Program :    Biomedical Research and Countermeasures	Ground Research
Element :    Physiology
Context-Specific Adaptation of Gravity-Dependent Vestibular Reflex Responses (NSBRI Vestibular Project 1)
Principal Investigator:
Mark J. Shelhamer, Sc.D. Department of Otolaryngology 210 Pathology Building Johns Hopkins University School of Medicine Baltimore, MD 21287	Phone: (410) 614-6302 Email: mjs@dizzy.med.jhu.edu Fax: (410) 614-1746 Congressional District: MD-7
Co-Investigator(s):
Goldberg, Jefim Minor, Lloyd B. Paloski, William H. Young, Laurence R. Zee, David S. Baylor College of Medicine Johns Hopkins University School of Medicine NASA Johnson Space Center Massachusetts Institute of Technology Johns Hopkins University School of Medicine
Monitoring Center: NSBRI	Solicitation: NSBRI
Initial Funding Date: 1997	Expiration: 2000
Students Funded Under Research: 3	Post-Doctoral Associates: 3
Required Hardware: Human short-radius centrifuge at JSC KC-135 parabolic flight aircraft
Task Description:
Eye movements are important for keeping the images of objects stationary on our retinas, since visual acuity can be significantly degraded with retinal slip of only a few degrees per second. Impairment of this ability can lead to disorientation and reduced performance in sensorimotor tasks such as piloting of spacecraft. Transitions between different gravitoinertial force environments - as during different phases of space flight - provide an extreme test of the adaptive mechanisms that maintain these reflexes. It is vitally important to determine the adaptive capabilities of space flight crew members in such circumstances, so that we can know to what extent the sensorimotor skills acquired in one gravity environment will or will not transfer to others. Our work lays the foundation for understanding these adaptive capabilities, and for determining how we can aid the processes of adaptation and readaptation. An integrated set of experiments is being conducted to address this issue. We use the general approach of adapting the vestibulo-ocular reflex (VOR), the vestibulo-colic reflex (VCR), or saccadic eye movements to a particular change in gain or phase in one condition of gravitoinertial force, and adapting to a different gain or phase (or asking for no change) in a second gravitoinertial force condition, and then seeing if the gravitoinertial force itself - the context cue - can recall the previously learned adapted responses. Previous evidence indicates that unless there is specific training to induce context- specificity, reflex adaptation is sequential rather than simultaneous. Various experiments investigate the behavioral properties, neurophysiological basis, and anatomical substrate of context-specific learning mechanisms using otolith (gravity) signals as the contextual cue for elaborating both the angular and the linear vestibulo-ocular reflex (AVOR and LVOR), saccades, and the VCR. (By linear VOR we mean the oculomotor responses - horizontal, vertical, and torsional - to linear translation of the head and body; it is sometimes referred to as the translational-LVOR.) We study the effect of context on adaptation of the phase and gain of both the AVOR and LVOR, on ocular counterrolling (OCR) in response to static head tilt, on saccadic eye movements, and on head/neck reflexes (VCR) in response to centered and off-axis (eccentric) rotation. Such research is particularly germane to potential problems of postural and oculomotor control upon exposure to different gravitational environments. The knowledge gained from these studies will help us to design pre-adaptation strategies to assist flight crews in making transitions between different gravitoinertial force situations, and can provide design data for spacecraft facilities (artificial gravity, exercise centrifuge) by delineating the limits of human adaptive capabilities.
