Rapid vestibular adaptation in a rotating environment by means of controlled head movements.
Head movements controlled for rapid vestibular adaptation in slow rotation room /SRR/, preventing motion sickness
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Head movements controlled for rapid vestibular adaptation in slow rotation room /SRR/, preventing motion sickness
In the present paper, we explore effects on the human of exposure to a visual virtual environment which has been enslaved to simulate the human user's head movements or eye movements. Specifically, we have studied the capacity of our experimental subjects to maintain stable spatial orientation in the context of moving their entire visible surroundings by using the parameters of the subjects' natural movements. Our index of the subjects' spatial orientation was the extent of involuntary sways of the body while attempting to stand still, as measured by translations and rotations of the head. We also observed, informally, their symptoms of motion sickness.
Horizontal head movements were studied in six subjects as they made rapid horizontal gaze adjustments while walking. The aim of the present research was to determine if gait-cycle events alter the head movement response to a visual target acquisition task. Gaze shifts of approximately 40deg were elicited by a step change in the position of a visual target from a central location to a second location in the left or right horizontal periphery. The timing of the target position change was constrained to occur at 25,50,75 and 100% of the stride cycle. The trials were randomly presented as the subjects walked on a treadmill at their preferred speed (range: 1.25 to 1.48 m/s, mean: 1.39 +/- 0.09 m/s ) . Analyses focused on the movement onset latencies of the head and eyes and on the peak velocity and saccade amplitude of the head movement response. A comparison of the group means indicated that the head movement onset lagged the eye onset (262 ms versus 252 ms). The head and eye movement onset latencies were not affected by either the direction of the target change nor the point in the gait cycle during which the target relocation occurred. However, the presence of an interaction between the gait cycle events and the direction of the visual target shift indicates that the peak head saccade velocity and head saccade amplitude are affected by the natural head oscillations that occur while walking.
The firing behavior of 51 non-eye movement related central vestibular neurons that were sensitive to passive head rotation in the plane of the horizontal semicircular canal was studied in three squirrel monkeys whose heads were free to move in the horizontal plane. Unit sensitivity to active head movements during spontaneous gaze saccades was compared with sensitivity to passive head rotation. Most units (29/35 tested) were activated at monosynaptic latencies following electrical stimulation of the ipsilateral vestibular nerve. Nine were vestibulo-spinal units that were antidromically activated following electrical stimulation of the ventromedial funiculi of the spinal cord at C1. All of the units were less sensitive to active head movements than to passive whole body rotation. In the majority of cells (37/51, 73%), including all nine identified vestibulo-spinal units, the vestibular signals related to active head movements were canceled. The remaining units (n = 14, 27%) were sensitive to active head movements, but their responses were attenuated by 20-75%. Most units were nearly as sensitive to passive head-on-trunk rotation as they were to whole body rotation; this suggests that vestibular signals related to active head movements were cancelled primarily by subtraction of a head movement efference copy signal. The sensitivity of most units to passive whole body rotation was unchanged during gaze saccades. A fundamental feature of sensory processing is the ability to distinguish between self-generated and externally induced sensory events. Our observations suggest that the distinction is made at an early stage of processing in the vestibular system.
Many secondary vestibular neurons are sensitive to head on trunk rotation during reflex-induced and voluntary head movements. During passive whole body rotation the interaction of head on trunk signals related to the vestibulo-collic reflex with vestibular signals increases the rotational gain of many secondary vestibular neurons, including many that project to the spinal cord. In some units, the sensitivity to head on trunk and vestibular input is matched and the resulting interaction produces an output that is related to the trunk velocity in space. In other units the head on trunk inputs are stronger and the resulting interaction produces an output that is larger during the reflex. During voluntary head movements, inputs related to head on trunk movement combine destructively with vestibular signals, and often cancel the sensory reafferent consequences of self-generated movements. Cancellation of sensory vestibular signals was observed in all of the antidromically identified secondary vestibulospinal units, even though many of these units were not significantly affected by reflexive head on trunk movements. The results imply that the inputs to vestibular neurons related to head on trunk rotation during reflexive and voluntary movements arise from different sources. We suggest that the relative strength of reflexive head on trunk input to different vestibular neurons might reflect the different functional roles they have in controlling the posture of the neck and body.
Saccade characteristics have been studied during coordinated eye-head movements in monkeys. Amplitude, duration, and peak velocity of saccades with head turning were compared with saccades executed while the head was artificially restrained. The results indicate that the saccade characteristics are modulated as a function of head movement, hence the gaze movement (eye+head) exactly matches saccades with head fixed. Saccade modulation is achieved by way of negative vestibulo-ocular feedback. The neck proprioceptors, because of their longer latency, are effective only if the head starts moving prior to the onset of saccade. It is concluded that saccades make with head turning are not 'ballistic' movements because their trajectory is not entirely predetermined by a central command.
