Sensorimotor aspects of high-speed artificial gravity: III. Sensorimotor adaptation

As a countermeasure to the debilitating physiological effects of weightlessness, astronauts could live continuously in an artificial gravity environment created by slow rotation of an entire spacecraft or be exposed to brief daily "doses" in a short radius centrifuge housed within a non-rotating spacecraft. A potential drawback to both approaches is that head movements made during rotation may be disorienting and nauseogenic. These side effects are more severe at higher rotation rates, especially upon first exposure. Head movements during rotation generate aberrant vestibular stimulation and Coriolis force perturbations of the head-neck motor system. This article reviews our progress toward distinguishing vestibular and motor factors in side effects of rotation, and presents new data concerning the rates of rotation up to which adaptation is possible. We have studied subjects pointing to targets during constant velocity rotation, because these movements generate Coriolis motor perturbations of the arm but do not involve unusual vestibular stimulation. Initially, reaching paths and endpoints are deviated in the direction of the transient lateral Coriolis forces generated. With practice, subjects soon move in straighter paths and land on target once more. If sight of the arm is permitted, adaptation is more rapid than in darkness. Initial arm movement trajectory and endpoint deviations are proportional to Coriolis force magnitude over a range of rotation speeds from 5 to 20 rpm, and there is rapid, complete motor adaptation at all speeds. These new results indicate that motor adaptation to high rotation rates is possible. Coriolis force perturbations of head movements also occur in a rotating environment but adaptation gradually develops over the course of many head movements.     

Adaptation to rotating artificial gravity environments

A series of pioneering experiments on adaptation to rotating artificial gravity environments was conducted in the 1960s. The results of these experiments led to the general belief that humans with normal vestibular function would not be able to adapt to rotating environments with angular velocities above 3 or 4 rpm. By contrast, our recent work has shown that sensory-motor adaptation to 10 rpm can be achieved relatively easily and quickly if subjects make the same movement repeatedly. This repetition allows the nervous system to gauge how the Coriolis forces generated by movements in a rotating reference frame are deflecting movement paths and endpoints and to institute corrective adaptations. Independent mechanisms appear to underlie restoration of straight movement paths and of accurate movement endpoints. Control of head movements involves adaptation of vestibulo-collic and vestibulo-spinal mechanisms as well as adaptation to motor control of the head as an inertial mass. The vestibular adaptation has a long time constant and the motor adaptation a short one. Surprisingly, Coriolis forces generated by natural turning and reaching movements in our normal environment are typically larger than those elicited in rotating artificial gravity environments. They are not recognized as such because self-generated Coriolis forces during voluntary trunk rotation are perceptually transparent. After adaptation to a rotating environment is complete, the Coriolis forces generated by movements within it also become transparent and are not felt although they are still present.     

Influence of visually induced self-motion on postural stability

CONCLUSION: Our results indicate that the illusion of self-motion is a significant factor leading to spatial disorientation. OBJECTIVE: Under normal circumstances, self-motion is perceived in response to motion of the head and body. However, under certain conditions, such as virtual reality environments, visually induced self-motion can be perceived even though the subject is not actually moving, a phenomenon known as "vection". The aim of this study was to examine the possible influence of illusory self-rotation (circular vection) on postural adjustments. MATERIAL AND METHODS: The subjects were 10 young females with no history of ocular or vestibular disease. Video-motion analysis was applied to measure postural movements during vertical optokinetic stimulation. RESULTS: For most subjects, movement of the visual surroundings induced head and body displacements in the same direction as that of the visual stimulus, regardless of the onset of self-motion perception. However, there was a significant increase in postural instability after the subjects began to perceive false self-motion in the opposite direction to that of the visual stimulus.     

