Physiology&Behavior,Vol. 52, pp. 475-480, 1992

0031-9384/92 $5.00 + .00 Copyright © 1992 Pergamon Press Ltd.

Printed in the USA.

Plasma Corticosterone Response of Rats With Sociopsychological Stress in the Communication Box MASAHIRO

ISHIKAWA, ~ CHIAKI

HARA,

SHIGEHIRO

OHDO

AND

NOBUYA

OGAWA

Department of Pharmacology, E h i m e University School of Medicine, Shigenobu-cho, Onsen-gun, Ehime-ken 791-02, Japan R e c e i v e d 12 A p r i l 1991 ISHIKAWA, M., C. HARA, S. OHDO AND N. OGAWA. Plasma corticosterone response of rats with sociopsychological stress in the communication box. PHYSIOL BEHAV 52(3) 475-480, 1992.--The purpose of present study was to investigate the physiological characteristics of sociopsychological stress induced by the communication box method. In this method, the nonfoot shocked rats were used as the psychologically stressed experimental group. In acute stress experiments, nonfoot shocked rats were exposed to emotional responses from foot shocked rats for 6 h in the light (0900-1500) or in the dark phase (2100-0300). In the light phase, the induced increase in plasma corticosterone levels of nonfoot shocked and foot shocked rats returned to corresponding control levels 6 h following the initiation of stress session, whereas those in the dark phase were significantly higher. Although there were some differences in corticosterone responses between both phases, the acute effect of sociopsychological stress was unclear. Chronic stress experiment with daily exposure for 1 h to sociopsychological stress caused the plasma corticosterone levels of nonfoot shocked rats to increase significantly not only in the postexposure level (just after stress exposure) but also in the preexposure level (before stress exposure) when naive rats were used daily as foot shocked animals. These results suggest that the repeated exposure of sociopsychological stress can induce physiological changes, and stressful situation can be established with only emotional responses from foot shocked rats. Corticosterone

Psychological stress

Communication box

Rats

Adaptation

Sensitization

communication because the conditioned stimuli themselves can induce stomach lesions (7). Recently, Ogawa et al. (30) reported that nonfoot shocked mice also suffered from stomach lesions when exposed to emotional responses arising from foot shocked mice. Namely, the stomach lesions in mice can be caused by an affective communication as exemplified by the monkey study of Miller et al. (24,25). However, little information is available on the physiological characteristics of this phenomenon. Enhancement of plasma corticosterone levels has been demonstrated by exposing animals to various stressful situations described above. Namely, corticosterone levels increase according to the intensity of these stimuli when animals are placed into novel environments or following handling. Furthermore, corticosterone level changes according to the degree of habituation or adaptation when an animal is exposed to physical stress repeatedly. These results suggest that the plasma corticosterone level is a sensitive index to reflect different intensities of psychological or physical stimuli. Therefore, in the present study, the plasma cortieosterone level was used to evaluate the physiological characteristics of sociopsychological stress in the communication box.

S O C I O P S Y C H O L O G I C A L stress is considered to be implicated in etiology of psychiatric or psychosomatic disorders such as depression, neurosis, hypertension, and gastroduodenitis. Various laboratory techniques including immobilization (2,3,20,36), induction of an electric shock (2,13-15,20,27,28,33), exposure to cold environment (20,21,40), inhalation of ether vapor (39), and noise (4,5) have been used in an attempt to simulate sociopsychological stress conditions. Moreover, various situations such as conditioned anxiety (1,37), fear motivated situation (1,22,23), and exposure to new environment ( 1,9,11,31,32) have also been used as models of sociopsychological stress. However, these methods do not always separate psychological factors from physical factors. The c o m m u n i c a t i o n box method developed by Ogawa et al. (29) seems to be an attractive model to study the behavioral and physiological changes under sociopsychological stress, since it can produce an experimental anxiety based on intraspecies emotional c o m m u n i c a t i o n without the direct physical stress. In this method, conditioned stimuli such as light and/ or tone followed by foot shock has previously been used for the development of ulcers in animals (7,8). However, these approaches are not always based on pure intraspecies emotional

l Requests for reprints should be addressed to Masahiro Ishikawa.

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ISHIKAWA ET AL.

