The goal of this multi-institutional, multi-investigator NSBRI neurovestibular research project is to better understand the process of visual orientation and spatial memory in 1-G and 0-g, and to develop countermeasures for these inflight problems, such as virtual reality based preflight visual orientation training procedures, both generic and mission specific.

Our specific aims are to study:

1. Human visual orientation. To better understand static and dynamic visual orientation illusions in 0-G by quantifying them in 1-G. To determine how visual frame, polarity, motion and gravireceptor cues influence the direction of the subjective vertical, the response of the oculomotor and motor control systems, stability of the visual world (oscillopsia), and how viewing one''s own body, environmental brightness and color cues determine the subjective vertical. (L.Harris, I. Howard et al, York University)

2. Three-dimensional spatial memory, learning and navigation. To understand why astronauts have difficulty making spatial judgments between modules with different visual verticals, by quantifying how humans use visual cues in l-G to establish "spatial frameworks" with in and between adjacent visual environments. To develop a computerized technique for teaching generic 3-D spatial orientation and memory skills. To investigate and evaluate ISS allocentric coordinate marking systems, and to develop methods so trainees can learn to visualize the spatial relationships of ISS modules and potential escape routes in three dimensions. (C. Oman, et al, MIT/W. Shebilske, et al, Wright State)

3. Neural coding of spatial orientation in an animal model. To define how the preferred direction of limbic system head direction cell depends on visual, vestibular, gravireceptive, proprioceptive and motoric cues in a rat animal model during three-dimensional locomotion. To understand how the vestibular system contributes to these head direction cell responses. Ultimately, to develop a neurophysiological understanding of visual reorientation illusions and spatial cognition in astronauts. (J. Taube, et al, Dartmouth).

Effect of foreground vs. background cues: Previous experiments on visually induced self motion illusions have shown that it is the relative motion of objects and surfaces perceived to be in the background of the scene that determines the strength of the illusory sense of motion that can be evoked by angular or linear movement (vection). More distant scenery is, in general, less likely to be in motion than are objects close at hand. The more distant of two displays therefore provides the best frame of reference for judging motion of the self. We hypothesized that static visual orientation illusions follow the same rule. We surmised that a scene in the background viewed through a window would be treated as a real environment, and thus be a better indicator of true vertical than the same scene suspended in front of a wall. To test this hypothesis, we placed subjects on the mirror bed on which subjects lie prone and view the world through a mirror set at 45° and had them view a large photograph of a room interior. In one condition, the photo was in a large picture frame and suspended in front of a large flat surface. In a second condition, the photograph was hung beyond a window aperture in the flat surface. Both scenes were actually vertical but, optically, they were horizontal and above the subject''s head. Those subjects who experienced a reorientation illusion were more likely to see the scene as vertical when it was viewed as a scene through a window compared with when it was viewed as a picture hanging inside a room. Oscillopsia: The visual correlates of a person moving relative to the world and of the world moving relative to a person are equivalent and independent of the presence of gravity. Yet during self movement on Earth, vestibular cues help us resolve the ambiguity and we normally lock the external world so it is perceived as stable, despite the relative movement signaled by visual and haptic systems. Post-rotatory illusory movement of the visual world after a sudden stop is a commonly experienced example of when this breaks down. Clinically, loss of perceptual stability of the surrounding environment is called oscillopsia. Strong oscillopisia is typically accompanied by disorientation and nausea. There have been occasional reports from astronauts of mild oscillopsia in orbit, and most crew members describe very prominent head-movement-contingent oscillopsia during rentry, landing and in the first hours after return. Currently there are no validated techniques for the assessment of oscillopsia or of more subtle illusory motion of surrounding objects during self-movement. (Visual acuity is often measured as an indirect assessment since blur and motion are equivalent.) Development of techniques for the quantitative assessment of oscillopsia is a high priority for NSBRI. To develop a quantitative oscillopsia assessment method, we used virtual reality techniques to separate the natural relationship between visual and head motion during active body movements (Jaeckl, et al, 2002; Harris et al 2002). We asked subjects either to set the relationship back to ''correct'' or judge whether the scene motion was more or less than expected. We compared subjects'' performance during active head movements in different directions relative to gravity. For head rotation, we compared the range of visual motion judged compatible with a stable environment while rotating around an axis orthogonal to gravity, with judgments made when rotation was around an earth-vertical axis. For translations, we compared the corresponding range of visual motion when translation was parallel to gravity with translations orthogonal to gravity. Subjects wore a head-mounted display and made active head movements at 0.5 Hz that were monitored by a head tracker and fed back to the display. Using the method of adjustment under normal gravity conditions, 10 subjects adjusted the visual gain until the visual world appeared stable. Using the method of constant stimuli, 7 subjects moved their heads in various directions and judged whether the virtual world appeared to move ''with'' or ''against'' their movement for several visual gains. On average, subjects preferred 20-40% more visual motion than was appropriate for the geometry of movement. The accuracy of judgments was unaffected by the relative direction of gravity. In a related experiment conducted in the 90 degree Tumbled Room, subjects lay on a bed mounted on air bearings and either actively translated themselves along their long body axis or were passively moved in a similar way. Since the interior of the Tumbled Room was tilted 90 degrees with respect to gravity, supine subjects tended to feel themselves upright. A target spot was projected on a clear Plexiglas sheet so that it appeared to hover between the subject and the far wall. Subjects adjusted the motion of the spot until it appeared room-stationary during their motion. Subjects consistently underestimated the motion of the spot but the amount of their underestimation depended on whether they were active or passive (larger errors when passive) and whether they were in the Tumbled room or a normally oriented environment (larger errors in the room). These data indicate that all head movements are associated with a small amount of perceptual instability or oscillopsia in which the world appears to move by at least 10% of each head movement.

