Behavior

Gravity plays an important role on behavioral responses such as maintenance of posture, swimming, walking, and the control of eye or head movements. It is, therefore, not surprising that both microgravity and hypergravity affect these types of behavior significantly in adults as well as in developing animals.

Eye and head movements offer the best possibility for a highresolution quantification of the standard developmental behavioral characteristics in vertebrates, in particular fish and amphibians. Reflexive eye movements are induced by stimulation of the vestibular sense organs, the so-called Vestibulo-Ocular Reflex (VOR). In some insects, compensatory head movements are induced by a change in body position, measured either by proprioceptors of the legs, or by special gravity sensing organs at the end of the abdomen (see Figure 5-01). The extent of these compensatory eye or head movements is clearly related to the animal's position relative to gravity and can, therefore, be measured as relative angular displacements (Horn 1985). Measurements include the reflex amplitude, i.e., the maximum displacement during a 360° lateral roll tilt of the animal, or the reflex gain, i.e., the ratio between eye angle and body angle. These measurements can be expressed as a function of the age of the animal. For this reason, the effects of altered gravity on eye and head movements can be detected with a higher stage-related resolution than by recording swimming, walking, or maintenance of upright posture.

Stage 14/16 group

0 60 120 180 240 300 360 Posture of Animal (°)

Figure 5-15. Development of the static roll-induced vestibulo-ocular reflex in a fish (Oreochromis mossambicus) during spaceflight. When the animal is tilted to one side, its eyes roll in the other direction. The postflight sine-like response characteristics from young fish flown in 0 g are compared with those of fish raised in 1 g. The developmental stage at onset of the microgravity period is indicated in each plot. Note that the young stage was sensitized by microgravity (STS-84 mission), as shown by the increased amplitude of eye movements. The older group (flown on the STS-55 mission) was not affected by microgravity.

«V

30-

0

m

20-

X

10-

■s. >

0-

-10-

CL

-20-

5J

>.

0 60 120 180 240 300 360 Posture of Animal (°)

30

"cs

20

1

1

10

>

0

c

o

-10-

o

Cu

-20-

<L>

w

.if).

0 60 120 180 240 300 360 Posture of Animal (°)

4.3.1 Compensatory Eye and Head Movements

Eye and head movements with respect to the gravitational vector that are induced by stimulation of the gravity sensing organs can be observed in many animals including vertebrates, cephalopods, crustaceans, or insects. The basic shape of the response characteristics is sine-like. This response is very reproducible: repeated recordings have revealed that short-term adaptation of the roll-induced response is weak or absent in the clawed toad Xenopus (Horn 2004).

Developmental characteristics of this response have been determined with a high stage-related resolution for three species: the fish Oreochromis mossambicus, the amphibian Xenopus laevis, and the house cricket Acheta domesticus. Their developmental characteristics differ in some respect. In Xenopus, gain and amplitude of the roll-induced Vestibulo-Ocular Reflex (rVOR) are the largest in young tadpoles during the period of limb development. After that period, in particular during the maturation of the cerebellum, the rVOR decreases towards a final constant level (Horn et al. 1986).

In Oreochromis, rVOR gain and amplitude also increase during early life. After reaching a maximum, it decreases during the formation of visual-vestibular connections, and later on it increases until maturity of the fish (Sebastian and Horn 1999). In crickets the gain of roll-induced head movement increases continuously after each molt until the final molt to an adult cricket (Horn and Foller 2001).

Microgravity modified the rVOR of young immature Oreochromis and Xenopus tadpoles. In very young fish that had not yet developed a functional rVOR response before entering into microgravity, the rVOR was augmented after a 10-day spaceflight. In older fish that were able to perform the rVOR at launch, no difference in the rVOR was found with respect to the ground control animals (Sebastian et al. 2001) (Figure 5-15).

