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Directional abnormalities of vestibular and optokinetic responses in cerebellar disease

Directional abnormalities of vestibular and optokinetic responses in patients with cerebellar degeneration are reported. Three-axis magnetic search-coil recordings of the eye and head were performed in eight cerebellar patients. Among these patients, examples of directional cross-coupling were found during (1) high-frequency, high-acceleration head thrusts; (2) constant-velocity chair rotations with the head fixed; (3) constant-velocity optokinetic stimulation; and (4) following repetitive head shaking. Cross-coupling during horizontal head thrusts consisted of an inappropriate upward eye-velocity component. In some patients, sustained constant-velocity yaw-axis chair rotations produced a mixed horizontal-torsional nystagmus and/or an increase in the baseline vertical slow-phase velocity. Following horizontal head shaking, some patients showed an increase in the slow-phase velocity of their downbeat nystagmus. These various forms of cross-coupling did not necessarily occur to the same degree in a given patient; this suggests that different mechanisms may be responsible. It is suggested that cross-coupling during head thrusts may reflect a loss of calibration of brainstem connections involved in the direct vestibular pathways, perhaps due to dysfunction of the flocculus. Cross-coupling during constant-velocity rotations and following head shaking may result from a misorientation of the angular eye-velocity vector in the velocity-storage system. Finally, responses to horizontal optokinetic stimulation included an inappropriate torsional component in some patients. This suggests that the underlying organization of horizontal optokinetic tracking is in labyrinthine coordinates. The findings are also consistent with prior animal-lesion studies that have shown a role for the vestibulocerebellum in the control of the direction of the VOR.

NASA Discipline Neuroscience

Inertial processing of vestibulo-ocular signals

New evidence for a central resolution of gravito-inertial signals has been recently obtained by analyzing the properties of the vestibulo-ocular reflex (VOR) in response to combined lateral translations and roll tilts of the head. It is found that the VOR generates robust compensatory horizontal eye movements independent of whether or not the interaural translatory acceleration component is canceled out by a gravitational acceleration component due to simultaneous roll-tilt. This response property of the VOR depends on functional semicircular canals, suggesting that the brain uses both otolith and semicircular canal signals to estimate head motion relative to inertial space. Vestibular information about dynamic head attitude relative to gravity is the basis for computing head (and body) angular velocity relative to inertial space. Available evidence suggests that the inertial vestibular system controls both head attitude and velocity with respect to a gravity-centered reference frame. The basic computational principles underlying the inertial processing of otolith and semicircular canal afferent signals are outlined.

NASA Discipline Neuroscience

Signal processing related to the vestibulo-ocular reflex during combined angular rotation and linear translation of the head

The contributions of vestibular nerve afferents and central vestibular pathways to the angular (AVOR) and linear (LVOR) vestibulo-ocular reflex were studied in squirrel monkeys during fixation of near and far targets. Irregular vestibular afferents did not appear to be necessary for the LVOR, since when they were selectively silenced with galvanic currents the LVOR was essentially unaffected during both far- and near-target viewing. The linear translation signals generated by secondary AVOR neurons in the vestibular nuclei were, on average, in phase with head velocity, inversely related to viewing distance, and were nearly as strong as AVOR-related signals. We suggest that spatial-temporal transformation of linear head translation signals to angular eye velocity commands is accomplished primarily by the addition of viewing distance multiplied, centrally integrated, otolith regular afferent signals to angular VOR pathways.

NASA Discipline Neuroscience

Emergence of postural patterns as a function of vision and translation frequency

Emergence of postural patterns as a function of vision and translation frequency. We examined the frequency characteristics of human postural coordination and the role of visual information in this coordination. Eight healthy adults maintained balance in stance during sinusoidal support surface translations (12 cm peak to peak) in the anterior-posterior direction at six different frequencies. Changes in kinematic and dynamic measures revealed that both sensory and biomechanical constraints limit postural coordination patterns as a function of translation frequency. At slow frequencies (0.1 and 0.25 Hz), subjects ride the platform (with the eyes open or closed). For fast frequencies (1.0 and 1.25 Hz) with the eyes open, subjects fix their head and upper trunk in space. With the eyes closed, large-amplitude, slow-sway motion of the head and trunk occurred for fast frequencies above 0.5 Hz. Visual information stabilized posture by reducing the variability of the head's position in space and the position of the center of mass (CoM) within the support surface defined by the feet for all but the slowest translation frequencies. When subjects rode the platform, there was little oscillatory joint motion, with muscle activity limited mostly to the ankles. To support the head fixed in space and slow-sway postural patterns, subjects produced stable interjoint hip and ankle joint coordination patterns. This increase in joint motion of the lower body dissipated the energy input by fast translation frequencies and facilitated the control of upper body motion. CoM amplitude decreased with increasing translation frequency, whereas the center of pressure amplitude increased with increasing translation frequency. Our results suggest that visual information was important to maintaining a fixed position of the head and trunk in space, whereas proprioceptive information was sufficient to produce stable coordinative patterns between the support surface and legs. The CNS organizes postural patterns in this balance task as a function of available sensory information, biomechanical constraints, and translation frequency.