Head and body center of gravity control strategies: adaptations following vestibular rehabilitation

OBJECTIVE: We present for the first time evidence that vestibulopathy impairs coordination of the head with the body center of gravity (CG) during free speed gait over ground. Vestibulopathic individuals demonstrate uncoordinated movement and gait due, at least in part, to impaired head stability and visual fixation. Vestibular rehabilitation increases speed and stability during gait and stair climbing, although the underlying mechanisms are poorly understood. MATERIAL AND METHODS: To determine whether these locomotor improvements are due to reorganized coordination of the head with whole body CG, three-dimensional kinematics were obtained from 10 vestibulopathic individuals before and after vestibular rehabilitation and from 10 matched healthy control subjects during unconstrained, paced and in-place gait. Head control patterns were characterized using both qualitative pattern analysis and quantification of coherence between head and body CG displacements. RESULTS: Patterns of head-CG coordination differ between normal and vestibulopathic individuals in all three directions of head rotation--pitch, roll and yaw--before rehabilitation. Following vestibular rehabilitation, subjects with vestibulopathy demonstrate more normal patterns in pitch and improvements toward normal in roll and yaw. CONCLUSION: These data strongly suggest that compensatory mechanisms, obtained during vestibular rehabilitation, mediate head-CG coordination.     

Gaze Shifts to Auditory and Visual Stimuli in Cats

While much is known about the metrics and kinematics of gaze shifts to visual targets in cats, little is known about gaze shifts to auditory targets. Here, cats were trained to localize auditory and visual targets via gaze shifts. Five properties of gaze shifts to sounds were observed. First, gaze shifts were accomplished primarily by large head movements. Unlike primates, the head movement in cats often preceded eye movement though the relative timing of eye in head and head latencies depended upon the target modality and gaze shift magnitude. Second, gaze shift latencies to auditory targets tended to be shorter than equivalent shifts to visual targets for some conditions. Third, the main sequences relating gaze amplitude to maximum gaze velocity for auditory and visual targets were comparable. However, head movements to auditory and visual targets were less consistent than gaze shifts and tended to undershoot the targets by 30 % for both modalities. Fourth, at the end of gaze movement, the proportion of the gaze shift accomplished by the eye-in-head movement was greater to visual than auditory targets. On the other hand, at the end of head movement, the proportion of the gaze shift accomplished by the head was greater to auditory than visual targets. Finally, gaze shifts to long-duration auditory targets were accurate and precise and were similar to accuracy of gaze shifts to long-duration visual targets. Because the metrics of gaze shifts to visual and auditory targets are nearly equivalent, as well as their accuracy, we conclude that both sensorimotor tasks use primarily the same neural substrates for the execution of movement.     

Role of central preprogramming in dynamic visual acuity with vestibular loss

OBJECTIVE: To determine the contribution of central preprogramming of eye movements to dynamic visual acuity (DVA) during head movement in patients with vestibular hypofunction. STUDY DESIGN: Prospective, clinical study. SETTING: Tertiary care, academic hospitals. PARTICIPANTS: Twenty-six healthy subjects and 20 patients with unilateral (UVL) and 7 with bilateral vestibular loss (BVL) (age range, 20-86 years). INTERVENTIONS: Diagnostic interventions, including caloric and rotational chair testing. MAIN OUTCOME MEASURE: Measurements of DVA during predictable (DVA-predictable) and unpredictable (DVA-unpredictable) head movements using a computerized test. RESULTS: There was a difference between DVA-predictable and DVA-unpredictable scores in all groups (P<.02). The difference between DVA-predictable and DVA-unpredictable scores for the BVL group was significantly greater than that for the other groups (P<.005). Age was a significant factor in DVA-unpredictable scores for the healthy subjects (P<.001) and UVL group (P<.02). Comparisons of DVA between groups were significant (P<.03), with the following exceptions: UVL group for head movements toward the unaffected side for DVA-predictable and DVA-unpredictable scores, compared with healthy subjects, and UVL group for head movements toward the affected side for DVA-predictable scores, compared with the BVL group. CONCLUSIONS: Unpredictable head movements cause a greater decrement in visual acuity than do predictable head movements. This suggests that central programming of eye movements and/or efference copy contributes to gaze stability during predictable head movements in healthy subjects and patients with vestibular hypofunction. Patients with BVL use central programming of eye movements to maintain gaze stability more than do healthy subjects or patients with UVL.     

