Ego- and Geo-Centered References: A Functional Neuroimagery Study.

INTRODUCTION: The integration of vestibular, visual, and somatosensory cues allows the perception of space through the orientation of our body and surrounding objects with respect to gravity. The main goal of this study was to identify the cortical networks recruited during the representation of body midline and the representation of verticality. METHODS: Thirty right-handed healthy participants were evaluated using fMRI. Brain networks activated during a subjective straight-ahead (SSA) task were compared to those recruited during a subjective vertical (SV) task. RESULTS: Different patterns of cortical activation were observed, with differential increases in the angular gyrus and left cerebellum posterior lobe during the SSA task, in right rolandic operculum and cerebellum anterior lobe during the SV task. DISCUSSION: The activation of these areas involved in visuo-spatial functions suggests that bodily processes of great complexity are engaged in body representation and vertical perception. Interestingly, the common brain networks involved in SSA and SV tasks were comprised of areas of vestibular projection that receive multisensory information (parieto-occipital areas) and the cerebellum, and reveal a predominance of the right cerebral and cerebellar hemispheres. The outcomes of this first fMRI study designed to unmask common and specific neural mechanisms at work in gravity- or body-referenced tasks pave a new way for the exploration of spatial cognitive impairment in patients with vestibular or cortical disorders.

Representation of Body Orientation in Vestibular-Defective Patients Before and After Unilateral Vestibular Loss.

Introduction: The unilateral vestibular syndrome results in postural, oculomotor, perceptive, and cognitive symptoms. This study was designed to investigate the role of vestibular signals in body orientation representation, which remains poorly considered in vestibular patients. Methods: The subjective straight ahead (SSA) was investigated using a method disentangling translation and rotation components of error. Participants were required to align a rod with their body midline in the horizontal plane. Patients with right vestibular neurotomy (RVN; n =8) or left vestibular neurotomy (LVN; n = 13) or vestibular schwannoma resection were compared with 12 healthy controls. Patients were tested the day before surgery and during the recovery period, 7 days and 2 months after the surgery. Results: Before and after unilateral vestibular neurotomy, i.e., in the chronic phases, patients showed a rightward translation bias of their SSA, without rotation bias, whatever the side of the vestibular loss. However, the data show that the lower the translation error before neurotomy, the greater its increase 2 months after a total unilateral vestibular loss, therefore leading to a rightward translation of similar amplitude in the two groups of patients. In the early phase after surgery, SSA moved toward the operated side both in translation and in rotation, as typically found for biases occurring after unilateral vestibular loss, such as the subjective visual vertical (SVV) bias. Discussion and Conclusion: This study gives the first description of the immediate consequences and of the recovery time course of body orientation representation after a complete unilateral vestibular loss. The overall evolution differed according to the side of the lesion with more extensive changes over time before and after left vestibular loss. It is noteworthy that representational disturbances of self-orientation were highly unusual in the chronic stage after vestibular loss and similar to those reported after hemispheric lesions causing spatial neglect, while classical ipsilesional biases were reported in the acute stage. This study strongly supports the notion that the vestibular system plays a major role in body representation processes and more broadly in spatial cognition. From a clinical point of view, SSA appeared to be a reliable indicator for the presence of a vestibular disorder.

Signs of spatial neglect in unilateral peripheral vestibulopathy.

BACKGROUND AND PURPOSE: In this study, the question of whether egocentric representation of space is impaired in chronic unilateral vestibulopathies was examined. The objective was to test current theories attributing a predominant role to vestibular afferents in spatial cognition and to assess whether representational neglect signs are common in peripheral vestibular loss. METHODS: The subjective straight-ahead (SSA) direction was investigated using a horizontal rod allowing the translation and rotation components of the body midline representation to be dissociated in 21 patients with unilateral vestibular loss (right, 13; left, eight) and in 12 healthy controls. RESULTS: Compared to the controls, the patients with unilateral vestibulopathy showed a translation bias of their SSA, without rotation bias. The translation bias was not lateralized towards the lesioned side as typically found for biases reported after unilateral vestibular loss. Rather, the SSA bias was rightward whatever the side of the vestibular loss. The translation bias correlated with the vestibular loss, as measured by caloric response and vestibulo-ocular reflex gain, but not with the subjective visual vertical or the residual spontaneous nystagmus. CONCLUSION: The present data suggest that the dysfunctions of neural networks involved in egocentred and allocentred representations of space are differentially compensated for in unilateral vestibular defective patients. In particular, they suggest that asymmetrical vestibular inputs to cortical regions lead to representational spatial disturbances as does defective cortical processing of vestibular inputs in spatial neglect after right hemisphere stroke. They also highlight the predominant role of symmetrical and unaltered vestibular inputs in spatial cognition.