NASA Discipline Neuroscience

Adaptation in a rotating artificial gravity environment

The centripetal force generated by a rotating space vehicle is a potential source of artificial gravity. Minimizing the cost of such a vehicle dictates using the smallest radius and highest rotation rate possible, but head movements made at high rotation rates generate disorienting, nauseogenic cross-coupled semicircular canal stimulation. Early studies suggested 3 or 4 rpm as the highest rate at which humans could adapt to this vestibular stimulus. These studies neglected the concomitant Coriolis force actions on the head/neck system. We assessed non-vestibular Coriolis effects by measuring arm and leg movements made in the center of a rotating room turning at 10 rpm and found that movement endpoints and trajectories are initially deviated; however, subjects readily adapt with 10-20 additional movements, even without seeing their errors. Equilibrium point theories of motor control errantly predict that Coriolis forces will not cause movement endpoint errors so that subjects will not have to adapt their reaching movements during rotation. Adaptation of movement trajectory acquired during Coriolis force perturbations of one arm transfers to the unexposed arm but there is no intermanual transfer of endpoint adaptation indicating that neuromotor representations of movement endpoint and trajectory are separable and can adapt independently, also contradictory to equilibrium point theories. Touching a surface at the end of reaching movements is required for complete endpoint adaptation in darkness but trajectory adapts completely with or without terminal contact. We have also made the first kinematic measurements of unconstrained head movements during rotation, these movements show rapid adaptation to Coriolis force perturbations. Our results point to methods for achieving full compensation for rotation up to 10 rpm. Copyright 1998 Published by Elsevier Science B.V.

Non-NASA Center

Neuronal plasticity: adaptation and readaptation to the environment of space

While there have been few documented permanent neurological changes resulting from space travel, there is a growing literature which suggests that neural plasticity sometimes occurs within peripheral and central vestibular pathways during and following spaceflight. This plasticity probably has adaptive value within the context of the space environment, but it can be maladaptive upon return to the terrestrial environment. Fortunately, the maladaptive responses resulting from neuronal plasticity diminish following return to earth. However, the literature suggests that the longer the space travel, the more difficult the readaptation. With the possibility of extended space voyages and extended stays on board the international space station, it seems worthwhile to review examples of plastic vestibular responses and changes in the underlying neural substrates. Studies and facilities needed for space station investigation of plastic changes in the neural substrates are suggested. Copyright 1998 Elsevier Science B.V.

unmanned

Cerebellar microfolia and other abnormalities of neuronal growth, migration, and lamination in the Pit1dw-J homozygote mutant mouse

The Snell dwarf mouse (Pit1dw-J homozygote) has a mutation in the Pit1 gene that prevents the normal formation of the anterior pituitary. In neonates and adults there is almost complete absence of growth hormone (GH), prolactin (PRL), thyroxin (T4), and thyroid-stimulating hormone (TSH). Since these hormones have been suggested to play a role in normal development of the central nervous system (CNS), we have investigated the effects of the Pit1dw-J mutation on the cerebellum and hippocampal formation. In the cerebellum, there were abnormalities of both foliation and lamination. The major foliation anomalies were 1) changes in the relative size of specific folia and also the proportional sizes of the anterior vs posterior cerebellum; and 2) the presence of between one and three microfolia per half cerebellum. The microfolia were all in the medial portion of the hemisphere in the caudal part of the cerebellum. Each microfolium was just rostral to a normal fissure and interposed between the fissure and a normal gyrus. Lamination abnormalities included an increase in the number of single ectopic granule cells in the molecular layer in both cerebellar vermis (86%) and hemisphere (40%) in comparison with the wild-type mouse. In the hippocampus of the Pit1dw-J homozygote mouse, the number of pyramidal cells was decreased, although the width of the pyramidal cell layer throughout areas CA1-CA3 appeared to be normal, but less densely populated than in the wild-type mouse. Moreover, the number of granule cells that form the granule cell layer was decreased from the wild-type mouse and some ectopic granule cells (occurring both as single cells and as small clusters) were observed in the innermost portion of the molecular layer. The abnormalities observed in the Pit1dw-J homozygote mouse seem to be caused by both direct and indirect effects of the deficiency of TSH (or T4), PRL, or GH rather than by a direct effect of the deletion of Pit1.