Susceptibility to motion sickness was tested in 44 subjects during parabolic flight maneuvers in a KC-135 aircraft. The subjects were categorized as: (1) insusceptible; (2) moderately susceptible; or (3) highly susceptible to motion sickness during exposure to varying degrees of gravito-inertial force. After categorization, three types of head movements were evaluated to determine the effect on the subjects' baseline susceptibility. Ten cycles of head movements were made in three different parabolas until nausea was reached or 40 parabolas had been completed. All types of head movements significantly increased susceptibility for all categories; eyes-open conditions were always more stressful than eyes-closed conditions for each type of head movement. It is concluded that head movements in microgravity can elicit symptoms of motion sickness. It is suggested that head movements play an etiological role in space motion sickness. In ground based studies where head movements are necessary to elicit symptoms, they are also necessary to elicit adaptation to the microgravity environment.
Relation of depth perception to head movement, and binocular and monocular vision
Astronauts report that head movements in flight tend to bring on symptoms of space motion sickness (SMS). The effects of head movements in pitch, yaw, and roll (made both with normal vision and with eyes occluded) on susceptibility to motion sickness in the zero G phase of parabolic flight maneuvers were evaluated. The findings are clear-cut: pitch head movements are most provocative, yaw least provocative, and roll intermediate. These experiments suggest that SMS is not a unique nosological entity, but is the consequence of exposure to nonterrestrial force levels. Head movements during departures in either direction from 1 G elicit symptoms.
The flocculus and ventral paraflocculus are adjacent regions of the cerebellar cortex that are essential for controlling smooth pursuit eye movements and for altering the performance of the vestibulo-ocular reflex (VOR). The question addressed in this study is whether these regions of the cerebellum are more globally involved in controlling gaze, regardless of whether eye or active head movements are used to pursue moving visual targets. Single-unit recordings were obtained from Purkinje (Pk) cells in the floccular region of squirrel monkeys that were trained to fixate and pursue small visual targets. Cell firing rate was recorded during smooth pursuit eye movements, cancellation of the VOR, combined eye-head pursuit, and spontaneous gaze shifts in the absence of targets. Pk cells were found to be much less sensitive to gaze velocity during combined eye-head pursuit than during ocular pursuit. They were not sensitive to gaze or head velocity during gaze saccades. Temporary inactivation of the floccular region by muscimol injection compromised ocular pursuit but had little effect on the ability of monkeys to pursue visual targets with head movements or to cancel the VOR during active head movements. Thus the signals produced by Pk cells in the floccular region are necessary for controlling smooth pursuit eye movements but not for coordinating gaze during active head movements. The results imply that individual functional modules in the cerebellar cortex are less involved in the global organization and coordination of movements than with parametric control of movements produced by a specific part of the body.
Secondary canal-related vestibulospinal neurons respond to an externally applied movement of the head in the form of a firing rate modulation that encodes the angular velocity of the movement, and reflects in large part the input "head velocity in space" signal carried by the semicircular canal afferents. In addition to the head velocity signal, the vestibulospinal neurons can carry a more processed signal that includes eye position or eye velocity, or both (see Boyle on ref. list). To understand the control signals used by the central vestibular pathways in the generation of reflex head stabilization, such as the vestibulocollic reflex (VCR), and the maintenance of head posture, it is essential to record directly from identified vestibulospinal neurons projecting to the cervical spinal segments in the alert animal. The present report discusses two key features of the primate vestibulospinal system. First, the termination morphology of vestibulospinal axons in the cervical segments of the spinal cord is described to lay the structural basis of vestibulospinal control of head/neck posture and movement. And second, the head movement signal content carried by the same class of secondary vestibulospinal neurons during the actual execution of the VCR and during self-generated, or active, rapid head movements is presented.
Space motion sickness has become an operational concern in manned space flight. Considerable evidence exists that head movements in free fall, especially pitch movements, are provocative until adaptation occurs. The question arises whether space motion sickness is an unique nosological entity or is due to body movements in a nonterrestrial force environment, a force environment for which the body's dynamic sensory-motor adaptions to 1 G are no longer appropriate. To evaluate this issue, subjects were asked to make controlled head movements during exposure to high gravitoinertial force levels, 1.8-2.0 G, in parabolic flight maneuvers. Head movements in pitch with eyes open were most evocative of motion sickness, yaw movements with eyes covered were least provocative. This pattern is identical to that which occurs when the same types of head movements are made in the free fall phase of parabolic maneuvers. It appears that space motion sickness is the consequence of prolonged exposure to a nonterrestrial force background rather than of exposure to free fall per se.