Indirect measurement of the perceived vertical: In our previous research on orientation perception, we have asked subjects to indicate their orientation with respect to the gravitational vertical by adjusting a pointer or physical rod. We have developed a complementary indirect psychophysical method, exploiting the shape-from-shading illusion (Jenkin et al, 2003). In the absence of information about the origin of illumination people interpret surface structure by assuming that light comes from above. Subjects judge the perceived convexity of a disk shaded in a gradient from one side to the other. The disk appears as a convex hemisphere when it is arranged with the lighter side up. By finding the orientation in which the disk appears most convex we can infer the perceived direction of illumination. The different cues contributing to this percept can be separated by varying the orientation of the subject and the visual background relative to gravity in the York tumbled room. We have found that the subject''s responses can be modeled by a simple vector sum of the up directions defined by vision, the body and gravity.

AIM 2- HUMAN 3D SPATIAL MEMORY AND LEARNING

Space stations such as Mir and the ISS consist of multiple elements, connected together by "nodes". Topologically, nodes are route turning points. They typically have six different hatches, separated by 90 degrees so each faces a principal spatial direction, forming a simple six-element spatial framework. Unlike terrestrial environments, astronauts can enter the node in any orientation, and face in any direction. We know humans can mentally rotate simple object arrays, but how well can they learn a spatial framework of six objects arrayed around them? Can they predict the relative direction to any one of the six objects (hatches) after any roll orientation or while facing a different hatch ? Is three dimensional object mental rotation ability an important component in performing this task ? If virtual reality techniques were used to teach astronaut crews to orient in specific environments, does one have to build a physical simulator, or can a virtual equivalent be used ? Does performance depend on the gravitational orientation of the subject ? Answers to these questions are important in the context of development of preflight visual orientation training methods for astronauts. To find the answers, we have conducted a series of experiments using both real and virtual environments, and with subjects in several different postures with respect to gravity. In our first two experiments (Oman, et al 2000; Richards et al 2003) we found that, with practice, most subjects were able to learn an environment and orient themselves accurately regardless of their orientation. Performance correlated with established measures of 2D and 3D mental rotation ability. When retested three weeks later, subjects could still recall the spatial arrangement and perform well. Many subjects made up mnemonic rules to help them remember the spatial framework, such as memorizing opposite pairs or corner configurations, showing they did not always rely on mental rotation. Teaching them such strategies improved performance. Display type (real vs. virtual) and gravitational posture had only minor effects on performance. In these experiments we randomized the order of roll-angle presentations, rather than presenting them in blocks which would have allowed the subject to practice each orientation. Though randomization makes training more difficult, we did this because theories for complex skill acquisition suggest if we were to retest skill retention or measure transfer to a second environment we would obtain better performance. Since preflight orientation training of astronauts will involve transfer and retention issues, we tested these assumptions in a third experiment (Shebilske, et al, 2003 submitted). We found performance was significantly improved for the blocked group during initial training, but was significantly lower during transfer and retention tests. For the randomly trained group, performance during all phases correlated significantly with 2D and 3D mental rotation test scores. For the blocked group, performance correlated for transfer and retention phases but not during the training phase, perhaps because spatial skills were less challenged.