Non-NASA Center

Gravitoinertial force background level affects adaptation to coriolis force perturbations of reaching movements

We evaluated the combined effects on reaching movements of the transient, movement-dependent Coriolis forces and the static centrifugal forces generated in a rotating environment. Specifically, we assessed the effects of comparable Coriolis force perturbations in different static force backgrounds. Two groups of subjects made reaching movements toward a just-extinguished visual target before rotation began, during 10 rpm counterclockwise rotation, and after rotation ceased. One group was seated on the axis of rotation, the other 2.23 m away. The resultant of gravity and centrifugal force on the hand was 1.0 g for the on-center group during 10 rpm rotation, and 1.031 g for the off-center group because of the 0.25 g centrifugal force present. For both groups, rightward Coriolis forces, approximately 0.2 g peak, were generated during voluntary arm movements. The endpoints and paths of the initial per-rotation movements were deviated rightward for both groups by comparable amounts. Within 10 subsequent reaches, the on-center group regained baseline accuracy and straight-line paths; however, even after 40 movements the off-center group had not resumed baseline endpoint accuracy. Mirror-image aftereffects occurred when rotation stopped. These findings demonstrate that manual control is disrupted by transient Coriolis force perturbations and that adaptation can occur even in the absence of visual feedback. An increase, even a small one, in background force level above normal gravity does not affect the size of the reaching errors induced by Coriolis forces nor does it affect the rate of reacquiring straight reaching paths; however, it does hinder restoration of reaching accuracy.

NASA Discipline Neuroscience

Dual adaptation of apparent concomitant motion contingent on head rotation frequency

Perceived movement of a stationary visual stimulus during head motion was measured before and after adaptation intervals during which participants performed voluntary head oscillations while viewing a moving spot. During these intervals, participants viewed the spot stimulus moving alternately in the same direction as the head was moving during either .25- or 2.0-Hz oscillations, and then in the opposite direction as the head at the other of the two frequencies. Postadaptation measures indicated that the visual stimuli were perceived as stationary only if traveling in the same direction as that viewed during adaptation at the same frequency of head motion. Thus, opposite directions of spot motion were perceived as stationary following adaptation depending on head movement frequency. The results provide an example of the ability to establish dual (or "context-specific") adaptations to altered visual-vestibular feedback.

NASA Discipline Neuroscience

A link-segment model of upright human posture for analysis of head-trunk coordination

Sensory-motor control of upright human posture may be organized in a top-down fashion such that certain head-trunk coordination strategies are employed to optimize visual and/or vestibular sensory inputs. Previous quantitative models of the biomechanics of human posture control have examined the simple case of ankle sway strategy, in which an inverted pendulum model is used, and the somewhat more complicated case of hip sway strategy, in which multisegment, articulated models are used. While these models can be used to quantify the gross dynamics of posture control, they are not sufficiently detailed to analyze head-trunk coordination strategies that may be crucial to understanding its underlying mechanisms. In this paper, we present a biomechanical model of upright human posture that extends an existing four mass, sagittal plane, link-segment model to a five mass model including an independent head link. The new model was developed to analyze segmental body movements during dynamic posturography experiments in order to study head-trunk coordination strategies and their influence on sensory inputs to balance control. It was designed specifically to analyze data collected on the EquiTest (NeuroCom International, Clackamas, OR) computerized dynamic posturography system, where the task of maintaining postural equilibrium may be challenged under conditions in which the visual surround, support surface, or both are in motion. The performance of the model was tested by comparing its estimated ground reaction forces to those measured directly by support surface force transducers. We conclude that this model will be a valuable analytical tool in the search for mechanisms of balance control.

NASA Discipline Neuroscience

Inertial vestibular coding of motion: concepts and evidence

Central processing of inertial sensory information about head attitude and motion in space is crucial for motor control. Vestibular signals are coded relative to a non-inertial system, the head, that is virtually continuously in motion. Evidence for transformation of vestibular signals from head-fixed sensory coordinates to gravity-centered coordinates have been provided by studies of the vestibulo-ocular reflex. The underlying central processing depends on otolith afferent information that needs to be resolved in terms of head translation related inertial forces and head attitude dependent pull of gravity. Theoretical solutions have been suggested, but experimental evidence is still scarce. It appears, along these lines, that gaze control systems are intimately linked to motor control of head attitude and posture.