Unilateral vestibular deafferentation impairs embodied spatial cognition.

A growing number of studies indicate that cognitive complaints are common in patients with peripheral vestibular disorders. A better understanding of how vestibular disorders influence cognition in these patients requires a clear delineation of the cognitive domains affected by vestibular disorders. Here, we compared the consequences of left and right vestibular neurectomy on third-person perspective taking-a visuo-spatial task requiring mainly own-body mental imagery, and on 3D objects mental rotation imagery-requiring object-based mental imagery, but no perspective taking. Patients tested 1 week after a unilateral vestibular neurectomy and a group of age- and gender-matched healthy participants played a virtual ball-tossing game from their own first-person perspective (1PP) and from the perspective of a distant avatar (third-person perspective, 3PP). Results showed larger response times in the patients with respect to their controls for the 3PP taking task, but not for the 1PP task and the 3D objects mental imagery. In addition, we found that only patients with left vestibular neurectomy presented altered 3PP taking abilities when compared to their controls. This study suggests that unilateral vestibular loss affects mainly own-body mental transformation and that only left vestibular loss seems to impair this cognitive process. Our study also brings further evidence that vestibular signals contribute to the sensorimotor bases of social cognition and strengthens the connections between the so far distinct fields of social neuroscience and human vestibular physiology.

Functional Neuroanatomy of Vertical Visual Perception in Humans.

Vertical representation is central to posture control, as well as to spatial perception and navigation. This representation has been studied for a long time in patients with vestibular disorders and more recently in patients with hemispheric damage, in particular in those with right lesions causing spatial or postural deficits. The aim of the study was to determine the brain areas involved in the visual perception of the vertical. Sixteen right-handed healthy participants were evaluated using fMRI while they were judging the verticality of lines or, in a control task, the color of the same lines. The brain bases of the vertical perception proved to involve a bilateral temporo-occipital and parieto-occipital cortical network, with a right dominance tendency, associated with cerebellar and brainstem areas. Consistent with the outcomes of neuroanatomical studies in stroke patients, The data of this original fMRI study in healthy subjects provides new insights into brain networks associated with vertical perception which is typically impaired in both vestibular and spatial neglect patients. Interestingly, these networks include not only brain areas associated with postural control but also areas implied in body representation.

Do Visual and Vestibular Inputs Compensate for Somatosensory Loss in the Perception of Spatial Orientation? Insights from a Deafferented Patient.

The present study aimed at investigating the consequences of a massive loss of somatosensory inputs on the perception of spatial orientation. The occurrence of possible compensatory processes for external (i.e., object) orientation perception and self-orientation perception was examined by manipulating visual and/or vestibular cues. To that aim, we compared perceptual responses of a deafferented patient (GL) with respect to age-matched Controls in two tasks involving gravity-related judgments. In the first task, subjects had to align a visual rod with the gravitational vertical (i.e., Subjective Visual Vertical: SVV) when facing a tilted visual frame in a classic Rod-and-Frame Test. In the second task, subjects had to report whether they felt tilted when facing different visuo-postural conditions which consisted in very slow pitch tilts of the body and/or visual surroundings away from vertical. Results showed that, much more than Controls, the deafferented patient was fully dependent on spatial cues issued from the visual frame when judging the SVV. On the other hand, the deafferented patient did not rely at all on visual cues for self-tilt detection. Moreover, the patient never reported any sensation of tilt up to 18° contrary to Controls, hence showing that she did not rely on vestibular (i.e., otoliths) signals for the detection of very slow body tilts either. Overall, this study demonstrates that a massive somatosensory deficit substantially impairs the perception of spatial orientation, and that the use of the remaining sensory inputs available to a deafferented patient differs regarding whether the judgment concerns external vs. self-orientation.

