Hand movement illusions show changes in sensory reliance and preservation of multisensory integration with age for kinaesthesia.

To perceive self-hand movements, the central nervous system (CNS) relies on multiple sensory inputs mainly derived from vision, touch, and muscle proprioception. However, how and to what extent the CNS relies on these sensory systems to build kinesthetic percepts as the systems decline with age remain poorly understood. Illusory sensations of right hand rotation were induced by separately stimulating these three sensory modalities at two intensity levels. A mechanical vibrator applied to the pollicis longus muscle, a textured disk for touching, and a visual pattern rotating under the participant's hand were used to activate muscle proprioception, touch, and vision, respectively. The perceptual responses of 19 healthy elderly adults (60-88 yrs) were compared to those of 12 younger adults (19-40 yrs). In the younger group, the three types of stimulation elicited similar kinesthetic illusions at each intensity level applied. The same visual and tactile stimuli elicited more salient and faster illusions in older adults than in younger adults. In contrast, the vibration-induced illusions were significantly fewer, less salient and delayed in the older adults. For the three modalities considered, increasing the intensity of stimulation resulted in smaller increases in illusion velocity in older adults than in younger adults. Lastly, a similar improvement in the perceptual responses was observed in older and younger adults when several stimulations were combined and older participants reported more salient illusions than younger participants only in the visuo-tactile condition. This study suggests that reliance on sensory inputs for kinesthetic purposes is profoundly reshaped with aging. The elderly may rely more on visual and tactile afferents for perceiving self-hand movements than younger adults likely due to relatively greater muscle proprioception degradation. In addition, multisensory integration seems preserved but not enhanced to compensate for the global decline of all sensory systems with age.

Optimal visuotactile integration for velocity discrimination of self-hand movements.

Illusory hand movements can be elicited by a textured disk or a visual pattern rotating under one's hand, while proprioceptive inputs convey immobility information (Blanchard C, Roll R, Roll JP, Kavounoudias A. PLoS One 8: e62475, 2013). Here, we investigated whether visuotactile integration can optimize velocity discrimination of illusory hand movements in line with Bayesian predictions. We induced illusory movements in 15 volunteers by visual and/or tactile stimulation delivered at six angular velocities. Participants had to compare hand illusion velocities with a 5°/s hand reference movement in an alternative forced choice paradigm. Results showed that the discrimination threshold decreased in the visuotactile condition compared with unimodal (visual or tactile) conditions, reflecting better bimodal discrimination. The perceptual strength (gain) of the illusions also increased: the stimulation required to give rise to a 5°/s illusory movement was slower in the visuotactile condition compared with each of the two unimodal conditions. The maximum likelihood estimation model satisfactorily predicted the improved discrimination threshold but not the increase in gain. When we added a zero-centered prior, reflecting immobility information, the Bayesian model did actually predict the gain increase but systematically overestimated it. Interestingly, the predicted gains better fit the visuotactile performances when a proprioceptive noise was generated by covibrating antagonist wrist muscles. These findings show that kinesthetic information of visual and tactile origins is optimally integrated to improve velocity discrimination of self-hand movements. However, a Bayesian model alone could not fully describe the illusory phenomenon pointing to the crucial importance of the omnipresent muscle proprioceptive cues with respect to other sensory cues for kinesthesia.

Anchoring the "floating arm": Use of proprioceptive and mirror visual feedback from one arm to control involuntary displacement of the other arm.

