Chronic noise stress and insulin secretion in male rats

Physiology& Behavior,Vol. 34, pp. 359-361. Copyright©Pergamon Press Ltd., 1985. Printed in the U.S.A.

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Chronic Noise Stress and Insulin Secretion in Male Rats A . A R M A R I O , * J. M . C A S T E L L A N O S t

A N D J. B A L A S C H *

*Departamento Fisiolog(a Animal, Facultad de Ciencias, Universidad Aut6noma de Barcelona, Bellaterra and tLaboratorio Hormonas, Hospital General Valle Hebr6n, Barcelona, Spain R e c e i v e d 2 J a n u a r y 1984 ARMARIO, A., J. M. CASTELLANOS AND J. BALASCH. Chronic noise stress and insulin secretion in male rats. PHYSIOL BEHAV 34(3)359--361, 1985.--The effect of chronic noise, followed by acute noise and forced swimming, on basal glucose and insulin levels was studied in adult male rats. Chronic noise did not modify basal levels of either measured variable before or after the exposure of rats to acute stress. Acute noise decreased serum glucose and insulin levels, although hypoglycemia was transient. Forced swimming decreased insulin and increased glucose levels. Our results indicate that: (1) serum insulin levels were sensitive to both physiological and psychological stresses, (2) forced swimming caused more marked glucose and insulin responses than noise exposure, (3) chronic intermittent noise did not alter pancreatic function, and (4) no sign of adaptation was apparent after repeated exposure to noise. Insulin

Glucose

Chronic stress

Noise

Forced swimming

IT has been clearly established that different types of acute stresses induce hyperglycemia and decreased insulin release in animals, including humans [12, 13, 17, 19, 20]. The reduced insulin secretion has been attributed to high sympathetic activity during stress, as cateeholamine-stimulation of a-adrenergic receptors in the pancreas inhibit insulin release [16]. It has been suggested that chronic stress could be an ethiological factor of diabetes in man [9,10]. In addition, the hormones released during stress such as catecholamines, adrenocorticotropin (ACTH) and corticosteroids have been reported to affect insulin secretion [7, 11, 14, 15, 18, 21, 22]. However, the effect of experimental models of chronic stress on insulin secretion has received little attention [23,24]. This work was designed to study the effect of chronic intermittent noise on serum insulin and glucose levels in adult male rats and to show whether or not insulin response changes after repeated exposure to the same stress stimulus.

to noise for 21 days. On the morning of the 22nd day they were killed by decapitation between 8.00 and 9.00 a.m. within 25 sec after being taken from their home cage. In the second experiment the rats were assigned to two groups: (a) control; and (b) chronic noise for 21 days. On the morning of the 22nd day, between 8.00 and 11.00 a.m., rats from both experimental groups were quickly killed without being stressed, or alternatively, exposed to acute stress for 10, 30 and 60 min. The acute stresses used were noise (with the same characteristics indicated above) and forced swimming in a water tank (50 cm diameter and 60 cm high, temperature= 18°C). Animal house, stress room and decapitation room were separated by at least one door. The trunk blood was collected in plastic tubes at 4°C and centrifuged (10 min, 2500 rpm) at the same temperature. Serum was frozen at -20°C. Insulin was determined by radioimmunoassay (Serono) and glucose by colorimetry with the glucose-oxidase method. To avoid interassay variations all serums were processed in the same assay. Statistical significance of the effects of acute and chronic treatments were assessed with A N O V A previous log transformation of data to achieve homogeneity of variances. When appropriate, individual comparisons of means were determined by the Tukey test.

METHOD Male Wistar rats (approximately eight weeks old) were maintained in groups of four per cage in a controlled quarter (temperature 24°C, light on from 6.00 to 18.00), water and food (Panlab rat chow) were available ad lib. On arrival the animals were randomly assigned to experimental groups. Chronically stressed animals were daily exposed to the noise provoked by an alarm bell (85 dB) between 8.00 and 12.00 a.m. In the first experiment the rats were assigned to three groups: (a) control, rats left undisturbed in the animal house for 21 days; (b) 5 days of chronic noise, rats left undisturbed in the animal house for 16 days and exposed to noise for the last five days; and (c) 21 days of chronic noise, rats exposed

RESULTS The effect of daily noise stress on basal serum glucose and insulin levels is depicted in Table 1. Neither 5 nor 21 days of exposure to noise modified glucose and insulin levels 20 hours after the last stress session. Table 2 shows the glucose response to noise and forced swimming stresses in control and chronically stressed

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ARMARIO, CASTELLANOS

TABLE 1 THE EFFECT OF CHRONIC NOISE ON BASAL GLUCOSE AND INSULIN LEVELS IN ADULT MALE RATS Glucose (mg/100 ml)

Days of chronic noise 0 5 21

70,

Insulin (mU/ml)

137.1 ± 2.3 (7) 141.8 ± 4.6 (4) 138.4 ± 3.5 (7)

AND BALASCH

50,

52.4 ± 2.8 (7) 50.1 ± 6.8 (4) 60.6 ± 5.5 (7)

E

30

Z

Means - SEM are represented. Number of animals per group in parentheses. The values were measured 20 hours after the last stress session.