In Xenopus, the effects were more complex. During the spaceflight, some of the tadpoles developed a dorsalization of the tail, a so-called tail lordosis, while other tadpoles developed normally. The dorsalized tadpoles that did not have a functional rVOR at launch showed a depressed rVOR after landing, while normal, "undorsalized" tadpoles were unaffected with respect to the ground controls. Older tadpoles that could perform the rVOR at launch and developed a dorsalized tail behaved like the younger group, i.e., their reflex was depressed (Figure 5-16). But those tadpoles from that older group with normal tails showed an augmented rVOR after the flight (Sebastian et al. 1996, Sebastian and Horn 1998, Sebastian and Horn 2001).

However, microgravity did not affect the compensatory head response of Acheta domesticus (Figure 5-17), although the activity of its PSI was strongly affected by microgravity (see Figure 5-11).

so-70-

,_^

60-

O

S

50-

cL S

40-

<

30-

O

20-

>

iO-

Og-lg lg

Figure 5-16. In the experiment with the amphibian Xenopus laevis, the duration of 0 g exposure was modif ied during the spaceflight (STS-84 mission) by means of an onboard centrifuge. Tadpoles were exposed to 0 g throughout the mission (Og), during the second half of the mission only (Ig-Og), during the first half of the mission (Og-lg), or they were exposed to 1 g throughout the mission (lg). The rVOR amplitude represents the maximal extent of eye movement during a 360 deg lateral roll body tilt. Only the Og and the Ig-Og groups show dorsalized tails after landing of the spacecraft. The extent of this dorsalization is ranked from 0 (norma!) to 3 (extreme). The lg-Og and the 1 g groups did not develop a dorsalization. Note that the rVOR amplitude is clearlv related to the extent of the dorsalization (Sebastian and Horn 2002).

I"3

ri^ht down left i/dw ri^ht down left i/dw

0 60 120 180 240 300 360 Body Roll Tilt {")

6th instar

60 120 180 240 300 360 Body Roil Ti!t (a)

Figure 5-17. Compensatory head tilt induced by a body roll tilt of crickets Acheta domesticus after a 16-day spaceflight. The sketch on the lower right shows the compensatoiy head response. V. vertical axis; H, dorsoventral axis of the head; T, dorsoventral axis of the thorax. These axes are colinear in the norma/ position of the cricket, but differ if the animal is tilted in roll, a, compensatory head roll tilt; y, roll body tilt. At launch, the animals were either at an embryonic stage shortly before hatching (egg) or they had reached the 6,h instar stage. Note that, for both developmental stages, microgravity exposure had no effect on the response characteristics, i.e. this behavior was insensitive to an exposure to microgravity. Adapted from Horn et al. (2003).

60 120 180 240 300 360 Body Roil Ti!t (a)

Figure 5-17. Compensatory head tilt induced by a body roll tilt of crickets Acheta domesticus after a 16-day spaceflight. The sketch on the lower right shows the compensatoiy head response. V. vertical axis; H, dorsoventral axis of the head; T, dorsoventral axis of the thorax. These axes are colinear in the norma/ position of the cricket, but differ if the animal is tilted in roll, a, compensatory head roll tilt; y, roll body tilt. At launch, the animals were either at an embryonic stage shortly before hatching (egg) or they had reached the 6,h instar stage. Note that, for both developmental stages, microgravity exposure had no effect on the response characteristics, i.e. this behavior was insensitive to an exposure to microgravity. Adapted from Horn et al. (2003).

Figure 5-18. This cartoon shows the sequence (from 0 to 3) of body movements 0 made by neonatal rats (P0) during righting after being placed on their back on a

Nevertheless, the increased response of the young fish and tadpoles after microgravity exposure can be considered as an increase in sensitivity of the vestibular response. It is interesting to note that such increase in sensitivity of the vestibular system was also obtained in some adult fish (Boyle et al. 2000) and in astronauts (Clément et al. 2001) after exposure to microgravity.

Figure 5-18. This cartoon shows the surface.

sequence (from 0 to 3) of body movements 0 made by neonatal rats (P0) during righting after being placed on their back on a

4.3.2 Righting Response

Righting responses from a supine posture to a prone posture are common in animals. Beside the vestibular system, tactile cues from the contact with the solid surface, as well as proprioceptive cues from muscle spindles and tendons contribute to a successful righting response.