Review

Altered astronaut lower limb and mass center kinematics in downward jumping following space flight

Astronauts exposed to the microgravity conditions encountered during space flight exhibit postural and gait instabilities upon return to earth that could impair critical postflight performance. The aim of the present study was to determine the effects of microgravity exposure on astronauts' performance of two-footed jump landings. Nine astronauts from several Space Shuttle missions were tested both preflight and postflight with a series of voluntary, two-footed downward hops from a 30-cm-high step. A video-based, three-dimensional motion-analysis system permitted calculation of body segment positions and joint angular displacements. Phase-plane plots of knee, hip, and ankle angular velocities compared with the corresponding joint angles were used to describe the lower limb kinematics during jump landings. The position of the whole-body center of mass (COM) was also estimated in the sagittal plane using an eight-segment body model. Four of nine subjects exhibited expanded phase-plane portraits postflight, with significant increases in peak joint flexion angles and flexion rates following space flight. In contrast, two subjects showed significant contractions of their phase-plane portraits postflight and three subjects showed insignificant overall changes after space flight. Analysis of the vertical COM motion generally supported the joint angle results. Subjects with expanded joint angle phase-plane portraits postflight exhibited larger downward deviations of the COM and longer times from impact to peak deflection, as well as lower upward recovery velocities. Subjects with postflight joint angle phase-plane contraction demonstrated opposite effects in the COM motion. The joint kinematics results indicated the existence of two contrasting response modes due to microgravity exposure. Most subjects exhibited "compliant" impact absorption postflight, consistent with decreased limb stiffness and damping, and a reduction in the bandwidth of the postural control system. Fewer subjects showed "stiff" behavior after space flight, where contractions in the phase-plane portraits pointed to an increase in control bandwidth. The changes appeared to result from adaptive modifications in the control of lower limb impedance. A simple 2nd-order model of the vertical COM motion indicated that changes in the effective vertical stiffness of the legs can predict key features of the postflight performance. Compliant responses may reflect inflight adaptation due to altered demands on the postural control system in microgravity, while stiff behavior may result from overcompensation postflight for the presumed reduction in limb stiffness inflight.

Clinical Trial

The role of reafference in recalibration of limb movement control and locomotion

The reafference model has frequently been used to explain spatial constancy during eye and head movements. We have found that its basic concepts also form part of the information processing necessary for the control and recalibration of reaching movements. Reaching was studied in a novel force environment--a rotating room that creates centripetal forces of the type that could someday substitute for gravity in space flight, and Coriolis forces which are side effects of rotation. We found that inertial, noncontacting Coriolis forces deviate the path and endpoint of reaching movements, a finding that shows the inadequacy of equilibrium position models of movement control. Repeated movements in the rotating room quickly lead to normal movement patterns and to a failure to perceive the perturbing forces. The first movements made after rotation stops, without Coriolis forces present, show mirror-image deviations and evoke perception of a perturbing force even though none is present. These patterns of sensorimotor control and adaptation can largely be explained on the basis of comparisons of efference copy, reafferent muscle spindle, and cutaneous mechanoreceptor signals. We also describe experiments on human locomotion using an apparatus similar to that which Mittelstaedt used to study the optomotor response of the Eristalis fly. These results show that the reafference principle relates as well to the perception of the forces acting on and exerted by the body during voluntary locomotion.

NASA Discipline Neuroscience

Postural perturbations: new insights for treatment of balance disorders

This article reviews the neural control of posture as understood through studies of automatic responses to mechanical perturbations. Recent studies of responses to postural perturbations have provided a new view of how postural stability is controlled, and this view has profound implications for physical therapy practice. We discuss the implications for rehabilitation of balance disorders and demonstrate how an understanding of the specific systems underlying postural control can help to focus and enrich our therapeutic approaches. By understanding the basic systems underlying control of balance, such as strategy selection, rapid latencies, coordinated temporal spatial patterns, force control, and context-specific adaptations, therapists can focus their treatment on each patient's specific impairments. Research on postural responses to surface translations has shown that balance is not based on a fixed set of equilibrium reflexes but on a flexible, functional motor skill that can adapt with training and experience. More research is needed to determine the extent to which quantification of automatic postural responses has practical implications for predicting falls in patients with constraints in their postural control system.