10

30

60

10

30

60

60 animals. T h e a n a l y s i s o f v a r i a n c e r e v e a l e d a significant effect o f t h e a c u t e s t r e s s p e r i o d s ( p < 0 . 0 5 for noise, p < 0 . 0 0 1 for f o r c e d s w i m m i n g ) b u t n o t o f p r e v i o u s c h r o n i c t r e a t m e n t ( c o n t r o l vs. noise) o n b l o o d glucose. While a t r a n s i e n t b u t significant ( p < 0 . 0 5 ) fall in s e r u m g l u c o s e w a s o b s e r v e d a f t e r 10 m i n o f noise e x p o s u r e , f o r c e d s w i m m i n g i n d u c e d a signifi c a n t ( p < 0 . 0 1 ) i n c r e a s e in s e r u m g l u c o s e a f t e r all s t r e s s periods. A significant effect o f a c u t e stress periods ( p < 0 . 0 5 for noise, p < 0 . 0 0 1 for f o r c e d s w i m m i n g ) b u t n o t o f p r e v i o u s c h r o n i c t r e a t m e n t o n insulin s e c r e t i o n was f o u n d (Fig. 1). T h e d e c r e a s e in insulin levels w a s m o r e m a r k e d a f t e r f o r c e d s w i m m i n g t h a n a f t e r noise in all t h e s t r e s s p e r i o d s ( p < 0 . 0 1 ) . DISCUSSION O u r d a t a clearly i n d i c a t e t h a t a c u t e stress d e p r e s s e d insulin release in k e e p i n g w i t h p r e v i o u s r e p o r t s [12, 13, 17, 20]. T h i s d e c r e a s e was m o r e c o n s p i c u o u s a f t e r f o r c e d s w i m m i n g t h a n a f t e r noise, p e r h a p s b e c a u s e s w i m m i n g was a m u c h

~'~40 E 7' ,,.J

--~

20,

0

FIG. 1. The effect of previous chronic noise on basal and acute stress-induced insulin secretion. Means and SEM are represented. Open bars indicate non-chronically stressed and closed bars chronically stressed rats. Number under bars indicate the period of acute stress (min). In each group n=5. The analysis of variance revealed non significant effect of previous chronic treatment on insulin response to both acute stresses. Therefore, the statistical significance of periods of acute stress on insulin secretion was assessed taking both chronically and non-chronically stressed rats together. * p<0.05, ,k,k p<0.01 vs. non-acutely stressed animals.

TABLE 2 THE EFFECT OF 21 DAYS OF PREVIOUS CHRONIC NOISE ON BASAL AND ACUTE STRESS-IHDUCED GLUCOSE (MG/100 ML) LEVELS IN ADULT MALE RATS Chronic treatment Acute noise stress (min) 0 Control Noise

135.2 ± 1.8 141.2 ± 0.8

10" 132.6 ± 3.7 130.0 ± 3.0

30 137.8 ± 138.2 ±

60 5.1 2.1

139.2 ± 138.2 ±

2.6 2.1

Forced swimming stress (min) 0 Control Noise

137.2 ± 3.4 137.0 ± 4.8

10t 199.2 ± 7.8 189.8 ± 4.8

30t 239.4 ± 13.1 252.2 ± 22.2

6O 230.6 ± 10.9 250.4 ± 18.9

Means ± SEM are represented. In each group n=5. *p<0.05, tp<0.01 vs. non-acutely stressed animals. The analysis of variance indicated non significant effect of previous chronic treatment on glucose response to both acute stresses. Therefore, the statistical significance of periods of acute stress on glucose levels was assessed taking both chronically and non-chronically stressed rats together.

INSULIN SECRETION AND CHRONIC STRESS

361

greater stress than noise, as suggested by A C T H response [4]. Serum glucose response to both stresses was qualitatively different: while forced swimming increased serum glucose in all periods after the onset of stress, noise induced a slight decrease in serum glucose 10 min after noise exposure with a return to pre-stress levels in spite of continued exposure to the stress. Since it is well-accepted that stress induces hyperglycemia [ 13,19], we cannot offer an explanation for this transient hypoglycemia in noise-stressed rats, but the results indicate that changes in blood glucose and insulin levels are dissociated during stress. The glucose levels observed during stress could be the results o f two opposite mechanisms; the hyperglycemic effect of catecholamines and glucocorticoids released during stress [8], and the a-adrenergic inhibition of insulin secretion [20]. It seems possible that forced swimming could induce both a-adrenergic inhibition of insulin secretion [8] and fl-adrenergic reduction in serum glucose clearance [8], whereas noise would induce only cz-adrenergic inhibition of insulin secretion. The effect of chronic stress on insulin secretion has received little attention. Recently, it has been reported that chronic electric foot-shock could raise basal insulin levels in rats [23,24]. In contrast, we have not observed any effect o f 5 and 21 days o f chronic noise on basal serum insulin in the present work. This discrepancy could be attributed to the different intensities of the stress agents. Thus, foot-shock might be considered a greater stress as indicated by the high

corticoadrenal activity found in the morning following the last stress session [24]. Conversely, chronic noise does not modify the weight of the endocrine # a n d s [5,6] nor does it alter the basal levels of anterior pituitary hormones and corticosterone 20 hours after the last exposure to the stress [1,15]. These data indicate that noise is a mild stress and the alterations induced by daily exposure to this stress are transient as being confirmed by the lack of effect on glucose and insulin responses to the same stress or to another (swimming) applied acutely. Our results suggest that insulin response to stress does not adapt after repeated experience with a stressful stimulus. We have previously reported that some, but not all, anterior pituitary hormones show some degree of adaptation to repeated exposure to noise [2-4]. Physiological mechanisms underlying the dissociation between different endocrine systems in response to chronic stress are not know. Regarding the lack of adaptation in insulin response to repeated noise stress, it is noteworthy that both medulloadrenal and pituitary-adrenal responses are reduced by repeated exposure to a stressful stimulus [2, 4, 16]. Since both systems influence serum glucose and insulin levels [22], it might have been expected that previous chronic stress could alter their responses to the same stress. Since this was not the case, our data suggest that physiological factors controlling insulin secretion during acute and chronic stress are at present poorly understood and that they require further study.

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