Arm movement control takes advantage of multiple inputs, including those originating from the contralateral arm. In the mirror paradigm, it has been suggested that control of the unseen arm, hidden by the mirror, is facilitated by the reflection of the other, moving arm. Although proprioceptive feedback originating from the moving arm, (the image of which is reflected in the mirror), is always coupled with visual feedback in the mirror paradigm, the former has received little attention. We recently showed that the involuntary arm movement following a sustained, isometric contraction, known as the "floating arm" or "Kohnstamm phenomenon", was adjusted to the passive-motorized displacement of the other arm. However, provision of mirror feedback, that is, the reflection in the mirror of the passively moved arm, did not add to this coupling effect. Therefore, the interlimb coupling in the mirror paradigm may to a large extent have a proprioceptive origin rather than a visual origin. The objective of the present study was to decouple mirror feedback and proprioceptive feedback from the reflected, moving arm and evaluate their respective contributions to interlimb coupling in the mirror paradigm. First (in Experiment 1, under eyes-closed conditions), we found that masking the proprioceptive afferents of the passively moved arm (by co-vibrating the antagonistic biceps and triceps muscles) suppressed the interlimb coupling between involuntary displacement of one arm and passive displacement of the other. Next (in Experiment 2), we masked proprioceptive afferents of the passively moved arm and specifically evaluated mirror feedback. We found that interlimb coupling through mirror feedback (though significant) was weaker than interlimb coupling through proprioceptive feedback. Overall, the present results show that in the mirror paradigm, proprioceptive feedback is stronger and more consistent than visual-mirror feedback in terms of the impact on interlimb coupling.

Bioceramic fabrics improve quiet standing posture and handstand stability in expert gymnasts.

Bioceramic fabrics have been claimed to improve blood circulation, thermoregulation and muscle relaxation, thereby also improving muscular activity. Here we tested whether bioceramic fabrics have an effect on postural control and contribute to improve postural stability. In Experiment 1, we tested whether bioceramic fabrics contribute to reduce body-sway when maintaining standard standing posture. In Experiment 2, we measured the effect of bioceramic fabrics on body-sway when maintaining a more instable posture, namely a handstand hold. For both experiments, postural oscillations were measured using a force platform with four strain gauges that recorded the displacements of the center of pressure (CoP) in the horizontal plane. In half of the trials, the participants wore a full-body second skin suit containing a bioceramic layer. In the other half of the trials, they wore a 'placebo' second skin suit that had the same cut, appearance and elasticity as the bioceramic suit but did not contain the bioceramic layer. In both experiments, the surface of displacement of the CoP was significantly smaller when participants were wearing the bioceramic suit than when they were wearing the placebo suit. The results suggest that bioceramic fabrics do have an effect on postural control and improve postural stability.

Passive or simulated displacement of one arm (but not its mirror reflection) modulates the involuntary motor behavior of the other arm.

Recent studies of both healthy and patient populations have cast doubt on the mirror paradigm's beneficial effect on motor behavior. Indeed, the voluntary arm displacement that accompanies reflection in the mirror may be the determining factor in terms of the motor behavior of the contralateral arm. The objective of the present study was to assess the respective effects of mirror reflection and arm displacement (whether real or simulated) on involuntary motor behavior of the contralateral arm following sustained, isometric contraction (Kohnstamm phenomenon). Our results revealed that (i) passive displacement of one arm (displacement of the left arm via a motorized manipulandum moving at 4°/s) influenced the velocity of the Kohnstamm phenomenon (forearm flexion occurring shortly after the cessation of muscle contraction) in the contralateral arm and (ii) mirror vision had no effect. Indeed, the velocity of the Kohnstamm phenomenon tended to be adjusted to match the velocity of the passive displacement of the other arm. In a second experiment, arm displacement was simulated by vibrating the triceps at 25, 50 or 75 Hz. Results showed that the velocity of the Kohnstamm phenomenon in one arm increased with the vibration frequency applied to the other arm. Our results revealed the occurrence of bimanual coupling because involuntary displacement of one arm was regulated by muscle-related information generated by the actual or simulated displacement of the other arm. In line with the literature data on voluntary motor behavior, our study failed to evidence an additional impact of mirror vision on involuntary motor behavior.

Evaluation of a visual biofeedback on the postural control in Parkinson's disease.