INTRODUCTION Impairment of gaze and head stabilization reflexes can lead to disorientation and reduced performance in sensorimotor tasks such as piloting of spacecraft. Transitions between different gravitoinertial force (gif) environments - as during different phases of space flight - provide an extreme test of the adaptive capabilities of these mechanisms. We wish to determine to what extent the sensorimotor skills acquired in one gravity environment will transfer to others, and to what extent gravity can serve as a context cue to assist in maintaining the appropriate sensorimotor responses in different environments. We use the general approach of adapting a response (such as the VOR) in a particular manner (e.g. gain increase) in one context, adapting in a different manner (e.g. gain decrease) in another context, and then seeing if the context cue itself can cause switching between the previously-learned adapted responses. Various experiments investigate the behavioral properties, neurophysiological bases, and anatomical substrate of context-specific learning, emphasizing otolith (gravity) signals as a context cue. The following is an outline of the methods and major results for each experiment which is a part of this project. CONTEXT-SPECIFIC ADAPTATION IN PARABOLIC FLIGHT (MS) This experiment studies the ability of human subjects to switch between two adapted saccade gains based on various context cues. Saccadic gain is adaptively increased (using a standard double-step paradigm) in one context, and decreased in the other context, then tested to see if the context cue can cause switching between the two adapted gains. Results show that saccades can be adapted in a context-specific manner, using vertical eye position, horizontal eye position, head tilt, and upright/supine orientation as cues. The effectiveness of a cue appears to depend on its relevance to the response being adapted: horizontal eye position is a more effective cue for horizontal saccade adaptation than is vertical eye position. Gravity magnitude (0g vs. 1.8g) during parabolic flight can also be used as a context cue. Some adaptation appears to be retained after 8 months. Lunar and Martian g levels can recall adaptations imposed during 0 g. CONTEXT-SPECIFIC ADAPTATION OF THE HUMAN LVOR (MS, DSZ) This experiment studies the ability of subjects to switch between two adapted LVOR gains based on the context cue of head tilt (gravity orientation). Subjects are translated laterally at 0.7 Hz, 0.3 g. During adaptation, for 5 min a visual display moves so as to ask for a gain of 0 with the head rolled left or pitched up, then for 5 min a gain of 2 is asked for with the head rolled right or pitched down. This is repeated for 1 hr. Sine and step translations before and after adaptation determine if head orientation alone causes switching between the two adapted gains. Results show that the orientation of gravity with respect to the head can serve as a context cue. For inter-aural translations, head roll is a more effective context cue than is head pitch. This is analogous to the situation with saccade adaptation: the closer the context cue is to the response being adapted, the more effective it is. CONTEXT-SPECIFIC ADAPTATION OF RESPONSES TO CENTRIFUGATION (LRY) This experiment studies context-specific adaptation in human subjects during repeated exposure to short-radius centrifugation, so that they will have the appropriate oculomotor responses and subjective orientation in both the rotating and non-rotating environments and be able to switch between them. Subjects make head movements while rotated at 23 rpm (1g gradient from head to feet), while eye position, subjective orientation, and motion sickness are assessed. Yaw head movements during rotation initially provoke disorientation and inappropriate vertical eye movements. Repeated head movements in this situation reduce (adapt out) the noncompensatory eye movements. Adaptation to the centrifugation does occur; three 10-min adaptation sessions produced adaptation that was retained (at reduced level) a week later. Adaptation to head movements to one side did not generalize to head movements in other directions. While motion sickness disappears after 10 adaptation sessions, vertical nystagmus and illusory tilt do not. Context-specificity of the adaptation is apparent since subjects did not experience motion illusions when off the centrifuge between test sessions. PROPERTIES AND CONTEXT-SPECIFICITY OF VESTIBULOCOLLIC REFLEX (JG, WHP) This experiment quantifies and models the contributions of canal and otolith feedback to head movements induced by trunk rotations and translations in 3 dimensions. The head/neck system is inherently unstable in 1 g and requires tonic neck activity, mediated via the vestibular system, for upright posture. Rotations (centered and eccentric) are applied to human subjects while upright or supine, to assess the contributions of gravity and tangential acceleration. Properties of the