Adaptation of multi-segmented body movements during vibratory proprioceptive and galvanic vestibular stimulation

Control of orthograde posture and use of adaptive adjustments constitutes essential topics of human movement control, both in maintenance of static posture and in ensuring body stability during locomotion. The objective was to investigate, in twelve normal subjects, how head, shoulder, hip and knee movements and torques induced towards the support surface were affected by vibratory proprioceptive and galvanic vestibular stimulation, and to investigate whether movement pattern, body posture and movement coordination were changed over time. Our findings suggest that the adaptive process to enhance stability involves both alteration of the multi-segmented movement pattern and alteration of body posture. The magnitude of the vibratory stimulation intensity had a prominent influence on the evoked multi-segmented movement pattern. The trial conditions also influenced whether the posture were altered and if these posture adjustments were done directly at stimulation onset or gradually over a longer period. Moreover, the correlation values showed that the subjects, primarily during trials with vibratory stimulation alone, significantly increased the body movement coordination at stimulation onset and maintained this movement pattern throughout the stimulation period. Furthermore, when exposed to balance perturbations the test subjects synchronized significantly the head and torso movements in anteroposterior direction during all trial conditions.     

Contribution of the vestibular apparatus to postural control when rising from a chair

OBJECTIVE: The everyday act of rising from a chair is known to require the combined angular control of a number of the body's joints, especially those within the pitch plane. Precisely how this control is exerted, however, remains controversial. The aim of this study was to obtain a better understanding of the contribution made by the vestibular apparatus to postural control of the body and head when an individual rises from a chair. MATERIAL AND METHODS: A total of 24 healthy controls and 38 patients with varying degrees of vestibular dysfunction were examined. Electromagnetic motion sensors were used to analyze the angular control of the head and body as subjects rose from a chair with their eyes open or closed. RESULTS: We found that unilateral vestibular dysfunction caused fixation of the head with respect to the body, resulting in a loss of spatial stability of the head which was not compensated for by visual input. Visual input did appear to compensate for bilateral vestibular loss, enabling patients with bilateral vestibular apparatus impairment or central disorders to fix the position of their head in space. CONCLUSION: The act of rising from a chair is normally controlled by vestibular and proprioceptive input; the head is aligned according to the gravitational reference so as to obtain stable visual information. In patients with unilateral vestibular hypofunction, posture is still controlled by these two inputs, although the ability to align the head is diminished. In patients with bilateral vestibular hypofunction or a central disorder, head alignment is maintained using visual input, although it may not be the sole or predominant stabilizing force.     

Influence of visually induced self-motion on postural stability

Conclusion Our results indicate that the illusion of self-motion is a significant factor leading to spatial disorientation.

Objective Under normal circumstances, self-motion is perceived in response to motion of the head and body. However, under certain conditions, such as virtual reality environments, visually induced self-motion can be perceived even though the subject is not actually moving, a phenomenon known as “vection”. The aim of this study was to examine the possible influence of illusory self-rotation (circular vection) on postural adjustments.

Material and methods The subjects were 10 young females with no history of ocular or vestibular disease. Video-motion analysis was applied to measure postural movements during vertical optokinetic stimulation.

Results For most subjects, movement of the visual surroundings induced head and body displacements in the same direction as that of the visual stimulus, regardless of the onset of self-motion perception. However, there was a significant increase in postural instability after the subjects began to perceive false self-motion in the opposite direction to that of the visual stimulus.     

Low-frequency loud acoustic stimulation and goal-directed arm movements

Objective To analyse the effects of low-frequency loud acoustic stimulation on goal-directed movements involving the arm. Low-frequency sound stimulation impairs eye stability, evokes a subjective tilt of the visual surround in subjects presenting Tullio's phenomenon and induces, in normal subjects, short-latency evoked potentials in the neck and limb muscles.

Material and Methods Healthy subjects performed goal-directed movements in the horizontal plane with the right (dominant) arm to a fixed 3°-wide target positioned at an angle of 30°, with the instruction to perform fast and accurate movements to the target and to hold the final position. This fast-pointing task was performed in association with sound-induced vestibular–otolithic stimulation (110 dB SPL, 500 Hz) in the absence of visual guidance (i.e. pointing at a memorized target in the absence of target or pointer cues). Pointing errors were analysed by computing the constant errors made by the subjects (mean error). Pointing errors were also correlated with movement kinematics (movement duration, peak velocity, time to peak velocity) and with the reaction time of movement.

Results The low-frequency loud acoustic stimulation modified the final position of the arm-pointing task at the memorized target in the absence of vision.

Conclusion Goal-directed movements are achieved by means of sensory interactions between visual, somatosensory and vestibular information and the vestibular–otolithic signals contribute to the accuracy of voluntary arm movements.     