OBJECTIVES: Both stabilization and orientation components of postural control are affected in Parkinson's disease (PD). These deficits are partly due to proprioceptive impairments, which frequently coexist with a visual dependence. This study aimed to evaluate if a visual biofeedback - i.e. real time anteroposterior trunk and head orientations indicated with a simplified avatar and represented in a head-mounted display - could improve the postural control of PD patients in response to a postural disturbance. The influence of focusing on one specific component of the postural control (stabilization or orientation) was also examined. METHODS: Seventeen medicated PD patients performed sequences of pull-tests, either with eyes open, eyes closed or visual biofeedback, crossed with the verbal instruction to focus either on the stabilization or on the vertical body orientation. Kinematics data were collected. RESULTS: Backward trunk tilts consequent to the pulls were unchanged across the different conditions. With eyes open and eyes closed, patients did not recover their initial vertical orientation by adopting a slightly tilted backward position. This bias disappeared with the visual biofeedback. Moreover, falls consecutive to the test were significantly less frequent with the visual biofeedback than in the two other visual conditions. These different orientation and stabilization parameters were not affected by the instruction. CONCLUSION: Unlike a verbal instruction, visualizing in real time their own body's geometry improved both components of postural control of PD patients. This provides evidences in PD about links between impaired vertical orientation, deficits in balance control, and contribution of supplementary sensory cues.

Integration of visual and proprioceptive afferents in kinesthesia.

Proprioceptive signals are of prime importance in kinesthesia. However, in conditions of visuo-proprioceptive conflicts, strong visual-evoked biases can be observed. In three experiments, we parsed the interaction between visual and proprioceptive afferents using the 'mirror box' paradigm. Participants' left arm, the image of which was reflected in a mirror, was passively moved into flexion/extension or remained static. In Experiment 1 proprioceptive afferents of the unseen static right arm were masked with diffuse arm vibration. In Experiments 2 and 3, afferent signals were enhanced by muscle vibration of biceps or triceps stretch receptors. Illusory arm movements were evaluated with subjective reports and matching adjustments. Results revealed that participants did not experience kinesthetic illusions when the mirror reflected the image of a static arm while proprioceptive afferents conveyed signals of a moving arm (Experiment 2). In this specific case, vision apparently contributed much more strongly to the final percept than proprioceptive signals. However, in most circumstances, the percept reflected integration of both afferent signals (Experiments 1-3). For instance, when both sensory channels conveyed signals of arm displacement but in the opposite direction, kinesthetic illusions occurred but were either proprioceptively (vibration illusion) or visually driven (mirror illusion), according to individual sensorial preferences (Experiments 2 and 3). These results indicate that kinesthesia is the product of cooperative integration processes in which the final percept strongly depends on the experimental conditions as well as sensorial preferences. The observed changes in the relative contribution of each input across experimental conditions likely reflect reliability-dependent weights.

Ocular versus extraocular control of posture and equilibrium.

Vision has been shown for almost a century to be heavily involved in postural control. However, the mechanism by which it operates is still an open debate. The purpose of this manuscript is to review the evidence supporting the view that there are two modes of visual detection of body sway: ocular and extraocular. The former is based on the characteristics of the visual flow (retinal slip), the second one is based on either the copy of the motor command (efference copy) or the extraocular muscle afferents (re-afferences) consecutive to eye movements. Results from the literature indicate that these two modes of visual detection of body sway are effective and can operate congruently. For sufficiently large body sway with respect to eye-target distance, the ocular and the extraocular perception systems could provide two sources of visual information about body displacements. However, the afferent system might remain the only one used for small lateral body sway.

Dissociation of visual and haptic vertical in two patients with vestibular nuclear lesions.

The somatosensory (haptic) vertical (HV) and visual vertical (VV) were assessed in two patients with vestibular nuclear lesions. Patient 1 had paroxysmal nystagmus, and was tested "on" and "off." The HV was normal "on" and "off" but the VV was severely tilted during vestibular paroxysms. Patient 2, with a brainstem stroke, was tested at months 1 and 6. The VV was severely tilted on both occasions (>12 degrees) but the HV was marginally tilted (4 degrees) in the acute stage only. These VV-HV dissociations suggest that vestibular nuclear lesions influence gravity perception mostly via ocular torsional effects rather than by disrupting a single, internal representation of verticality.

Visual vertigo: symptom assessment, spatial orientation and postural control.