AIM 3 NEURAL CODING OF 3D SPATIAL ORIENTATION IN ANIMALS

Heading direction (HD) cell responses when the rat locomotes on a spiral track in a gravitationally horizontal and vertical plane: During the past year we have completed a new experiment on HD cell responses while rats locomoted along a spiral track (Kim et al 2003). The track could be tilted and rotated. The spiral path compelled the animals to turn through a total angle of 360 degrees in the plane of the track. The rats were initially trained with the track gravitationally horizontal and then tilted, and then finally in a gravitationally vertical plane. When the track was horizontal, and rotated in various directions, most HD cells continued in an allocentric (laboratory) coordinate frame. However, when the track was switched to the vertical, the cells now appeared to switch reference frames and respond with respect to the track itself, regardless of the azimuthal orientation of the track within the room. This result differs from that of our earlier study (Stackman, et al 2000) in which the HD cells of rats crawling onto the gravitationally vertical, inside surface of a cylinder from the floor appeared to remain locked on the laboratory frame.

HD cell responses in parabolic flight: A paper quantifying responses recorded in parabolic flight from seven HD cells in the rat anterior dorsal nucleus of thalamus (ADN) has been completed. (Taube, et al 2002, submitted). We found that cells maintained their direction-specific discharge when the rat was on the cage floor during the 0-g and 1.8 g pull-out periods. However, direction-specific firing was usually disrupted when the rats were placed on the ceiling or wall and there was no single orientation at which the cells fired. There also appeared to be an increase in background firing. At least two cells consistently responded during some parabolas when the rat''s head was oriented 180° opposite the preferred direction of the cell measured when the rat was on the floor. These responses suggest that during these particular parabolas the rats maintained a normal allocentric frame of reference in 0-g and 1-g when on the floor, but when placed on the ceiling or wall in 0-g, the rats appeared to be disoriented (as judged by the loss of directional specificity in HD cell firing). The occasional reversal of HD cell preferred direction across the cage axis of symmetry suggests that the rats may have experienced a VRI. If so, this is the first demonstration in an animal model of a limbic correlate of a human 0-G spatial orientation illusion. HD cell responses during disorientation: In humans, we distinguish three types of spatial disorientation (Gillinham and Previc, 1997): Type I spatial disorientation involves a misperception of orientation and is unrecognized by the observer. Direction-specific firing of HD cells would presumably be maintained in this situation, albeit at an incorrect orientation with respect to the environment. Type II spatial disorientation entails a conscious recognition by subjects that they are disoriented and attempts are then made to become re-oriented by using any available information. Type III spatial disorientation occurs when subject become so disoriented that they are incapacitated. How HD cells respond when a rat experiences the equivalent of Type II or III disorientation is not known. Do HD cells become quiescent, or do they discharge in a random manner with respect to directional heading? Rats were blindfolded and rotated for two minutes in alternating clockwise and counterclockwise directions on a turntable. When rotations were performed at high speeds (for example 240 deg/sec), HD cells from blindfolded rats retained some direction specific firing for the first several platform revolutions, but then the cells showed only a non-direction specific elevation in firing rate. Once the platform was stopped, direction specific firing returned. At lower rotation speeds (less than 90 deg/sec) directional firing remained for a longer period (15-30 seconds), though with some shifting of the preferred direction. When the experiment was repeated with non-blindfolded animals who could view the stationary laboratory surround while rotating, direction specific firing was maintained. Role of semicircular canal afferents in HD cell responses: Our previous work showed that neurotoxic lesions of the vestibular labyrinth in rats disrupted direction-specific rat ADN HD cell firing. This was surprising, because the vestibular nuclei were still intact and likely to have recovered their tonic activity. We first attempted to repeat the experiment by occluding the semicircular canals with a plug, but surgical access in rats proved problematic. Hence, we switched to a chinchilla preparation. Last year we reported that chinchilla ADN HD cells respond in a directional fashion very similar to that of the rat. This year, Dr. Minor (an Investigator on Dr. Shelhamer''s NSBRI neurovestibular project) taught us the chinchilla occlusion procedure, and confirmed they have an impaired VOR after canal plugging. Preliminary ADN recordings show a similar pattern of activity as seen in the Neurotoxin-lesioned rats.

Journal of Vestibular Research 11: 250 (B18.4) , Sep-2003

Journal of Vestibular Research 11: 307 (BP12.4). , Sep-2003

Journal of Vestibular Research 11: 197 (SP6.1). , Sep-2003

2003, Jan-2003

31: 30. , Oct-2002

11(3-5): 338 , Oct-2002

11(3-5): 323 , Jan-2003

28: 584.4 , Oct-2002

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73(3):237 , Oct-2002

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pp. 251-258 , Oct-2002