Hence, it seems as if the normal functioning of both extra-thalamic as well as posterior thalamic structures is integral to perceiving gravity and controlling upright body orientation in humans.     

Vestibular reafference shapes voluntary movement

The vestibular organs in the inner ear are commonly thought of as sensors that serve balance, gaze control, and higher spatial functions such as navigation. Here, we investigate their role in the online control of voluntary movements. The central nervous system uses sensory feedback information during movement to detect and correct errors as they develop. Vestibular organs signal three-dimensional head rotations and translations and so could provide error information for body movements that transport the head in space. To test this, we electrically stimulated human vestibular nerves during a goal-directed voluntary tilt of the trunk. The stimulating current waveform was made identical to the angular velocity profile of the head in the roll plane. With this, we could proportionally increase or decrease the rate of vestibular nerve firing, as if the head were rotating faster or slower than it actually was. In comparison to movements performed without stimulation, subjects tilted their trunk faster and further or slower and less far, depending upon the polarity of the stimulus. The response was negligible when identical stimulus waveforms were replayed to stationary subjects. We conclude that the brain uses vestibular information for online error correction of planned body-movement trajectories.     

Internal reference frame for the representation and storage of visual information during standing

The roles of different afferent systems in the organization of an internal reference frame was studied. The task of visual comparison was performed by subjects under different experimental conditions: in the upright standing position and with the body or head inclined in the frontal plane and with the visual information about an external environment available or not available. It was shown that the dominant orientation of a referent stimulus (the minimum value of the mean error in the reproduction of the stimulus and the minimal variability of the error) was correlated with the body position, mainly the position of the head, more than with the gravitational or visual vertical, even when the visual information was available. This means that the proprioceptive information about the longitudinal axis of body, rather than gravity, is mainly used by the central nervous system for creating the internal representing of vertical during standing.     

Perspectives for the comprehensive examination of semicircular canal and otolith function.

A review is presented on the three-dimensional aspects of the vestibulo-oculomotor system and the current functional tests for unilateral examination of the individual receptors in the vestibular labyrinth. In the presentation, attention is directed towards the recently developed vestibular tests, which promise a more comprehensive examination of labyrinth function. More explicitly, unilateral tests for the utricle, saccule and the individual semicircular canals are discussed. Caloric irrigation and rotatory testing are widely used as tests for the integrity of the (horizontal) semicircular canals. Little useful diagnosis is made however on the vertical canals, not to mention the otolith organs. A promising approach to the examination of individual semicircular canal function has been described. This involves the perception of self-rotation in each of the planes of the semicircular canals. The patient/subject is rotated by an arbitrary amount on a standard Barany chair and then required to return the chair to its original position, by joystick control of the chair velocity. In order to test the vertical canals, the head of the subject/patient is positioned so that the plane of each canal lies in the plane of rotation. A promising unilateral test of saccular function involves the use of vestibular evoked myogenic potentials. Here it has been demonstrated that the saccules can be activated using brief, high-intensity acoustic clicks. The myogenic potential is measured using surface electrodes over the sternocleidomastoid muscles. Initial data from patients has indicated that the test is specific for unilateral saccule disorders. The unilateral test of utricle function is based on the eccentric displacement profile. Thus, eccentric displacement of the head to 3.5 cm during constant velocity rotation about the earth-vertical axis generates an adequate unilateral stimulation of the otolith organ, without involving the semicircular canals. This paradigm has also proved efficient in localizing peripheral otolith dysfunction by means of SVV estimation. This represents a novel test of otolith function that can be easily integrated into routine clinical testing. In contrast to the otolith-ocular response, the subjective visual vertical also reflects the processing of otolithic information in the higher brain centres (thalamus, vestibular cortex). Exploitation of the two complementary approaches therefore provides useful information for both experimental and clinical scientists. Of direct interest is the finding that testing with the subject rotating on-centre is sufficient to localize peripheral otolith dysfunction by means of SVV estimation. This represents a novel test of otolith function that can be easily integrated into routine clinical testing. In addition to caloric testing, which has remained the classical unilateral test of vestibular function, the newly developed tests should improve the differential diagnosis of vestibular disorders.     

Effects of postural changes and vestibular lesions on genioglossal muscle activity in conscious cats.

Previous studies in humans showed that genioglossal muscle activity is higher when individuals are supine than when they are upright, and prior experiments in anesthetized or decerebrate animals suggested that vestibular inputs might participate in triggering these alterations in muscle firing. The present study determined the effects of whole body tilts in the pitch (nose-up) plane on genioglossal activity in a conscious feline model and compared these responses with those generated by roll (ear-down) tilts. We also ascertained the effects of a bilateral vestibular neurectomy on the alterations in genioglossal activity elicited by changes in body position. Both pitch and roll body tilts produced modifications in muscle firing that were dependent on the amplitude of the rotation; however, the relative effects of ear-down and nose-up tilts on genioglossal activity were variable from animal to animal. The response variability observed might reflect the fact that genioglossus has a complex organization and participates in a variety of tongue movements; in each animal, electromyographic recordings presumably sampled the firing of different proportions of fibers in the various compartments and subcompartments of the muscle. Furthermore, removal of labyrinthine inputs resulted in alterations in genioglossal responses to postural changes that persisted until recordings were discontinued approximately 1 mo later, demonstrating that the vestibular system participates in regulating the muscle's activity. Peripheral vestibular lesions were subsequently demonstrated to be complete through the postmortem inspection of temporal bone sections or by observing that vestibular nucleus neurons did not respond to rotations in vertical planes.     

