Motion sickness in guinea pigs (Cavia porcellus) indexed by body rotation-induced conditioned taste aversions

Physiology& Behavior,Vol. 47, pp. 467--470. ©Pergamon Press plc, 1990. Printed in the U.S.A.

0031-9384/90 $3.00 + .00

Motion Sickness in Guinea Pigs (Cavia porcellus) Indexed by Body Rotation-Induced Conditioned Taste Aversions K L A U S - P E T E R O S S E N K O P P A N D M A R G I T T A D. O S S E N K O P P

Department of Psychology, University of Western Ontario, London, Ontario, Canada, N6A 5C2 R e c e i v e d 5 S e p t e m b e r 1989

OSSENKOPP, K.-P. AND M. D. OSSENKOPP. Motion sickness in guinea pigs (Cavia porcellus) indexedby body rotation-induced conditioned taste aversions. PHYSIOL BEHAV 47(3) 467--470, 1990. --The presence of motion sickness in albino guinea pigs (Cavia porcellus) was examined by using a conditioned taste aversion (CTA) as an index. Eighteen animals were divided into three groups. One group received four pairings of a novel 0.15% saccharin solution followed by 20 min of body rotation at 70 rpm (on a schedule of 15 see on and 5 see off). Another group received four pairings of the saccharin solution followed by exposure to sham rotation. The third group experienced the rotation procedure following access to water. The group receiving the rotation procedure contingent on presentation of the novel saccharin taste exhibited a conditioned aversion to this fluid (relative to the control groups) over days of acquisition (p<0.01), which subsequently dissipated when rotation was no longer contingent on the presentation of the saccharin solution (extinction). These data thus demonstrate the presence of motion sickness in guinea pigs when CTA is used as an index. Body rotation

Motion sickness

Conditioned taste aversion

MOTION sickness is a phenomenon observed in a wide variety of animal species (26). In humans motion sickness is a syndrome involving such signs as pallor and cold sweating, and symptoms such as nausea and vomiting. Experimental evidence for motion sickness in nonhuman primates [e.g., (7, 19, 42)], cats and dogs [e.g., (2, 9, 28, 41)] and shrews (23) is well established when an emetic response is used as the criterion response. Anecdotal evidence for motion sickness in horses, cows, seals and various kinds of birds is available [see (8,21)], as is evidence for motion sickness in fish (8,22). Not all vertebrate species possess an emetic reflex (3) and thus, cannot vomit when subjected to the appropriate vestibular stimulation. Pozerski (34) reported that rabbits, guinea pigs, chickens and pigeons were immune to motion sickness because these species did not vomit when subjected to rhythmically oscillating body motion. However, it is not clear that these species possess an emetic reflex and the absence of vomiting during or following vestibular stimulation cannot be taken as evidence for immunity to motion sickness. Rats lack an emetic reflex (18), yet display behaviors indicative of motion sickness [of. (12, 25, 30)]. When a novel taste stimulus has been paired with immediate exposure to body rotation or other types of vestibular stimulation in rats [e.g., (4, 13, 15, 16, 20, 29, 38)], subsequent strong avoidance of this taste stimulus has been observed. This conditioned taste aversion (CTA) induced by exposure to the vestibular stimulation has been taken as evidence for the presence of motion sickness [see (32)].

Guinea pigs

Similar motion sickness-induced CTAs have been found in other nonemetic species, such as mice (14) and japanese quail (33), as well as in species capable of vomiting, such as cats (9), squirrel monkeys (35,43), and humans (1,24). Conditioning of these taste aversions in such a variety of emetic and nonemetic species may involve similar mechanisms (32). In the present study we examined the formation of a conditioned aversion to a novel saccharin taste in guinea pigs subjected to body rotation about a vertical axis. Guinea pigs previously have been conditioned to avoid gustatory (e.g., saccharin taste) and visual cues (e.g., color) in the formation of poison-based aversions (5,6). Furthermore, these experiments showed that taste cues were more important than visual cues in the formation of these conditioned aversions. Thus, the present experiment examined the acquisition and extinction of a body rotation-induced CTA to a novel taste cue. METHOD

Subjects Eighteen male albino guinea pigs (Cavia porceUus) were individually housed in stainless steel cages (19 x 25 × 43 cm). The animals were kept in a colony room on a 12 hr light:12 hr dark cycle with lights on from 0700 to 1900 hr and with a temperature of approximately 20"C. The guinea pigs weighed 240 to 300 g at the start of the experiment and were kept on ad lib food (Purina)

467

468

OSSENKOPP AND OSSENKOPP

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FIG. 1. Mean group saccharin solution intake across days of the conditioning and extinction phases. Error bars are standard errors of the mean. See text for explanation of the group labels.

for the duration of the experiment.