Improving postural control by applying mechanical noise to ankle muscle tendons.

The application of subthreshold mechanical vibrations with random frequencies (white mechanical noise) to ankle muscle tendons is known to increase muscle proprioceptive information and to improve the detection of ankle movements. The aim of the present study was to analyze the effect of this mechanical noise on postural control, its possible modulation according to the sensory strategies used for postural control, and the consequences of increasing postural difficulty. The upright stance of 20 healthy young participants tested with their eyes closed was analyzed during the application of four different levels of noise and compared to that in the absence of noise (control) in three conditions: static, static on foam, and dynamic (sinusoidal translation). The quiet standing condition was conducted with the eyes open and closed to determine the subjects' visual dependency to maintain postural stability. Postural performance was assessed using posturographic and motion analysis evaluations. The results in the static condition showed that the spectral power density of body sway significantly decreased with an optimal level of noise and that the higher the spectral power density without noise, the greater the noise effect, irrespective of visual dependency. Finally, noise application was ineffective in the foam and dynamic conditions. We conclude that the application of mechanical noise to ankle muscle tendons is a means to improve quiet standing only. These results suggest that mechanical noise stimulation may be more effective in more impaired populations.

Changing perspective: The role of vestibular signals.

Social interactions depend on mechanisms such as the ability to take another person's viewpoint, i.e. visuo-spatial perspective taking. However, little is known about the sensorimotor mechanisms underpinning perspective taking. Because vestibular signals play roles in mental rotation and spatial cognition tasks and because damage to the vestibular cortex can disturb egocentric perspective, vestibular signals stand as important candidates for the sensorimotor foundations of perspective taking. Yet, no study merged natural full-body vestibular stimulations and explicit visuo-spatial perspective taking tasks in virtual environments. In Experiment 1, we combined natural vestibular stimulation on a rotatory chair with virtual reality to test how vestibular signals are processed to simulate the viewpoint of a distant avatar. While they were rotated, participants tossed a ball to a virtual character from the viewpoint of a distant avatar. Our results showed that vestibular signals influence perspective taking in a direction-specific way: participants were faster when their physical body rotated in the same direction as the mental rotation needed to take the avatar's viewpoint. In Experiment 2, participants realized 3D object mental rotations, which did not involve perspective taking, during the same whole-body vestibular stimulation. Our results demonstrated that vestibular stimulation did not affect 3D object mental rotations. Altogether, these data indicate that vestibular signals have a direction-specific influence on visuo-spatial perspective taking (self-centered mental imagery), but not a general effect on mental imagery. Findings from this study suggest that vestibular signals contribute to one of the most crucial mechanisms of social cognition: understanding others' actions.

Unilateral vestibular loss impairs external space representation.

The vestibular system is responsible for a wide range of postural and oculomotor functions and maintains an internal, updated representation of the position and movement of the head in space. In this study, we assessed whether unilateral vestibular loss affects external space representation. Patients with Menière's disease and healthy participants were instructed to point to memorized targets in near (peripersonal) and far (extrapersonal) spaces in the absence or presence of a visual background. These individuals were also required to estimate their body pointing direction. Menière's disease patients were tested before unilateral vestibular neurotomy and during the recovery period (one week and one month after the operation), and healthy participants were tested at similar times. Unilateral vestibular loss impaired the representation of both the external space and the body pointing direction: in the dark, the configuration of perceived targets was shifted toward the lesioned side and compressed toward the contralesioned hemifield, with higher pointing error in the near space. Performance varied according to the time elapsed after neurotomy: deficits were stronger during the early stages, while gradual compensation occurred subsequently. These findings provide the first demonstration of the critical role of vestibular signals in the representation of external space and of body pointing direction in the early stages after unilateral vestibular loss.