Certain patients with balance disorders report a 'visual vertigo' in which their symptoms are provoked or aggravated by specific visual contexts (e.g. supermarkets, driving or movement of objects). In order to determine the causes of visual vertigo (VV), we assessed symptoms, anxiety and the influence of disorienting visual stimuli in 21 such patients. In 17 out of 21 patients, a peripheral vestibular disorder was diagnosed. Sixteen bilateral labyrinthine-defective subjects (LDS) and 25 normal subjects served as controls. Questionnaire assessment showed that the levels of trait anxiety and childhood motion sickness in the three subject groups were not significantly different. Reporting of autonomic symptoms and somatic anxiety was higher than normal in both patient groups but not significantly different between LDS and VV patients. Handicap levels were not different in the two patient groups, but the reporting of vestibular symptoms was higher in the VV than in the LDS group. The experimental stimuli required subjects to set the subjective visual vertical in three visual conditions: total darkness, in front of a tilted luminous frame (rod and frame test) and in front of a large disc rotating in the frontal plane (rod and disc test). Body sway was also measured in four visual conditions: eyes closed, eyes open, facing the tilted frame and during disc rotation. In psychophysical and postural tests, both LDS and VV patients showed: (i) a significant increase in the tilt of the visual vertical both with the static tilted frame and with the rotating disc; and (ii) an increased postural deviation whilst facing the tilted frame and the rotating disc. The ratio between sway path with eyes closed and eyes open (i.e. the stabilizing effect of vision) was increased in the LDS, but not in VV patients, compared with normal subjects. In contrast, the ratio between sway path during disc rotation and sway path during eyes open (i.e. the destabilizing effect of a moving visual stimulus) was increased in the VV patients but not in LDS. Taken together, these data show that VV patients have abnormally large perceptual and postural responses to disorienting visual environments. VV is not related to trait anxiety or a past history of motion sickness. The results indicate that VV emerges in vestibular patients if they have increased visual dependence and difficulty in resolving conflict between visual and vestibulo-proprioceptive inputs. It is argued that treating these patients with visual motion desensitization, e.g. repeated optokinetic stimulation, should be beneficial.

Reference frames and haptic perception of orientation: body and head tilt effects on the oblique effect.

The aim of this study was to examine the effect of body and head tilts on the haptic oblique effect. This effect reflects the more accurate processing of vertical and horizontal orientations, relative to oblique orientations. Body or head tilts lead to a mismatch between egocentric and gravitational axes and indicate whether the haptic oblique effect is defined in an egocentric or a gravitational reference frame. The ability to reproduce principal (vertical and horizontal) and oblique orientations was studied in upright and tilted postures. Moreover, by controlling the deviation of the haptic subjective vertical provoked by postural tilt, the possible role of a subjective gravitational reference frame was tested. Results showed that the haptic reproduction of orientations was strongly affected by both the position of the body (Experiment 1) and the position of the head (Experiment 2). In particular, the classical haptic oblique effect observed in the upright posture disappeared in tilted conditions, mainly because of a decrease in the accuracy of the vertical and horizontal settings. The subjective vertical appeared to be the orientation reproduced the most accurately. These results suggest that the haptic oblique effect is not purely gravitationally or egocentrically defined but, rather, depends on a subjective gravitational reference frame that is tilted in a direction opposite to that of the head in tilted postures (Experiment 3).

Effect of visual surrounding motion on body sway in a three-dimensional environment.