~16cm

METHOD

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Male Wistar rats weighing 200-220 g were used. Rats were housed four per plastic cage with woodshavings in a light-controlled room (lights on from 0700 to 1900 h) at a room temperature of 23 _+ 1°C and a humidity of 60 ___ 10% with food and water ad lib. All rats were handled daily for at least 1 week prior to the experiment.

Apparatus A communication box devised by Ogawa et al. (29) was used as the apparatus for setting intraspecies emotional stimuli. This box (64 × 64 X 40 cm) was equipped with a grid floor composed of 0.5 cm diameter stainless steel rods placed 1.3 cm apart. The box consisted of 16 smaller compartments (16 × 16 cm) divided by transparent plastic sheets. Plastic plates were placed on the grid floors of eight compartments to prevent animals from receiving electric shock (Fig. 1). An electric foot shock generator(Tech Serv Inc.) produced foot shocks (2 mA) for a 10-s duration at intervals of 120 s. Rats were randomly divided into three groups as follows. 1. Physical stress group (foot shocked group; FS) consisting of eight rats which were placed into the foot shocked compartments. These animals received foot shock without a warning signal for physical stress. 2. Sociopsychological stress group (nonfoot shocked group; NFS) consisted of eight rats were placed into the nonfoot shocked compartments. These rats never received foot shock but were exposed to various emotional conditioned stimuli from FS. 3. The control group (CON) was placed under the same conditions as NFS on a different day. These rats did not receive either foot shock nor sociopsychological stress from FS.

Preliminary Experiments This study was designed to determine the duration required to reach stable plasma corticosterone levels in the communication box. Rats were randomly divided into two groups: 1. home cage housing group (HCH) as control (n = 5) and 2. experimental group (EXP; n = 7) which were placed in the nonfoot shocked compartments. All treatments were performed between 0900-1030 h. Because plasma corticosterone levels during this period are at the trough of the circadian rhythm and exhibit little variability. The EXP group was individually placed in the nonfoot shocked compartments for 1 h between 0900-1000 h. Blood was drawn from tail vein l h following their placement in the communication box. Blood sampling was completed within 15 s per rat. Blood samples were taken on days 1, 3, and 5 following repeated daily exposure (1 h) of rats to the communication box.

Acute Stress Experiments Change of plasma corticosterone level under acute sociopsychological stress was examined both in the light and in the dark phase. The animals were exposed for 6 h to stressful stimuli 2 h following the onset of light (0900-1500) or dark phase (21000300). Rats were randomly divided into three groups: 1. control group (CON; n = 8), 2. foot shocked group (FS; n = 8) and 3. nonfoot shocked group (NFS; n = 8). Blood was drawn from tail vein at 0, 1, 3, and 6 h after the experiment had started.

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FIG. 1. Schema of the communication box. Foot shock rats were placed individually in the eight shaded areas (foot shock compartments). Sociopsychological stress rats were placed in the eight solid areas (nonfoot shock compartments). Foot shock was delivered through grids of the floor in shaded areas. Solid areas were insulated by plastic plates.

Chronic Stress Experiment This experiment consisted of the following: 1. using the same rats as FS throughout the experiment (chronic Experiment 1) and 2. using naive rats as FS every day (chronic Experiment 2). Thirty-two rats were randomly allocated to the control group (CON) and nonfoot shocked group (NFS). Both of NFS and FS rats were placed in the communication box at 0830. Blood was drawn only from the NFS group at 0845 (NFS preexposure) and the foot shock started at 0900. One hour following stress, exposure blood was drawn from NFS again (NFS postexposure). Blood samples were also taken 1, 3, 5, 7, and 10 days following the experiment. Jumping frequency for FS rats was daily recorded by a video system. After the end of experiment the numbers were scored.