Rotation Apparatus The apparatus for producing the rotational stimulation consisted of a turntable capable of revolving at 70 rpm and a 32 × 32 × 32 cm clear Plexiglas chamber mounted on the turntable [see (31) for a photograph]. The turntable was programmed to rotate for 15-sec periods separated by 5-sec periods of no rotation. Another Plexiglas chamber of the same dimensions could be placed on a surface of the apparatus adjacent to the turntable such that animals in this chamber would be subjected to the noise and vibration of the apparatus but would not be rotated. This condition was designated as a sham rotation condition.

Conditioning Procedure Phase 1. Acquisition. The guinea pigs were randomly assigned to 3 equal groups and all animals were adjusted to a 23.5 hr/day water deprivation procedure (11), with water available for 30 min in the morning. On Days 12-14 of the deprivation schedule,

baseline water intake of each guinea pig was measured. On Days 15-22, 30-min access to a 0.15% (w/v) sodium saccharin solution in the home cages was provided to all subjects on odd-numbered days, and tap water was available for 30 min on even-numbered days. Immediately following the presentation of saccharin on odd-numbered days, guinea pigs from group S-R (n = 6) were placed in the Plexiglas chamber and exposed to the rotation procedure for 20 min. Subjects from group S-S (n = 6) were given 20 min of sham rotation following exposure to saccharin. Subjects in the third group (W-R, n = 6) remained in their home cages on odd-numbered days following exposure to saccharin. Immediately following presentation of water on even-numbered days, group W-R was exposed to the rotation procedure for 20 min and groups S-R and S-S remained in their home cages. Thus, animals in group S-R were rotated following presentation of the conditioned stimulus (CS), subjects in group S-S experienced only the noise and vibration of the apparatus following CS presentation, and group W-R experienced rotation only following presentation of water. Fluid (water or saccharin solution) was presented in the home cage in glass cylinders with stainless steel drinking spouts containing ball bearings to minimize leakage. Plastic dishes located beneath the animal cages were used to catch any fluid spilled during the drinking period, and appropriate adjustments were made in calculating each guinea pig's daily fluid intake. Phase 2. Extinction. On Days 23-32 all guinea pigs continued to receive 30-min presentation of the taste CS on odd-numbered days and 30 min of access to water on even-numbered days. However, the rotation and sham rotation procedures were discontinued and the guinea pigs remained in their home cages during this phase of the experiment.

Data Analysis The dependent variables consisted of fluid intake on each of the conditioning and extinction days. Data for fluid intake during phase 1 and 2 were analyzed separately with mixed design repeated measures analysis of variance and post hoc comparisons were done with the Newman-Keuls procedure. Significance levels were set at a =0.05 for purposes of hypothesis testing. RESULTS

Acquisition Phase Analysis of variance of the baseline water intake by each of the

TABLE 1 G R O U P M E A N AMOUNTS O F WATER INTAKE (ml) D U R I N G THE BASELINE, ACQUISITION, A N D EXTINCTION PHASES O F THE STUDY

Days Baseline Group

Acquisition

Extinction

1

2

3

4

1

2

3

4

S-R

29.1 (1.9)*

25.1 (1.8)

27.5 (1.5)

30.8 (2.5)

30.8 (2.2)

34.6 (3.9)

32.8 (2.4)

29.1 (1.6)

33.3 (1.1)

S-S

28.5 (1.0)

28.9 (2.8)

29.5 (2.4)

24.3 (3.3)

36.5 (2.6)

29.4 (3.3)

31.9 (1.4)

28.9 (2.2)

35.5 (3.1)

W-R

28.2 (1.1)

28.8 (2.0)

29.7 (2.2)

26.7 (0.6)

30.9 (1.7)

29.3 (2.3)

30.2 (2.0)

33.3 (3.8)

32.8 (2.3)

*Numbers in the parentheses are standard errors of the mean.