It is well know that the strategy of this type of response changes during development. For example, newborn rats assume a U-shaped posture (ventroflexion) followed by a rotation of the head, neck, and shoulders, with forepaw support (Ronca and Alberts 2000). The last step is a rapid axial rotation, a response known as the corkscrew behavior (Figure 5-18). By contrast, adult rats execute a complete lateral (axial) roll without any U-shape of the body (Kalb et al. 2003). For this reason, this righting response is a good experimental model to test maturation of vestibular function.

In addition, to separate the contribution of vestibular from other sensory inputs, such as touch, the righting response can be studied during water immersion, i.e., the animal is positioned in the supine position in a water-filled container and then released (Figure 5-19).

Testing this type of righting behavior, both on land and in water, can start on the day of birth (P0).

Synchronous Flight

Figure 5-19. This cartoon shows the sequence of body movements during the righting response in water by neonatal rats raised on Earth (Synchronous) or exposed to microgravity (Flight). Left: Pups raised in 1 g. Right: Pups raised in microgravity.

Synchronous Flight

Figure 5-19. This cartoon shows the sequence of body movements during the righting response in water by neonatal rats raised on Earth (Synchronous) or exposed to microgravity (Flight). Left: Pups raised in 1 g. Right: Pups raised in microgravity.

Prenatal animals were exposed to microgravity during the beginning of morphological and physiological development of the vestibular apparatus. This exposure significantly altered postnatal maturation of righting.

On a solid surface, attempts for righting were achieved by all neonates at the day of birth. Usually, 50% of these attempts were successful and the animal reached the prone position with both forelimbs in contact with the surface, independent of whether they were bom from microgravity-exposed dams or from 1-g ground (vivarium and synchronous) controls (Figure 5-20).

Figure 5-20. Percentage of neonatal rats showing successful contact righting response after exposure to microgravity (Flight) and in the control groups. The vivarium group (Vivar) includes animals in standard laboratory conditions. The synchronous group (Synchro) is considered as the real ground-control group, because the animals were reared under the same conditions, including feeding and caging, and schedule as the flight animals.

Flight Synchro Vivar

However, righting behavior from the supine to prone position in the water immersion test, i.e., in the absence of tactile cues, revealed clear response deficits in neonates that underwent prenatal development in space (Ronca and Alberts 2000). This deficit persisted until postnatal day P3. Normalization of righting took place at P5 (Figures 5-19 and 5-21).

Exposure to microgravity (STS-90) during postnatal periods of life significantly retarded the development of this righting behavior. Indeed, rats launched at postnatal day P14 and tested on the day of landing showed a U-shape posture, which is typical of immature behavior. In contrast, the axial rotation clearly dominated in the ground control animals (Kalb et al. 2003).

Figure 5-21. Only flown P5 neonatal rats showed successful righting response during water immersion. By contrast, flown PI and P3 neonates (Flight) showed abnormal behavior compared to the vivarium group (Vivar). * p<0,05. Adapted from Ronca and Alberts (2000) and Plaut et al. (2000).

4.3.3 Locomotion

Locomotion is strongly affected by the gravity load because the legs are regularly moved with and against the gravitational force. Thus, it was assumed that gravity-related information contributed to the patterns of leg movements. To test the impact of load deprivation on locomotion, young animals were exposed to tail suspension or to microgravity. During suspension, the fore limbs wear the weight of the animal, while the hind limbs are unloaded (Figure 5-22, left). Suspended animals move their forelegs similar to non-suspended animals while hind limbs provide a torque such that the young rats walk in circles.

The studies revealed that a suspension applied to the animals from postnatal days P13 to P31 induced an increase in the ankle angle during walking. This increase persisted for more than one month thereafter. After exposure to real microgravity for 9 days during the NIH.R3 mission, the analysis of free walking showed differences in hind limb and forelimb joint

Figure 5-21. Only flown P5 neonatal rats showed successful righting response during water immersion. By contrast, flown PI and P3 neonates (Flight) showed abnormal behavior compared to the vivarium group (Vivar). * p<0,05. Adapted from Ronca and Alberts (2000) and Plaut et al. (2000).

0 0

Post a comment