Contribution of the Vestibular Apparatus to Postural Control when Rising from a Chair

Objective—The everyday act of rising from a chair is known to require the combined angular control of a number of the body's joints, especially those within the pitch plane. Precisely how this control is exerted, however, remains controversial. The aim of this study was to obtain a better understanding of the contribution made by the vestibular apparatus to postural control of the body and head when an individual rises from a chair.

Material and Methods—A total of 24 healthy controls and 38 patients with varying degrees of vestibular dysfunction were examined. Electromagnetic motion sensors were used to analyze the angular control of the head and body as subjects rose from a chair with their eyes open or closed.

Results—We found that unilateral vestibular dysfunction caused fixation of the head with respect to the body, resulting in a loss of spatial stability of the head which was not compensated for by visual input. Visual input did appear to compensate for bilateral vestibular loss, enabling patients with bilateral vestibular apparatus impairment or central disorders to fix the position of their head in space.

Conclusion—The act of rising from a chair is normally controlled by vestibular and proprioceptive input; the head is aligned according to the gravitational reference so as to obtain stable visual information. In patients with unilateral vestibular hypofunction, posture is still controlled by these two inputs, although the ability to align the head is diminished. In patients with bilateral vestibular hypofunction or a central disorder, head alignment is maintained using visual input, although it may not be the sole or predominant stabilizing force.     

Three-dimensional Analysis of Human Locomotion in Normal Subjects and Patients with Vestibular Deficiency

The purpose of this study was to clarify the role of the vestibular system in human locomotion. The subjects were nine healthy controls, nine patients with unilateral vestibular deficiency (UVD) and nine patients with bilateral vestibular deficiency (BVD). The UVD subjects were Ménière's disease patients who were being treated with administration of gentamicin into the tympanic cavity. BVD subjects were hearing-impaired individuals who showed no response to the ice-water caloric test. A total of 13 markers were attached to the head, trunk (C7), hip and foot in order to measure translational and rotational motions with the aid of a video image processing system. All subjects were instructed to restrict their stride length to 80 cm while walking on a treadmill and watching a visual target. However, walking speed varied depending on the ability of the subject to maintain body equilibrium. The results showed that walking speed and step frequency were significantly lower for the UVD and BVD groups than for the normal group. Analysis of head movements in the sagittal plane showed a counteracting motion between pitch rotations and vertical translation as previously reported. We also found head counteracting motions between yaw rotation and lateral translation in the horizontal plane. These mechanisms are thought to help stabilize the gaze during walking. When the head fixation point was calculated by projecting the naso-occipital axis line during walking, the head counteracting motion was found to assist the vestibulo-ocular reflex in stabilizing the gaze. In addition, normal subjects seemed to use head stabilization as a space strategy in order to minimize head yaw movement. In contrast, UVD and BVD subjects adopted head stabilization as a trunk strategy.     

Three-dimensional analysis of human locomotion in normal subjects and patients with vestibular deficiency

The purpose of this study was to clarify the role of the vestibular system in human locomotion. The subjects were nine healthy controls, nine patients with unilateral vestibular deficiency (UVD) and nine patients with bilateral vestibular deficiency (BVD). The UVD subjects were Ménière's disease patients who were being treated with administration of gentamicin into the tympanic cavity. BVD subjects were hearing-impaired individuals who showed no response to the ice-water caloric test. A total of 13 markers were attached to the head, trunk (C7), hip and foot in order to measure translational and rotational motions with the aid of a video image processing system. All subjects were instructed to restrict their stride length to approximately 80 cm while walking on a treadmill and watching a visual target. However, walking speed varied depending on the ability of the subject to maintain body equilibrium. The results showed that walking speed and step frequency were significantly lower for the UVD and BVD groups than for the normal group. Analysis of head movements in the sagittal plane showed a counteracting motion between pitch rotations and vertical translation as previously reported. We also found head counteracting motions between yaw rotation and lateral translation in the horizontal plane. These mechanisms are thought to help stabilize the gaze during walking. When the head fixation point was calculated by projecting the naso-occipital axis line during walking, the head counteracting motion was found to assist the vestibulo-ocular reflex in stabilizing the gaze. In addition, normal subjects seemed to use head stabilization as a space strategy in order to minimize head yaw movement. In contrast, UVD and BVD subjects adopted head stabilization as a trunk strategy.     