Unilateral and bilateral fatiguing contractions similarly alter postural stability but differently modify postural position on bipedal stance.

The aim of the present study was to compare the effects of unilateral and bilateral muscle fatigue on bipedal postural control and neuromuscular activities. Nineteen subjects completed bilateral fatiguing contractions (BI group), and seventeen subjects completed unilateral fatiguing contractions (UNI group) of the quadriceps femoris. Postural control, maximal voluntary contraction (MVC) and central activation ratio (CAR) were measured before and after the completion of fatiguing tasks for both groups. Postural control was evaluated by using a force platform, which recorded the center of foot pressure (COP). MVC was quantified with an ergometer and CAR was determined with the superimposed electrical stimulation technique. Spatio-temporal COP parameters were used to evaluate postural stability (displacements of COP) and postural position (coordinates of COP) and a frequency analysis of COP excursions (wavelet transform) was performed to estimate the contribution of different neuronal loops. Postural stability, MVC and CAR were similarly affected after unilateral and bilateral fatiguing contractions. Moreover, the impairment of postural position was higher after unilateral fatiguing contractions than after bilateral fatiguing contractions. The study's results indicated that unilateral and bilateral fatigue equally disturbs postural control as well as central drive. However, unilateral muscle fatigue creates postural asymmetries while bilateral muscle fatigue does not engender any.

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.

Biases in the perception of self-motion during whole-body acceleration and deceleration.

Several studies have investigated whether vestibular signals can be processed to determine the magnitude of passive body motions. Many of them required subjects to report their perceived displacements offline, i.e., after being submitted to passive displacements. Here, we used a protocol that allowed us to complement these results by asking subjects to report their introspective estimation of their displacement continuously, i.e., during the ongoing body rotation. To this end, participants rotated the handle of a manipulandum around a vertical axis to indicate their perceived change of angular position in space at the same time as they were passively rotated in the dark. The rotation acceleration (Acc) and deceleration (Dec) lasted either 1.5 s (peak of 60°/s(2), referred to as being "High") or 3 s (peak of 33°/s(2), referred to as being "Low"). The participants were rotated either counter-clockwise or clockwise, and all combinations of acceleration and deceleration were tested (i.e., AccLow-DecLow; AccLow-DecHigh; AccHigh-DecLow; AccHigh-DecHigh). The participants' perception of body rotation was assessed by computing the gain, i.e., ratio between the amplitude of the perceived rotations (as measured by the rotating manipulandum's handle) and the amplitude of the actual chair rotations. The gain was measured at the end of the rotations, and was also computed separately for the acceleration and deceleration phases. Three salient findings resulted from this experiment: (i) the gain was much greater during body acceleration than during body deceleration, (ii) the gain was greater during High compared to Low accelerations and (iii) the gain measured during the deceleration was influenced by the preceding acceleration (i.e., Low or High). These different effects of the angular stimuli on the perception of body motion can be interpreted in relation to the consequences of body acceleration and deceleration on the vestibular system and on higher-order cognitive processes.

Postural performance of vestibular loss patients under increased postural threat.

The effects of increasing postural task difficulty on balance control was investigated in 9 compensated vestibular loss patients whose results were compared to 11 healthy adults. Subjects were tested in static (stable support) and dynamic (sinusoidal translation of the support) conditions, both at floor level and at height (62 cm above the floor), and with and without vision, to create an additional postural threat. Wavelet analysis of the center of foot pressure displacement and motion analysis of the body segments were used to evaluate the postural performance. Evaluation questionnaires were used to examine the compensation level of the patients (DHI test), their general anxiety level (SAST), fear of height (subjective scale), and workload (NASA TLX test). (Vestibular loss patients rely more on vision and spend more energy maintaining balance than controls, but they use the same postural strategy as normals in both static and dynamic conditions.) Questionnaire data all showed differences in behavior and perceptions between the controls and the patients. However, at height and without vision, a whole body strategy leading to rigid posture replaces the head stabilization strategy found for standing at floor level. The effects of height on postural control can be attributable to an increase in postural threat and attention changes resulting from modifications in perception.