Unidirectional motion of a uniplanar background induces a codirectional postural sway. It has been shown recently that fixation of a stationary foreground object induces a sway response in the opposite direction (Bronstein & Buckwell, 1997) when the background moves transiently. The present study investigated factors determining this contradirectional postural response. In the experiments presented, center of foot pressure and head displacements were recorded from normal subjects. The subjects faced a visual background of 2 x 3 m, at a distance of 1.5 m, which could be moved parallel to the interaural axis. Results showed that when the visual scene consisted solely of a moving background, the conventional codirectional postural response was elicited. When subjects were asked to fixate an earth-fixed foreground (window frame) placed between them and the moving background, a consistent postural response in the opposite direction to background motion was observed. In addition, we showed that this contradirectional postural response was not transient but was sustained for the 11 sec of background motion. We investigated whether this contradirectional postural response was the consequence of the induced movement of the foreground by background motion. Although induced movement was verbally reported by subjects when viewing an earth-fixed target projected onto the moving background, the contradirectional sway did not occur. These results indicate that foreground-background separation in depth was necessary for the contradirectional postural response to occur rather than induced movement. Another experiment showed that, when the fixated foreground was attached to the head of the observer, the contradirectional sway was not observed and was therefore unrelated to vergence. Finally, results showed that the contradirectional postural response was, in the main, monocularly mediated. We conclude that the direction of the postural sway produced by a moving background in a three-dimensional environment is determined primarily by motion parallax.

Influence of action and expectation on visual control of posture.

Previous studies have shown that human subjects presented with a moving visual environment initiate a postural re-adjustment in the direction of motion. The present study investigated how active control or expectation of the displacement of a visual scene affects this postural response. Center of foot pressure (COP) and head displacement were recorded using a sway platform and a tracking system, respectively. The subjects faced a visual scene (1 x 1 m, at a distance of 45 cm) which moved transiently (with a velocity of 1 cm/s) in a direction parallel to the interaural axis. When the displacement of the visual scene was under the active control of the subjects, visually induced body sway was strongly inhibited, in comparison with the response to unexpected stimuli. Prior knowledge of the characteristics of the forthcoming displacement was sufficient, in most subjects, to reduce postural re-adjustment, even when subjects did not exert active control. Finally, the visually induced postural response was strongly reduced even when subjects only triggered the stimulus, without any knowledge about the direction of motion. In conclusion, it appears that although vision is of primary importance in the control of postural orientation, high level processes such as expectation can modulate its impact by providing cues as to whether forthcoming visual flow is the consequence of self-motion or object-motion.

The role of neck afferents in subjective orientation in the visual and tactile sensory modalities.

We studied the influence of neck afferents on the perception of orientation. In Experiment 1, we investigated the effect of head tilt on the subjective vertical in both the visual and tactile modalities. The results showed that head tilt triggers an Aubert effect in the visual modality and a Müller effect in the tactile modality. Significant positive correlations between the two adjustment modalities were restricted to head tilt to the left. In Experiment 2, we investigated the role of neck afferents on tactile orientation in seated and supine positions. The results showed that, in the supine position, the tactile E-effect was twice as large as in the seated position. These experiments confirm that tactile perception of orientation is affected by neck afferents, and show that the influence of neck afferents is limited by relevant gravitational cues.

Visual control of postural orientation and equilibrium in congenital nystagmus.

PURPOSE: To investigate how humans with congenital nystagmus (CN) use visual information to stabilize and orient their bodies in space. METHODS: Center of foot pressure (COP) and head displacements in the lateral plane were recorded using a sway platform and Schottky barrier photodetector, respectively. In experiment 1, a comparison was made of the oscillatory characteristics of body sway with eyes open compared with eyes closed. Experiment 2 studied the postural readjustments made in response to absolute or relative motion (motion parallax) of objects in the visual scene, generated by lateral displacement of background scenery. RESULTS: Experiment 1 revealed that subjects with CN were not able to use visual information to stabilize COP but were able to stabilize the head at frequencies lower than 1 Hz. Experiment 2 showed that in response to the displacement of a visual display, for both absolute motion and motion parallax, subjects with CN reoriented their body in space in a manner similar to control subjects. CONCLUSIONS: The results suggest that despite involuntary eye movements, subjects with CN use orientation cues to control their posture, but not dynamic cues useful to control the rapid oscillations that are particularly important at the level of COP. These findings suggest that in CN, visual control of posture is restricted by low-frequency sampling of the visual scene.

Changes in horizontal oculomotor behaviour coincide with a shift in visual motion perception.