Review

Locomotor head-trunk coordination strategies following space flight

During locomotion, angular head movements act in a compensatory fashion to oppose the vertical trunk translation that occurs during each step in the gait cycle. This coordinated strategy between head and trunk motion serves to aid gaze stabilization and perhaps simplifies the sensory coordinate transformation between the head and trunk, allowing efficient descending motor control during locomotion. Following space flight, astronauts often experience oscillopsia during locomotion in addition to postural and gait instabilities, suggesting a possible breakdown in head-trunk coordination. The goal of the present investigation was to determine if exposure to the microgravity environment of space flight induces alteration in head-trunk coordination during locomotion. Astronaut subjects were asked to walk (6.4 km/h, 20 s trials) on a motorized treadmill while visually fixating on a centrally located earthfixed target positioned either 2 m (FAR) or 30 cm (NEAR) from the eyes. In addition, some trials were also performed during periodic visual occlusion. Head and trunk kinematics during locomotion were determined with the aid of a video-based motion analyzing system. We report data collected preflight (10 days prior to launch) and postflight (2 to 4 hours after landing). The coherence between pitch head and vertical trunk movements during gaze fixation of both FAR and NEAR targets was significantly reduced following space flight indicating decreased coordination between the head and trunk during postflight locomotion. Astronauts flying on their first mission showed greater alterations in the frequency spectra of pitch head movements as compared to their more experienced counterparts. These modifications in the efficacy of head movement control may account for the reported disruption in gaze performance during locomotion and may contribute to postflight postural and gait dysfunction.

NASA Discipline Neuroscience

Coupling of fingertip somatosensory information to head and body sway

Light touch contact of a fingertip with a stationary surface can provide orientation information that enhances control of upright stance. Slight changes in contact force at the fingertip provide sensory cues about the direction of body sway, allowing attenuation of sway. In the present study, we asked to which extent somatosensory cues are part of the postural control system, that is, which sensory signal supports this coupling? We investigated postural control not only when the contact surface was stationary, but also when it was moving rhythmically (from 0.1 to 0.5 Hz). In doing so, we brought somatosensory cues from the hand into conflict with other parts of the postural control system. Our focus was the temporal relationship between body sway and the contact surface. Postural sway was highly coherent with contact surface motion. Head and body sway assumed the frequency of the moving contact surface at all test frequencies. To account for these results, a simple model was formulated by approximating the postural control system as a second-order linear dynamical system. The influence of the touch stimulus was captured as the difference between the velocity of the contact surface and the velocity of body sway, multiplied by a coupling constant. Comparison of empirical results (relative phase, coherence, and gain) with model predictions supports the hypothesis of coupling between body sway and touch cues through the velocity of the somatosensory stimulus at the fingertip. One subject, who perceived movement of the touch surface, demonstrated weaker coupling than other subjects, suggesting that cognitive mechanisms introduce flexibility into the postural control scheme.

NASA Discipline Neuroscience

Vinculin promotes cell spreading by mechanically coupling integrins to the cytoskeleton

Mouse F9 embryonic carcinoma 5.51 cells that lack the cytoskeletal protein vinculin spread poorly on extracellular matrix compared with wild-type F9 cells or two vinculin-transfected clones (5.51Vin3 and Vin4; Samuels et al., 1993, J. Cell Biol. 121, 909-921). In the present study, we used this model system to determine how the presence of vinculin promotes cytoskeletal alterations and associated changes in cell shape. Microscopic analysis of cell spreading at early times, revealed that 5.51 cells retained the ability to form filopodia; however, they could not form lamellipodia, assemble stress fibers, or efficiently spread over the culture substrate. Detergent (Triton X-100) studies revealed that these major differences in cell morphology and cytoskeletal organization did not result from differences in levels of total polymerized or cross-linked actin. Biochemical studies showed that 5.51 cells, in addition to lacking vinculin, exhibited slightly reduced levels of alpha-actinin and paxillin in their detergent-insoluble cytoskeleton. The absence of vinculin correlated with a decrease in the mechanical stiffness of the integrin-cytoskeleton linkage, as measured using cell magnetometry. Furthermore, when vinculin was replaced by transfection in 5.51Vin3 and 5.51Vin4 cells, the levels of cytoskeletal-associated alpha-actinin and paxillin, the efficiency of transmembrane mechanical coupling, and the formation of actin stress fibers were all restored to near wild-type levels. These findings suggest that vinculin may promote cell spreading by stabilizing focal adhesions and transferring mechanical stresses that drive cytoskeletal remodeling, rather than by altering the total level of actin polymerization or cross-linking.

NASA Program Space Biology