Corticosterone Assay Plasma corticosterone level was determined in duplicate using a modification of the protein-binding radioassay developed by Murphy (26). Immediately after 100 #1 of blood was drawn, the blood sample was centrifuged at 3000 rpm for 15 rain (Kubota KN-70). Twenty-five/~1 plasma was transferred to a 10 ml conic centrifuge tube, extracted with 1 mt of ethyl alcohol by vortexing for 3 min and then centrifuged at 3000 rpm for 15 rain. A 400 ~1 organic layer was transferred to a 10 ml conic centrifuge tube and evaporated to dryness under nitrogen gas. The tube was stored in a desiccator until the assay. One ml solution containing both 0.5% human serum and [l,2,6,7-3H]-corticosterone (0.05 #Ci/ml; NEN Chemicals) was added to the sample. After shaking at 37°C for 10 min, the mixture was incubated at 0°C for 20 min and then 30 mg Florisil (Nakarai, Japan) was added. The sample was kept at 0°C for 3 h and shaken every 30 min. The radioactive material unbound to Florisil was measured by the liquid scintillation counter (Aloka LSC900). The calibration curve for corticosterone exhibited a good reproducibility in the range of 0-80 #g/dl (19). Standard corticosterone was purchased

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Statistical Analysis Results for each experiment presented as means +_ SE (standard error). Corticosterone level patterns were first analyzed with the two-way analysis of variance (ANOVA). Further analysis was made by the Scheff6's test and Student's t-test (two-tailed) to determine the source of detected significance in the ANOVA. Jumping frequencies were analyzed with a Wilcoxon signed rank test. The criterion of significance was set at p < 0.05. All statistical analysis were performed by means of IBM 3090-20J using SAS software (SAS Institute, Japan). RESULTS

Preliminary Experiments The changes of plasma corticosterone (/~g/dl of plasma) response to a new environment (i.e., communication box) is shown in Fig. 2. Plasma corticosterone levels of the E X P group were significantly higher than those of H C H (treatment; F(1, 30) = 14.42, p < 0.01, day; F(2, 30) = 4.00, p < 0.05), especially on day 1 and day 3 [(day 1, EXP; 14.6 _+ 2.5, H C H ; 6.0 _+ 1.7)(day 3, EXP; 13.2 _+ 2.4 H C H ; 5.2 _+ 0.7 #g/dl), p < 0.05]. On day 5, plasma corticosterone levels of EXP group were not significantly different from those of r i C H (EXP; 6.7 _+ 2.1, H C H ; 3.7 + 0.9 #g/dl). Rats repeatedly exposed to the same novel test apparatus (communication box) for 1 h daily appear to adapt by day 5. Therefore, the adaptation period of 5 days was chosen for the subsequent experiments.

Acute Stress Experiments Figure 3 represents the changes of plasma corticosterone response in NFS or FS for 6 h in the light or in the dark phase. A N O V A revealed that there was a significant treatment effect between FS and C O N groups in the light phase as well as in the dark phase [in the light phase: a significant difference in treatment effect, F(2, 84) = 227.99, p < 0.0001; a significant time of day effect, F(3, 84) = 8 i.80, p < 0.0001, and a significant interaction effect, F(6, 84) = 79.35, p < 0.0001] [in the dark phase: a significant difference in treatment effect, F(2, 84) = 30.86, p < 0.0001; a significant time of day effect, F(3, 83) = 12.89, p < 0.0001, and a significant interaction effect, F(6, 84) = 8.79, p

< 0.0001]. The Scheff6 comparisons showed that the plasma corticosterone levels of FS at 1 h differed significantly from other time intervals (p < 0.01). Plasma corticosterone levels of FS group were significantly higher than those of C O N at 1 (FS; 98.3 + 7.4 CON; 2.2 + 0.5 #g/dl, p < 0.01), 3 (FS; 56.2 + 6.1 CON; 1.7 + 0.3 #g/all, p < 0.01), and at 6 h (FS; 8.9 + 1.0 CON; 5.7 + 0.7 #g/dl, p < 0.05) after the initiation of the stress session in the light phase. In the dark phase, similar differences were observed at 1 (FS; 92.0 _+ 15.5 CON; 11.0 + 2.9 #g/dl, p < 0.01), 3 (FS; 30.1 +_ 8.9 CON; 7.2 _+ 1.1 /Lg/dl, p < 0.05), and at 6 h (FS; 34.0 + 4.3 CON; 4.4 + 0.8 #g/dl, p < 0.01) after the stress session. However, unlike the dark phase, the plasma corticosterone levels of FS approached those of C O N group 6 h following stress session in the light phase. On the other hand, there were no significant differences between NFS and C O N in the light phase. However, corticosterone of NFS appeared to be higher relative to those of the C O N group (NFS; 15.3 + 2.5 CON; 4.4