head-neck control system (VCR) in three dimensions can be adequately modeled by a relatively simple, 2nd-order linear system, plus a single dead-zone nonlinearity. Adaptation of this system to changes in head inertia can be induced. This adaptation can be made dual-state, such that the appropriate neural control mechanisms for head stabilization change modes immediately upon a change in head inertia. CEREBELLAR CONTRIBUTION TO CONTEXT-SPECIFIC ADAPTATION (DSZ, LBM) These experiments determine the role of the vestibulocerebellum in otolith- ocular reflexes and their adaptation, and the relationship between the translational LVOR and pursuit. In rhesus monkey, bilateral removal of the flocculus and paraflocculus produced almost complete loss of the horizontal LVOR (even after the angular VOR had recovered). Likewise, human cerebellar patients have comparable defects in pursuit and the LVOR, while the AVOR appears to be controlled independently. This suggests that the vestibulocerebellum plays a critical role in the generation of the LVOR, and that there is a tight relationship between the generation of the LVOR and smooth pursuit. A separate experiment showed systematic variations in the axis of eye rotation at different vertical elevations, during pursuit, AVOR, and LVOR. Axis tilts for pursuit and LVOR were almost identical, and different from that for the AVOR, again showing a close relationship between neural processing for pursuit and the LVOR. Context-specific adaptation of smooth pursuit eye movements has been demonstrated in both humans and rhesus monkeys. Using vertical eye position as a context cue, the initial acceleration of the eyes, when presented with a moving target, can be made to decrease with the eyes elevated, and to increase with the eyes depressed. LVOR gain adaptation has been induced in squirrel monkeys, and was specific to the frequency used for adaptation. Following adaptation of LVOR gain, there was no significant change in the torsional eye movements to head tilt, suggesting that the responses to head tilt and head translation are not tightly coupled. CONCLUSIONS During extended space flight crew members may live in artificial gravity and make transitions to and from weightlessness for planetary exploration and return to Earth. If they learn sensorimotor skills such as piloting in the normal gravity of Earth, will they be able to perform them adequately in the weightless or the artificial gravity environment? We have convincing evidence for context- specificity in various sensorimotor responses. Such context-specific adaptation is a potential countermeasure to the performance decrements seen during these transitions. In addition, experiments on the relationship between pursuit and LVOR have implications for countermeasures based on adapting translation versus tilt responses mediated by the otoliths.
This research can be of potential benefit in the area of physical therapy and rehabilitation following loss of vestibular function. Since many such rehabilitation exercises take place in the clinic, their beneficial effects may be strongly associated with the specific environment or stimulus conditions that are present in that setting, and may not transfer readily to normal everyday settings. Recognition and better understanding of this type of context-specific behavior can aid in the design of better programs of rehabilitation.
FY00 Publications, Presentations, and Other Accomplishments:
Walker, M.F., Zee, D.S., Shelhamer, M.J., Roberts, D.C., and Lasker, A.G. ''Variation of eye velocity axis with vertical eye position during horizontal pursuit, interaural translation, and yaw rotation in normal humans.'' (abstract) Soc Neurosci Abstr 2000. Cheung, C. ''Regulator control of a short-arm centrifuge and subjective responses to head movements in the rotating environment.'' Department of Aeronautics and Astronautics, Massachusetts Institute of Technology (2000). Lyne, L. ''Artificial gravity: Evaluation of adaptation to head movements during short-radius centrifugation using subjective measures.'' Department of Aeronautics and Astronautics, Massachusetts Institute of Technology (2000). Sienko, K. ''Artificial gravity: Adaptation of the vestibulo-ocular reflex to head movements during short-radius centrifugation.'' Department of Aeronautics and Astronautics, Massachusetts Institute of Technology (2000). Young, L.R. ''Artificial gravity considerations for a Mars exploration mission.'' Otolith Function in Spatial Orientation and Movement, ed. Hess, B.J.M., and Cohen, B., New York, New York Academy of Sciences, 871: 367-378, (1999). Hegemann, S., Patel, V., Shelhamer, M.J., Kramer, P.D., and Zee, D.S. ''Adaptation of the phase of the human linear vestibulo-ocular reflex (LVOR) and effects on the oculomotor neural integrator.'' J Vestibular Res., in press, (2000). Paloski, W.H., and Young, L. Artificial gravity workshop: Proceedings and recommendations. (2000).

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