Animal experiments in 0G

Does the CNS actually maintain an internal allocentric coordinate frame in weightlessness that establishes a "floor"-like navigation plane? Over the past two decades, the neural basis of spatial memory in humans and animals has become better understood based on electrophysiological studies in animals, and functional neuroimaging in humans. Portions of the limbic system, including the hippocampus, post-subiculum, thalamic nuclei, and entorhinal cortex function together to interrelate various external (e.g. visual) and internal (e.g. vestibular and haptic) sensory cues and determine place and direction relative to the environment. Wiener and Taube (2005) provide a comprehensive review. One type, "head direction" cells (Taube, 1998), are found in several limbic areas and consistently discharge as a function of a rat's head direction in the spatial plane the animal is walking in, independent of place or head pitch or roll up to 90 degrees. The direction of maximum response ("preferred direction") varies from cell to cell. The range of firing is typically about 90 degrees. The preferred directions of the entire ensemble of cells reorient in unison when distant visual landmarks in the room are rotated about the animal. Comparable cells have also been found in primate. Head direction cells in turn provide the essential azimuthal reference input to at least two other classes of limbic cells: "grid cells" (Hafting et al., 2005) and "place cells" (Best et al., 2001) that ensemble code various attributes of the rat's location- also in the two dimensional plane of the animal's locomotion. (It is important to note that though these particular cell classes respond in a 2D plane, the animals show 3D orienting behavior. Presumably there are other as-yet-undiscovered limbic cell classes that code other orientation or place attributes in third dimension defined by the orientation of this 2D locomotion plane - e.g. height, elevation angle or roll angle).

A critical question is the extent to which gravity anchors the orientation of the response plane of these cell classes. In 1-G laboratory experiments, head direction cells usually maintain directional tuning when the animal climbs a vertical wall, but if the rat crawls inverted across a gridded ceiling, many cells show reduced directional tuning, or lose it entirely (Calton and Taube, 2005). In parabolic flight experiments, we monitored rat head direction cell responses while animals in a visually up-down symmetrical cage successively experienced 1G, 0G and 1.8G (Taube et al., 2004). Allocentric directional tuning was maintained in 0-G while the animal crawled on the familiar floor of the cage, despite the absence of gravity.

Figure 13-8. Rat head direction cell directional tuning curves on cage ceiling and floor during 0-G parabolic flight. Data recorded on ceiling indicated with arrow (Taube et al., 2004).

Figure 13-8. Rat head direction cell directional tuning curves on cage ceiling and floor during 0-G parabolic flight. Data recorded on ceiling indicated with arrow (Taube et al., 2004).

When we manually transferred the rat to the ceiling in 0-G, most cells lost directional tuning, and statistically showed an increase in overall background firing level, which could reflect an instability in orientation perception. We predicted that if the rat occasionally experienced a VRI and adopted the ceiling rather than the floor as the navigation reference plane, but continued to use a primary visual landmark to determine azimuth, the preferred firing direction should flip across the visual axis of symmetry of the cage. Bursts of firing in other than the original preferred direction occurred on the ceiling in several animals, and in some animals were 2-3 times more frequent in the expected ceiling-preferred directions than in the original floor-preferred directions. Fig. 13-8 shows the ceiling and floor tuning curves for one such cell, which shifted through about 180 deg in azimuth. Such shifts in azimuth may correspond to the common human perception during a 180 degree VRI that one is in a familiar but somehow mirror-reversed place, since objects remembered on the left are now to be found on the right.

In a related experiment conducted in on the Neurolab Shuttle mission, Knierim et al. (2000, 2003) recorded place cell activity as trained rats walked across three surfaces defining the corner of a cage. Their path required a yawing 90 degree turn while on each surface, followed by a pitching 90 degree turn to move onto the next surface. After a total of 3 yaws and 3 pitches, they returned to the original starting point. The investigators' original hypothesis was that in 0-G only the yaw rotations would be taken into account, and the animal would have to yaw 360 deg. and traverse four successive surfaces to do it before the same place cell would fire again. However, when tested on the fourth flight day, one animal's place cells responded in only a single area of the 6 turn track, suggesting this animal had incorporated the pitch rotations, and was maintaining a 3D allocentric sense of place within the cage. In the other two animals, place cell fields were abnormal, with one of them exhibiting symmetric firing fields on each successive surface. We suggested that this would fully be expected if the animal experienced the equivalent of human VRIs: After each pitch back, the view of the track ahead was virtually identical on each surface, so they might have the illusion of traversing the same one turn segment of the track three times in succession. The third animal did not exhibit consistent place fields - which might be expected if it was disoriented, and simply following the track using a route strategy. However when tested after five more days in weightlessness, the place fields of the second and third animals appeared unimodal, suggesting they had learned to orient to the entire cage, rather than successive locomotion surfaces.

Taken together, these experiments show that even in the physical absence of gravity, limbic head direction and place cells in animals responses define a two dimensional navigation plane parallel to the "floor" of the animal's environment. In 0-G if the animals crawl or are placed on adjacent or opposite surfaces, direction and place tuning can disappear or change in ways suggesting the navigation plane has reoriented into alignment with the adjacent or opposite surface. Note that humans and animals not only spatially "re-orient", but also "re-position". We cannot ask animals their perceptions of surface identities, but the neural behavior of their limbic navigation plane in 0-G does correspond to that posited for humans, based on the character of 0-G disorientation and VRIs.

So far head direction and place cell responses have been characterized only in terrestrial animals. It is interesting to speculate about what we will ultimately find in other vertebrate species. Birds, marine mammals and cartilaginous fish rely on dynamic lift to oppose gravity, and usually fly/swim upright. Most bony fish have gas bladders, which ballast them upright. Certain species - notably the marine mammals - apparently have the ability to remain allocentrically oriented while performing multiple graceful rotations about axes perpendicular to gravity, yet it is ecologically important for them to remain allocentrically oriented with respect to the ocean surface or bottom. Do marine mammals have a more robust ability than rodents and humans apparently do to maintain allocentric orientation when gravitationally inverted or in weightlessness? To what extent can vertebrate limbic neural networks reorganize during life to respond to new environmental challenges?

0 0

Post a comment