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Chronic Stress Experiment Figure 4 represents the changes of plasma corticosterone responses of NFS and CON when the same rats were used as FS throughout t h e experiment. ANOVA showed that there was a significant treatment effect in postexposure level between NFS and CON, F(1, 70) = 12.48, p < 0.01, but exhibited no significant day effect, F(4, 70) = 1.04, NS. On the other hand, in preexposure levels, there were not significant treatment effect or day effect [treatment; F(1, 70) = 2.58, NS, day; F(4, 70) = 1.95, NS]. The NFS postexposure level increased on day 1 and day 3 compared to the C O N level. The increased levels on day 3 were statistically significant (p < 0.05). Those on day 1 were not significant probably due to the large variance within NFS, but those on day 10 were small but statistically significant (p < 0.05). Figure 5 shows changes in the frequency of j u m p i n g in the FS group. Day effect was statistically significant (p < 0.05). The j u m p i n g frequency of FS on day 1 was four- to fifteenfold higher than those on other days. Thus, the jumping frequency remained at consistently low levels from day 2 to day 10. Figure 6 represents the changes of plasma corticosterone responses of NFS and CON when naive rats were used as the FS group daily. ANOVA indicated that there were significant difference between NFS and CON in the preexposure levels as well as in the postexposure level [i.e., in the preexposure level: a significant difference treatment effect, F(1, 70) = 42.59, p < 0.0001; a significant day effect, F(4, 70) = 7.32, p < 0.0001, and a significant interaction effect, F(4, 70) = 4.04, p < 0.01; in the postexposure level: a significant difference treatment effect, F(1, 70) = 95.86, p < 0.0001; a significant day effect, F(4, 70) = 2.93, p < 0.05, and a significant interaction effect, F(4, 70) = 2.98, p < 0.05]. The Scheff6 comparisons showed that there were significant differences between day 1 and days 7 and 10 in the preexposure level (p < 0.01). Exposure to sociopsychologieal stress caused significant increase in corticosterone levels throughout the 10-day testing period in the NFS postexposure group (day 1, NFS; 14.6 _+ 2.5 CON; 4.9 + 1.2 tzg/dl, p < 0.01). In the NFS preexposure group a similar pattern of increased was observed except the

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significance of difference was apparent on days 5, 7, and 10 (day 5, NFS; 9.4 _+ 1.5 CON; 2.7 +_+_0.6 ~g/dl, p < 0.01). The difference between the preexposure and postexposure level of NFS was kept at all measured points constantly. As shown in Fig. 7, a significant positive linear relationship was found between the preexposure and postexposure level of NFS [r = 0.60, F(1, 38) = 21.0, p < 0.0001 ]. Thus, the increase in the postexposure level in NFS seems to be closely related to that of the preexposure level. DISCUSSION The c o m m u n i c a t i o n box method designed by Ogawa and Kuwahara (29) has been used to investigate the physiological changes caused by sociopsychological stress. The important feature of this method is that an animal exposed to physical stress such as a foot shock can induce sociopsychological stress in another animal by using an intraspecies emotional communication.