MOTION SICKNESS IN GUINEA PIGS

groups (see Table 1) revealed no significant differences (F
Group mean saccharin solution intake levels during the extinction phase are presented in Fig. 1. During this phase, group S-R showed an increase in CS fluid intake over days, relative to the other two groups. By the end of the extinction phase all 3 groups showed comparable levels of saccharin intake. Statistical analysis of the extinction data (trial 5 of acquisition and trials 1-4 of extinction) provided support for extinction of the CTA, which had developed in group S-R during the acquisition phase. A significant groups by trials interaction, F(8,60)= 2.92, p =0.008, reflected the relatively rapid increase in saccharin solution by group S-R to levels comparable to the other two groups. Post hoc comparisons revealed no significant differences between groups S-R and S-S by trial 1 of the extinction period, suggesting fairly rapid extinction of the induced CTA. Statistical analysis of the water intake data during this phase (see Table l) revealed no significant effects with all ps>0.20.

DISCUSSION The finding that, by the end of the conditioning phase, the

469 group receiving the novel taste followed by vestibular stimulation (group S-R) exhibited significantlylower saccharin solution intake than the two control groups (S-S and W-R) clearly demonstrates the presence of a body rotation-induced CTA in guinea pigs. Previous studies have shown that these animals can acquire a CTA to a novel taste paired with lithium toxicosis [e.g., (5,6)]. The induction of a CTA with body rotation can be taken as evidence for susceptibility to motion sickness in this species [cf. (32)] and also demonstrates that body rotation is an effective nonpharmacological UCS. Comparison of the present data to previous studies on body rotation-induced CTA in rats, which used similar types of rotation procedures and a one-bottle test to index the CTAs [e.g., (29,30)], reveals some similarities in CTA formation between rats and guinea pigs. Both species show increasing levels of saccharin intake when this taste is paired with sham rotation. When the saccharin taste is paired with body rotation both species show a relative decrement in saccharin intake across conditioning trials (i.e., in comparison to the sham-rotated animals). Fluid deprivation levels of course reduce the degree of aversion shown by subjects when tested with the one-bottle test procedure. In contrast, when rats are tested with two-bottle test procedures during body rotation-induced taste aversions (29), an across trial reduction in preference ratio for the conditioning fluid can be demonstrated. Guinea pigs would be predicted to show similar across trial reductions in CS preference when two-bottle tests are employed. The observation that subjects in Group S-R often would bite the drinking tubes when presented with saccharin solution on trials 2 and 3 of the acquisition period provides additional support for the conditioned aversive nature of the taste CS. Such behavior was not observed in the S-S control group or group W-R and may represent a conditioned somatic response reflecting a shift in palatability of the saccharin taste in group S-R. A previous study [cf. (17)] similarly noted that rats would bite the edge of a food dish that contained a CS previously paired with an illness-inducing UCS. Another study examined in a quantitative fashion the expression of target biting in rats when conditioned with a saccharin-lithium gustatory avoidance procedure (40). High target biting rates were associated with avoidance of the CS taste stimulus. It has been considered an evolutionary anomaly that motion sickness should occur at all, as the success of a species does not seem to be enhanced by such a response. Triesman (39) suggested that ingestion of some toxic foods produces perceptual distortions or sensory conflicts very similar in nature to the effects of excessive vestibular stimulation. The subsequent expression of an emetic response (if present in the species), or formation of a CTA to the food containing the toxin, is clearly advantageous if the purpose is to clear the digestive tract of the poisonous food or to avoid further ingestion of the food. Vomiting and formation of a CTA in response to certain kinds of vestibular stimulation, which mimic the effects of some toxins, may just be a cost of having a detection system for ingested toxins (39). Several studies have noted that the vestibular system seems to be involved in how the organism responds to drugs or poisons [e.g., (27,36)]. Because guinea pigs presumably might encounter food items containing natural toxins, to which a conditioned avoidance response would clearly be advantageous, the presence of motion sickness in this species would be predicted by Triesman's hypothesis. Finally, the demonstration of motion sickness in guinea pigs is of importance since a substantial body of evidence exists concerning the physiology of vestibular function in these animals [e.g., (10,37)] and, together with the present findings, suggest that this species may be a useful animal model of motion sickness with relevance to the human condition.

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