Vestibular information is necessary for maintaining metric properties of representational space: evidence from mental imagery.

The vestibular system contributes to a wide range of functions, from postural and oculomotor reflexes to spatial representation and cognition. Vestibular signals are important to maintain an internal, updated representation of the body position and movement in space. However, it is not clear to what extent they are also necessary to mentally simulate movement in situations that do not involve displacements of the body, as in mental imagery. The present study assessed how vestibular loss can affect object-based mental transformations (OMTs), i.e., imagined rotations or translations of objects relative to the environment. Participants performed one task of mental rotation of 3D-objects and two mental scanning tasks dealing with the ability to build and manipulate mental images that have metric properties. Menière's disease patients were tested before unilateral vestibular neurotomy and during the recovery period (1 week and 1 month). They were compared to healthy participants tested at similar time intervals and to bilateral vestibular-defective patients tested after the recovery period. Vestibular loss impaired all mental imagery tasks. Performance varied according to the extent of vestibular loss (bilateral patients were frequently the most impaired) and according to the time elapsed after unilateral vestibular neurotomy (deficits were stronger at the early stage after neurotomy and then gradually compensated). These findings indicate that vestibular signals are necessary to perform OMTs and provide the first demonstration of the critical role of vestibular signals in processing metric properties of mental representations. They suggest that vestibular loss disorganizes brain structures commonly involved in mental imagery, and more generally in mental representation.

Betahistine treatment improves the recovery of static symptoms in patients with unilateral vestibular loss.

Vestibular loss induces a combination of postural, oculomotor, and perceptive symptoms that are compensated over time. The aim of this study was to analyze the influence of betahistine dihydrochloride on vestibular compensation. A randomized, double-blind, placebo-controlled study was performed in Menière's disease patients who underwent a curative unilateral vestibular neurotomy (UVN). The effects of betahistine treatment were investigated on a broad spectrum of vestibular-induced changes resulting from vestibular loss: body sway, head orientation, ocular cyclotorsion, spontaneous nystagmus, verticality perception, and self-evaluation of the postural stability. The time course of the recovery was compared in 16 patients who received either a placebo or betahistine (24 mg b.i.d.) from 3 days up to 3 months after UVN. Patients were examined before (day -1) and after UVN (days 7, 30, and 90). Results indicate that betahistine reduces the time to recovery by 1 month or more depending on the tested functions. Betahistine was effective as soon as 4 days after treatment administration, and the effect remained during the whole compensation period (up to 3 months). The observed clinical effects may be attributed to an action of betahistine in rebalancing the neuronal activity between contralateral vestibular nuclei.

Disturbance of contralateral unipedal postural control after stimulated and voluntary contractions of the ipsilateral limb.

One session of sustained unilateral voluntary muscular contractions increases central fatigue and induces a cross-over of fatigue of homologous contralateral muscles. It is not known, however, how this cross-transfer affects contralateral unipedal postural control. Moreover, contralateral neurophysiological effects differ between voluntary muscular contractions and electrically stimulated contractions. The aims of this study were thus to examine the effects of muscle fatigue on contralateral unipedal postural control and to compare the effects of stimulated and voluntary contractions. Fifteen subjects took part in the protocol. Fatigue of the ipsilateral quadriceps femoris was generated either by neuromuscular electrical stimulation (NMES) or by isometric voluntary muscular contraction (VOL). Postural control on the contralateral limb was measured before (PRE condition) and after the completion of the two fatiguing exercises (POST condition) using a force platform. We analyzed body sway area and the spectral power density given by the wavelet transform. In POST condition, postural control recorded in the unipedal stance on the contralateral limb was disturbed after NMES and VOL fatiguing exercises. In addition, postural control was similarly disturbed for both exercises. These results suggest that cross-over fatigue is able to disturb postural control after both stimulated and voluntary contractions.

Stimulated and voluntary fatiguing contractions of quadriceps femoris differently disturb postural control.