A model of the nystagmus induced by off vertical axis rotation

A three-dimensional model is proposed that accounts for a number of phenomena attributed to the otoliths. It is constructed by extending and modifying a model of vestibular velocity storage. It is proposed that the otolith information about the orientation of the head to gravity changes the time constant of vestibular responses by modulating the gain of the velocity storage feedback loop. It is further proposed that the otolith signals, such as those that generate L-nystagmus (linear acceleration induced nystagmus), are partially coupled to the vestibular system via the velocity storage integrator. The combination of these two hypotheses suggests that a vestibular neural mechanism exists that performs correlation in the mathematical sense which is multiplication followed by integration. The multiplication is performed by the otolith modulation of the velocity storage feedback loop gain and the integration is performed by the velocity storage mechanism itself. Correlation allows calculation of the degree to which two signals are related and in this context provides a simple method of determining head angular velocity from the components of linear acceleration induced by off-vertical axis rotation. Correlation accounts for the otolith supplementation of the VOR and the sustained nystagmus generated by off-vertical axis rotation. The model also predicts the cross-coupling of horizontal and vertical optokinetic afternystagmus that occurs in head-lateral positions and the reported effects of tilt on vestibular responses.     

Introductory remarks on this issue. On the role of the ampulla in disturbances of vestibular function.

The article reports on the use of pigeons as models in the study of vestibular dysfunction. In the experiment reported, the cupula was loosened by raising the endolymph pressure on one side of the ampulla. The pigeon eyes showed a nystagmus. One day later, the pigeons were able to stand upright, but with head tilted toward the side of operation. The pigeons were able to fly within 15 days. Vestibular defects added in some experimental birds resulted in an inability to regain flying capacity.     

The Noh mask effect: vertical viewpoint dependence of facial expression perception.

Full-face masks, worn by skilled actors in the Noh tradition, can induce a variety of perceived expressions with changes in head orientation. Out-of-plane rotation of the head changes the two-dimensional image characteristics of the face which viewers may misinterpret as non-rigid changes due to muscle action. Three experiments with Japanese and British viewers explored this effect. Experiment 1 confirmed a systematic relationship between vertical angle of view of a Noh mask and judged affect. A forward tilted mask was more often judged happy, and one backward tilted more often judged sad. This effect was moderated by culture. Japanese viewers ascribed happiness to the mask at greater degrees of backward tilt with a reversal towards sadness at extreme forward angles. Cropping the facial image of chin and upper head contour reduced the forward-tilt reversal. Finally, the relationship between head tilt and affect was replicated with a laser-scanned human face image, but with no cultural effect. Vertical orientation of the head changes the apparent disposition of facial features and viewers respond systematically to these changes. Culture moderates this effect, and we discuss how perceptual strategies for ascribing expression to familiar and unfamiliar images may account for the differences.     

Function of otolith organ in goldfish revealed from analysis of eye movement induced by acceleration.

An otolith organ on ground behave as a detector of both gravity and linear acceleration, and play an important role in controlling posture and eye movement for tilt of the head or translational motion. On the other hand, a gravitational acceleration ingredient to an otolith organ disappears in microgravity environment. However, linear acceleration can be received by otolith organ and produce a sensation that is different from that on Earth. It is suggested that in microgravity signal from the otolith organ may cause abnormality of posture control and eye movement. Therefore, the central nervous system may re-interprets all output from the otolith organ to indicate linear motion. A study of eye movement has been done a lot as one of a reflection related to an otolith organ system. In this study, we examined function of otolith organ in goldfish revealed from analysis of eye movement induced by linear acceleration or the tilt of body. We analyzed both torsional and vertical eye movements from video images frame by frame. For tilting stimulation, torsional eye movements induced by head down was larger than that induced by head up for larger tilt angle than 30 degrees. In the case of linear acceleration below 0.4 G, however, no clear differences were observed in both torsional and vertical eye movement. These results suggest that body tilt and linear acceleration may not be with equivalent stimulation to cause eye movement on the ground.     

Gravity-dependent and gravity-independent gain changes during vertical vestibulo-ocular reflex (VOR) adaptation

The gain of the vertical angular vestibulo-ocular reflex (aVOR) was adaptively increased or decreased with monkeys in a side down position, and the gains were tested with the axis of rotation tilted in 10 degrees increments from left- to right-side-down. Gain changes, expressed as a percentage of the preadapted values, were plotted as a function of head tilt, and fit with a cosine function. The amplitude of the cosine was half of the gravity-dependent component of the gain change and the bias, the gravity independent component. The largest changes in the gain of both components occurred in the first 30 min and continued at a slower rate throughout adaptation. The gravity-dependent and -independent gain changes were larger for gain decreases than for gain increases, but both components had similar dynamics. We conclude that the alteration in gain of the aVOR always occurs in the context of gravity.     

Postural control mechanisms in the upside-down catfish (Synodontis nigriventris)

The catfishSynodontis nigriventris normally swims upside-down but can assume any posture in response to a substrate it swims close to. Postural reflexes of the body and the eyes, labyrinthine anatomy and passively maintained posture were investigated to obtain indications for possible mechanisms controlling the peculiar postural behavior of this fish. Saccade-like resetting movements of the eyes during counter-roll to body tilt about the longitudinal axis, and maintained tilted swimming positions in blinded fish suggest that these animals reset their vestibular CNS circuits to zero when in tilted positions.Synodontis nigriventris is thus able to maintain any posture without interference from tilt-counteracting vestibular reflexes. The normal upside-down swimming apparently results from a central bias for this position and a supporting ventral light response.We conclude that if the reafference principle applies to the phenomena investigated, the efference copy may be fed through an integrator before reaching vestibular reflex circuits.