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PSYCHOLOGICAL STRESS AND CORTICOSTERONE That is, emotional responses of FS such as struggling, vocalizing, defecating, urinating, and jumping can induce an experimental anxiety in NFS. In the present study, the plasma corticosterone level was measured as an index of an experimental anxiety. However, it is known that brief exposure to a new environment induces a rapid rise in plasma corticosterone (1,9,11,31,32). Thus, it was necessary to familiarize the animals to the communication box. Therefore, preliminary experiments were performed to find the duration required to reach stable plasma corticosterone levels. The plasma corticosterone level of the EXP group returned to control levels on the fifth day and, therefore, an adaptation period of 5 days was used in the subsequent experiments. Acute stress experiments were performed to investigate whether corticosterone response to sociopsychological stress differed in the light phase and the dark phase. Plasma corticosterone levels of NFS and FS returned toward control levels 6 h after the stress exposure in the light phase, whereas those in the dark phase were still higher. The maximum mean plasma corticosterone level of FS in the light phase was similar to that in the dark phase. This result seems to reflect a ceiling effect on the upper limit of eorticosterone response to stress. Similar findings have been reported for the adrenal hormones response to immobilization stress (6,38). On the other hand, the increased plasma corticosterone levels of NFS seemed to be much larger in the dark phase than in the light phase. The variance of corticosterone level in the dark phase was also much larger than that in the light phase. However, the increase in the ratio of NFS to CON on the plasma corticosterone level at 1 h after the stress session was much larger in the light phase than in the dark phase (light: 300%, dark: 199%). Thus, the corticosterone response to stressful stimuli seems to vary with the time of day when the stress is applied. A larger corticosterone response is observed when stressful stimuli is applied at the nadir rather than at the peak of the corticosterone rhythm (6,16). Our present findings support these results. Although therewere some differences in corticosterone response between the light and dark phase, physiological changes of sociopsychological stress were unclear under acute stress experiments. In the chronic Experiment 1, the change of plasma corticosterone level in NFS was investigated using the same ES rats throughout the study. The NFS postexposure levels showed a tendency to increase on days 1 and 3, but afterward returned to CON levels. There was no significant difference in the preexposure levels between NFS and CON. In this experimental situation, the jumping response of the FS group decreased rapidly following the second day. Hormonal response to repeated stress shows similar adaptation or habituation such that repeated exposure to the same stress evokes less of a hormonal response to each stress session (17,18,20,33,35). Therefore, this change of the NFS plasma corticosterone level seems to be due to the de-

479 creased intensity of sociopsychological stress associated with the decreased jumping response of FS under chronic foot shock. These results suggest that a constant emotional response exposure is necessary for the FS group to show a physiological response. Thus, naive rats were used as FS daily to avoid the reduction in the emotional responses. The NFS postexposure level increased daily depending on the repeated exposure to sociopsychological stress. Although there was no significant increase in the NFS postexposure level on day 1 in chronic Experiment 1, a significant difference between NFS and CON was observed. This discrepancy is not clear. The elevation of the NFS postexposure level seems to be related not only with the direct sociopsychological stress but also with the increased NFS preexposure level because the relationship between postexposure and preexposure levels shows a significant positive correlation and the difference between preexposure and postexposure is constant. Psychological stress has been reported to cause an acute mild enhancement of noradrenalin turnover in the hypothalamus and amygdala which was increased further by repeated exposure to stress (12). The increased NFS postexposure corticosterone levels in the present investigation supports these findings. Moreover, the NFS preexposure level as well as the NFS postexposure level increased significantly by the repeated exposure to sociopsychological stress. NFS seems to be undergoing sensitization rather than adaptation, since the NFS preexposure level increased with the repeated exposure to sociopsychological stress. As for the NFS preexposure level, the psychological stimuli imply two factors. One is the acquired experience of a prior stress episode and the other is the communication box environment itself. Relative to the latter factor, the former effect seems to play a more important role in the sociopsychological stress because the NFS preexposure level did not increase in the chronic Experiment 1 where the same FS group was used daily. Therefore, the elevation of the NFS preexposure level may reflect buildup of a predictable anxiety based on the repeated experience of a prior stress episode. Recently, it has been shown that unpredictable (e.g., irregularly applied) aversive events are more stressful and provoke more arousal or anxiety than predictable events (e.g., regularly applied) with warning signals (4,5,34). However, the stress situation in the present study differs from the cited reports because the sociopsychological stress induced by emotional response in the FS group can increase a predictable anxiety without warning signals. We observed not only physiological changes induced by direct sociopsychological stress but also effects for reflecting buildup of a predictable anxiety when naive rats were used daily as the FS group. In summary, the present study suggests that a stressful situation can be established by means of emotional response only, and strongly support our previous report that stomach lesions were induced by sociopsychological stress (30). Therefore, the communication box method seems to be a valuable tool for setting sociopsychological stress and can induce an experimental anxiety based on sociopsychological stress.

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Plasma corticosterone response of rats with sociopsychological stress in the communication box.

The purpose of present study was to investigate the physiological characteristics of sociopsychological stress induced by the communication box method...
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