Muscle fatigue affects muscle strength and postural control. However, it is not known whether impaired postural control after fatiguing muscular exercise depends on the nature of the muscle contraction. To answer this question, the present study analyzes changes in postural control after two fatiguing exercises of equal duration and intensity but that induced different magnitudes of strength loss. The effects of fatiguing contractions of the femoris quadriceps were compared for voluntary muscular contraction (VOL) and neuromuscular electrical stimulation (ES) on muscle strength and postural control. Seventeen subjects completed these two fatiguing exercises. Maximal voluntary contraction (MVC) and postural control were recorded using an isokinetic dynamometer and a force platform that recorded the center of foot pressure. Recordings were performed before and after the completion of both fatiguing tasks. Results indicate that, after a fatiguing exercise, the ES exercise affected MVC more than the VOL exercise. Inversely, postural control was disturbed more after VOL exercise than after ES exercise. In conclusion, postural control disturbance is influenced by the nature of the muscular contraction (voluntary vs. non-voluntary) and the type of the motor unit solicited (tonic vs. phasic) rather than by the magnitude of strength loss.

Tell me your vestibular deficit, and i'll tell you how you'll compensate.

Most patients with unilateral vestibular loss exhibit a similar static and dynamic vestibular syndrome consisting of vestibulo-ocular, posturolocomotor, and perceptive deficits. This vestibular syndrome recovers more or less completely and more or less rapidly over time. One open question is whether recovery mechanisms differ according to vestibular pathology and/or patients. It is reported here (1) data from three different cat models of unilateral vestibular loss reproducing vestibular pathology with sudden (unilateral vestibular neurectomy [UVN] model), gradual (unilateral labyrinthectomy [UL] model), or reversible (tetrodotoxine [TTX]) model) loss of vestibular function, and (2) clinical observations in a population of unilateral vestibular loss patients suffering the same pathology (Menière's disease). Animal models show that time courses and mechanisms of recovery depend on the type of vestibular deafferentation, and clinical findings show that Menière's patients compensate their postural and perceptive deficits using different vicarious processes. Taken together, results point to a more complex picture of compensation after unilateral vestibular loss, which cannot be reduced either to a common recovery mechanism or to a single process identical for all individuals. These findings should guide physiotherapists in treatment and rehabilitation for vestibular deficits.

Dental occlusion and postural control in adults.

We studied the influence of a dental occlusion perturbation on postural control. The tests were performed in three dental occlusion conditions: (Rest Position: no dental contact, Maximal Intercuspal Occlusion: maximal dental contact, and Thwarted Laterality Occlusion: simulation of a dental malocclusion) and four postural conditions: static (stable platform) and dynamic (unstable platform), with eyes open and eyes closed. A decay of postural control was noted between the Rest Position and Thwarted Laterality Occlusion conditions with regard to average speed and power indexes in dynamic conditions and with eyes closed. However, the head position and stabilization were not different from those in the other experimental conditions, which means that the same functional goal was reached with an increase in the total energetic cost. This work shows that dental occlusion differently affects postural control, depending on the static or dynamic conditions. Indeed, dental occlusion impaired postural control only in dynamic postural conditions and in absence of visual cues. The sensory information linked to the dental occlusion comes into effect only during difficult postural tasks and its importance grows as the other sensory cues become scarce.

How body position changes visual vertical perception after unilateral vestibular loss.

Visual vertical perception, posture and equilibrium are impaired in patients with a unilateral vestibular loss. The present study was designed to investigate whether body position (standing upright, sitting on a chair and lying supine) influences the visual vertical perception in Menière's patients tested before and after a unilateral vestibular neurotomy. Data were compared with sex- and age-matched healthy participants. During the first postoperative month the body position strongly influences the visual vertical perception. The ipsilesional deviation of the visual vertical judgment gradually increased from standing upright to sitting and to lying supine. The present data indicate that visual vertical perception improves when postural control is more demanding. This suggests that postural balance is a key reference for vertical perception, at least up to one month after vestibular loss.