Short-radius centrifugation is a potential countermeasure to long-term weightlessness. Unfortunately, head movements in a rotating environment induce serious discomfort, non-compensatory vestibulo-ocular reflexes, and subjective illusions of body tilt. In two experiments we investigated the effects of pitch and yaw head movements in participants placed supine on a rotating bed with their head at the center of rotation, feet at the rim. The vast majority of participants experienced motion sickness, inappropriate vertical nystagmus and illusory tilt and roll as predicted by a semicircular canal model. However, a small but significant number of the 28 participants experienced tilt in the predicted plane but in the opposite direction. Heart rate was elevated following one-second duration head turns. Significant adaptation occurred following a series of head turns in the light. Vertical nystagmus, motion sickness and illusory tilt all decreased with adaptation. Consequences for artificial gravity produced by short-radius centrifuges as a countermeasure are discussed. Grant numbers: NCC 9-58. c 2001. Elsevier Science Ltd. All rights reserved.
Exposure to the microgravity conditions of space flight induces adaptive modification in the control of vestibular-mediated reflexive head movement during locomotion after space flight. Space flight causes astronauts to be exposed to somatosensory adaptation in both the vestibular and body load-sensing (BLS) systems. The goal of these studies was to examine the contributions of vestibular and BLS-mediated somatosensory influences on head movement control during locomotion after long-duration space flight. Subjects were asked to walk on a treadmill driven at 1.8 m/s while performing a visual acuity task. Data were collected using the same testing protocol from three independent subject groups; 1) normal subjects before and after exposure to 30 minutes of 40% bodyweight unloaded treadmill walking, 2) bilateral labyrinthine deficient (LD) patients and 3) astronauts who performed the protocol before and after long duration space flight. Motion data from head and trunk segmental motion data were obtained to calculate the angular head pitch (HP) movements during walking trials while subjects performed the visual task, to estimate the contributions of vestibular reflexive mechanisms in HP movements. Results showed that exposure to unloaded locomotion caused a significant increase in HP movements, whereas in the LD patients the HP movements were significantly decreased. Astronaut subjects results showed a heterogeneous response of both increases and decreases in the amplitude of HP movement. We infer that BLS-mediated somatosensory input centrally modulates vestibular input and can adaptively modify head-movement control during locomotion. Thus, space flight may cause a central adaptation mediated by the converging vestibular and body load-sensing somatosensory systems.
The central and reflexive control strategies underlying movements were elucidated by studying the effects of external loads on human head movement control systems. Some experimental results are presented on dynamic changes weigh the addition of aviation helmet (SPH4) and lead weights (6 kg). Intended time-optimal movements, their dynamics and electromyographic activity of neck muscles in normal movements, and also in movements made with external weights applied to the head were measured. It was observed that, when the external loads were added, the subject went through complex adapting processes and the head movement trajectory and its derivatives reached steady conditions only after transient adapting period. The steady adapted state was reached after 15 to 20 seconds (i.e., 5 to 6 movements).
An experimental study was conducted on seven normal subjects to evaluate the effectiveness of passive head movements in suppressing the optokinetically-induced illusory self-rotation. Visual simulation was provided by a servo-controlled optokinetic drum. Each subject participated in two experimental sessions. In one condition, the subject's head remained stationary while he gazed passively at a moving stripe pattern. In the other, he gazed passively and relaxed his neck muscles while his head was rotated from side to side. It appears that suppression of optokinetically-induced illusory self-rotation with passive head movements results from the operation of a spatial constancy mechanism interrelating visual, vestibular, and kinesthetic information on ongoing body orientation. The results support the view that optokinetic 'motion sickness' is related, at least in part, to an oculomotor disturbance rather than a visually triggered disturbance of specifically vestibular etiology.
Head movement role in motion sickness as function of angular velocity, discussing prediction of human tolerance in space station
Neglecting the eccentric position of the eyes in the head can lead to erroneous interpretation of ocular motor data, particularly for near targets. We discuss the geometric effects that eye eccentricity has on the processing of target-directed eye and head movement data, and we highlight two approaches to processing and interpreting such data. The first approach involves determining the true position of the target with respect to the location of the eyes in space for evaluating the efficacy of gaze, and it allows calculation of retinal error directly from measured eye, head, and target data. The second approach effectively eliminates eye eccentricity effects by adjusting measured eye movement data to yield equivalent responses relative to a specified reference location (such as the center of head rotation). This latter technique can be used to standardize measured eye movement signals, enabling waveforms collected under different experimental conditions to be directly compared, both with the measured target signals and with each other. Mathematical relationships describing these approaches are presented for horizontal and vertical rotations, for both tangential and circumferential display screens, and efforts are made to describe the sensitivity of parameter variations on the calculated results.