During full-field rotation of the visual field, subjects commonly experience an initial perception of object-motion which 'switches' to a perception of self-motion. We studied the characteristics of the horizontal optokinetic nystagmus responses evoked by a moving visual stimulus in these two perceptual states over a range of stimulus velocities. During self-motion perception mean eye position was found to shift more in the direction of the newly appearing stimulus elements with a slight reduction in slow phase gain in comparison to the nystagmus evoked during object-motion perception. The results may reflect a modified strategy of spatial attention with increased emphasis on anticipatory eye movements during visually induced self-motion perception.

Influence of motion parallax in the control of spontaneous body sway.

Visual control of postural sway during quiet standing was investigated in normal subjects to see if motion parallax cues were able to improve postural stability. In experiment 1, six normal subjects fixated a fluorescent foreground target, either alone or in the presence of full room illumination. The results showed that subjects reduced body sway when the background was visible. This effect, however, could be mediated not only by parallax cues but also by an increase in the total area of visual field involved. In experiment 2, other parameters such as image angular size and target distance were controlled for. Twelve subjects fixated a two light-emitting diode (LED) target placed at 45 cm from their eyes in a dark room. A second similar two-LED target was placed either at 170 cm (maximum parallax) or at 85 cm (medium parallax) from the fixated target, or in the same plane of the fixated target (0 cm, no parallax). It was found that the amplitude of sway was reduced significantly, by approximately 20%, when the two targets were presented in depth (parallax present) as compared to when they were in the same plane (no parallax). The effect was only present in the lateral direction and for low frequency components of sway (up to 0.5 Hz). We confirmed in experiment 3 on eight subjects with a design similar to that used in experiment 2 that the effect of motion parallax on body sway was of monocular origin since observed with monocular and binocular vision. Geometrical considerations based on these results support the existence of two modes of visual detection of body sway, afferent (retinal slippage) and efferent (extra-retinal or eye-movement based).

Visual-vestibular control of posture and gait: physiological mechanisms and disorders.

The scientific analysis of clinical disorders of posture and gait is an emerging field. Precise definition of the forces and postural movements involved has been pivotal to understanding many aspects of the visual and vestibular contributions to balance. However, a great deal of argument still surrounds the question of how much gait and posture laboratories actually contribute to improve the clinical management of individual patients. One of the reasons why gait analysis techniques have not penetrated rehabilitation clinics may be that the research questions asked have been aimed at understanding mechanisms rather than at quantifying disability. The condition known as primary orthostatic tremor, which is not too well known to many neuro-otologists and posturographists, is briefly reviewed here. We propose that posturography could be the easiest way to diagnose this treatable condition.

Head orientation involvement in assessment of the subjective vertical during whole body tilt.

The aim of this research was to investigate the involvement of head tilt in the assessment of the subjective vertical during whole body tilt. For inclinations up to 28 degrees, it appears that the whole body tilt gives rise to more important deviations towards its direction (A-effect) than when the tilt was restricted to the head. A multiple regression analysis shows that errors in head-tilt condition partially account for the global errors observed in condition of whole body tilt. Other factors (relative to the degree of inclination) also played a role in the determination of the subjective vertical in whole body tilt but were less important than head tilt. These results are highly compatible with the assumption of head orientation as the major determinant in roll-tilt effects.

The role of head-centric spatial reference with a static and kinetic visual disturbance.

A static or kinetic visual disturbance affects subjects' ability to estimate the direction of the gravitational vertical. This kind of error is increased by a head roll inclination. In two experiments, we combined head orientation with a static (Experiment 1: tilted frame) versus kinetic (Experiment 2: rotating disk) visual disturbance. The results showed that with a static visual disturbance, the increase of errors in the inclined head condition was mainly the consequence of a postural head effect like an Aubert effect. On the contrary, with a kinetic visual disturbance, it appears that the disk effect increases with head inclination. However, individual errors observed with the head inclined in front of a stationary disk were systematically correlated with the errors triggered by the same head inclination in front of a rotating disk. These observations confirm that the head axis spatial reference plays an important role in orientation perception, whatever the head position and the kind of visual display.