Contribution of self-motion perception to acoustic target localization

CONCLUSION: The findings of this study suggest that acoustic spatial perception during head movement is achieved by the vestibular system, which is responsible for the correct dynamic of acoustic target pursuit. OBJECTIVE: The ability to localize sounds in space during whole-body rotation relies on the auditory localization system, which recognizes the position of sound in a head-related frame, and on the sensory systems, namely the vestibular system, which perceive head and body movement. The aim of this study was to analyse the contribution of head motion cues to the spatial representation of acoustic targets in humans. MATERIAL AND METHODS: Healthy subjects standing on a rotating platform in the dark were asked to pursue with a laser pointer an acoustic target which was horizontally rotated while the body was kept stationary or maintained stationary while the whole body was rotated. The contribution of head motion to the spatial acoustic representation could be inferred by comparing the gains and phases of the pursuit in the two experimental conditions when the frequency was varied. RESULTS: During acoustic target rotation there was a reduction in the gain and an increase in the phase lag, while during whole-body rotations the gain tended to increase and the phase remained constant. The different contributions of the vestibular and acoustic systems were confirmed by analysing the acoustic pursuit during asymmetric body rotation. In this particular condition, in which self-motion perception gradually diminished, an increasing delay in target pursuit was observed.     

Low-frequency loud acoustic stimulation and goal-directed arm movements

OBJECTIVE: To analyse the effects of low-frequency loud acoustic stimulation on goal-directed movements involving the arm. Low-frequency sound stimulation impairs eye stability, evokes a subjective tilt of the visual surround in subjects presenting Tullio's phenomenon and induces, in normal subjects, short-latency evoked potentials in the neck and limb muscles. MATERIAL AND METHODS: Healthy subjects performed goal-directed movements in the horizontal plane with the right (dominant) arm to a fixed 3 degree-wide target positioned at an angle of 30 degrees, with the instruction to perform fast and accurate movements to the target and to hold the final position. This fast-pointing task was performed in association with sound-induced vestibular-otolithic stimulation (110 dB SPL, 500 Hz) in the absence of visual guidance (i.e. pointing at a memorized target in the absence of target or pointer cues). Pointing errors were analysed by computing the constant errors made by the subjects (mean error). Pointing errors were also correlated with movement kinematics (movement duration, peak velocity, time to peak velocity) and with the reaction time of movement. RESULTS: The low-frequency loud acoustic stimulation modified the final position of the arm-pointing task at the memorized target in the absence of vision. CONCLUSION: Goal-directed movements are achieved by means of sensory interactions between visual, somatosensory and vestibular information and the vestibular-otolithic signals contribute to the accuracy of voluntary arm movements.     

Optimal parameters for the clinical test of dynamic visual acuity in patients with a unilateral vestibular deficit

OBJECTIVE: To determine the influence of frequency and direction of head movement and type of vision chart on the score of a clinical test of dynamic visual acuity (DVA). METHODS: The subjects were 31 healthy individuals (22 to 79 years old) and 10 patients (19 to 70 years old) with a unilateral vestibular deficit owing to surgical resection of an acoustic neuroma. They read a Snellen or an E-chart while their head was passively moved +/- 20 degrees back and forth in the horizontal or vertical direction at one of four frequencies (0.5, 1.0, 1.5, and 2.0 Hz). The DVA score was the difference in the number of lines on the vision chart that could be read with the head passively moved versus with the head immobile. RESULTS: Four healthy subjects had a low DVA score during horizontal head movements at the fastest frequency (2.0 Hz) with the Snellen chart. In patients, DVA scores significantly decreased as head movement frequency increased from 0.5 to 1.0 Hz and from 1.0 to 1.5 Hz, during horizontal and vertical movements, and with both vision charts (p < .001). The DVA scores of healthy subjects were more consistent across three trials with the E-chart than with the Snellen chart at 1.0 and 0.5 Hz (horizontal movements, p < .01) and at 1.5 and 1.0 Hz (vertical movements, p < .01). CONCLUSIONS: This study provides new indications on the optimal parameters for the clinical test of DVA. From the results, it is recommended that DVA be tested during horizontal and vertical head movements at a frequency of 1.5 Hz with the E-chart.     

Gaze stabilization test: a new clinical test of unilateral vestibular dysfunction.

OBJECTIVE: Evaluate the sensitivity, specificity, and reliability of the Gaze Stabilization Test (GST) for detection of unilateral vestibular dysfunction. STUDY DESIGN: Prospective controlled clinical trial. SETTING: Tertiary academic referral laboratory. PATIENTS: Fourteen patients (mean age, 63.8 yr; range, 43-77 yr) with history of vertigo and greater than 50% bithermal caloric asymmetry; 14 control subjects (mean age, 45.8 yr; range, 23-78 yr). INTERVENTION(S): Diagnostic test protocol with computerized system of target presentation and head velocity monitoring. MAIN OUTCOME MEASURE(S): Comparison of peak head velocity with ipsilesional and contralesional head movement-allowing gaze stability by randomly presenting transient (75 ms) targets of three optotypes above static acuity in patients and healthy subjects during self-generated headshake movements. RESULTS: GST demonstrated 93% specificity, 64% sensitivity, and a reliability index of 0.91 for the detection of unilateral dysfunction with ipsilesional movement. Peak head velocity in healthy subjects averaged 147 degrees per second, whereas ipsilesional velocities dropped significantly to an average of 84 degrees per second. Surprisingly, peak velocities were also significantly reduced to an average of 112 degrees per second with contralesional movements. CONCLUSION: GST is a reliable specific test of gaze stability which has diagnostic and rehabilitative applications in patients with vestibular dysfunction. Reduced contralesional velocities may help explain oscillopsia in patients with unilateral dysfunction.     

Effects of adaptation of vestibulo-ocular reflex function on manual target localization

The goal of the present study was to determine if adaptive modulation of vestibulo-ocular reflex (VOR) function is associated with commensurate alterations in manual target localization. To measure the effects of adapted VOR on manual responses we developed the Vestibular-Contingent Pointing Test (VCP). In the VCP test, subjects pointed to a remembered target following passive whole body rotation in the dark. In the first experiment, subjects performed VCP before and after wearing 0.5X minifying lenses that adaptively attenuate horizontal VOR gain. Results showed that adaptive reduction in horizontal VOR gain was accompanied by a commensurate change in VCP performance. In the second experiment, bilaterally labyrinthine deficient (LD) subjects were tested to confirm that vestibular cues were central to the spatial coding of both eye and hand movements during VCP. LD subjects performed significantly worse than normal subjects. These results demonstrate that adaptive change in VOR can lead to alterations in manual target localization.     

Evidence for a vestibular input contributing to dynamic head stabilization in man

Horizontal head movements in response to unpredictable horizontal oscillations of the trunk were studied in 6 patients lacking vestibular function and in 6 normal subjects. In order to obtain compensatory (i.e. stabilizing with respect to earth) head movements, all subjects were required to look at an earth-fixed target, using their eyes and head. The turning points (maxima and minima) were determined from head and trunk position records. It was found that normal subjects reversed the direction of head movements in advance of trunk movements (mean lead = 82 ms) whereas the patients reversed head direction after the trunk (mean lag = 169 ms). The coherence function between head and trunk movements, measured with a spectral analyser in an additional labyrinthineless patient, was considerably lower than in normal controls. It is concluded that patients lacking vestibular function have impaired stabilization of the head in space, which can be taken as indirect evidence of the existence of active dynamic vestibulo-collic reflex (VCR) mechanisms in normal man. The lead found in normal subjects, notwithstanding the unpredictability of the stimuli, may reflect the detection of early acceleration signals by the vestibular apparatus to organize compensatory head movements.     

Visual feedback and lip-positioning skills of children with and without impaired hearing

Interplay between visual feedback and lip-positioning skill was studied in 10 5- to 14-year-old children with normal hearing and 10 with severe to profound hearing impairment. With visual feedback, the subjects in both groups had similar response times and accuracy in matching six visually specified lip separation "targets." Special skill in processing visual information by the hearing-impaired subjects was suggested by higher velocities of lip movement toward the targets and shorter latencies in reaching the goal positions. In the responses of the hearing children, lip-closing movements were executed more accurately than opening movements both with and without visual feedback. In general, the findings showed that, given visually displayed lip-position targets and feedback from positioning actions, children can achieve the targets with high accuracy regardless of hearing status or prior speaking experience.