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The Journal of Neuroscience, August 15, 1998, 18(16):6599-6607
Interleukin-1 Induces Slow-Wave Sleep at the Prostaglandin D2-Sensitive Sleep-Promoting Zone in the Rat Brain
Akira Terao1, 2, Hitoshi Matsumura1, 3, and Masayuki Saito2 1 Department of Molecular Behavioral Biology, Osaka Bioscience Institute, Suita City, Osaka 565-0874, Japan, 2 Laboratory of Biochemistry, Department of Biomedical Sciences, Graduate School of Veterinary Medicine, Hokkaido University, Sapporo 060-0818, Japan, and 3 Department of Neuropsychiatry, Osaka Medical College, Takatsuki City, Osaka 569-8686, Japan
ABSTRACT
Top
Abstract
Introduction
To determine the site of action of the sleep-promoting effect of interleukin-1 (IL-1), we continuously infused (between 11 P.M. and 5 A.M.) murine recombinant IL-1
into seven different locations in the ventricular and subarachnoid systems of the brain in freely moving rats. When IL-1 was infused at 10 ng/6 hr into the subarachnoid space underlying the ventral surface of the rostral basal forebrain, which previously was defined as the "prostaglandin (PG) D2-sensitive sleep-promoting zone" (PGD2-SZ), the total amount of slow-wave sleep (SWS) increased by 110.7 min (IL-1 was 208.1 ± 14.3 min vs control at 97.4 ± 9.3 min; n = 8; p < 0.01 by paired Student's t test) from the baseline control level obtained under continuous infusion of saline vehicle. The hourly SWS during the infusion period reached the level of daytime SWS, the physiological maximum, whereas paradoxical sleep (PS) was decreased transiently. This site of action for the SWS promotion was dissociated from the site in the third ventricle sensitive to the IL-1-mediated PS suppression, fever, and anorexia. The SWS increase caused by IL-1 infusion into the PGD2-SZ was blocked completely by coadministered diclofenac, a nonselective cyclooxygenase (COX) inhibitor. Pretreatment of rats with NS-398 or piroxicam (3 mg/kg of body weight, i.p.), which are said, respectively, to possess high and relative specificity for the COX-2 enzyme, also blocked the SWS-promoting effect of IL-1. We present a hypothesis that IL-1 induces SWS, at least in part, via COX-2-mediated PG production in the PGD2-SZ.
Key words: interleukin-1; prostaglandin D2; slow-wave sleep; subarachnoid space; ventral surface of the rostral basal forebrain; COX-2
INTRODUCTION
A variety of studies has demonstrated the important role of interleukin-1
) (for review, see Borbély and Tobler, 1989
On the other hand, a prostaglandin (PG) D2-sensitive sleep-promoting zone (PGD2-SZ) was demarcated in the rat within the ventral surface of the rostral basal forebrain, where PGD2 applied into the subarachnoid space of the zone during the night increased the SWS of this nocturnal animal up to the daytime level, the physiological maximum (Matsumura et al., 1994
Thus, both IL-1 and PGD2 possess sleep-promoting potency. It may be noted generally that IL-1 and PGs share some biological effects such as induction of fever (Dinarello et al., 1983
In this study we searched in freely moving rats for the site of action for the SWS-promoting effect of IL-1 and found that IL-1 increased SWS in the most pronounced manner when it was applied to the PGD2-SZ. This site of action was dissociated from the site(s) responsible for other effects of IL-1, such as suppression of paradoxical sleep (PS) and induction of fever and anorexia. Furthermore, inhibitors of cyclooxygenase (COX), which is said to be the rate-limiting enzyme for the synthesis of PGs, clearly were demonstrated to block the SWS promotion caused by IL-1. We hypothesize that IL-1 promotes SWS via activated synthesis of PGs in the PGD2-SZ.
MATERIALS AND METHODS
Animals. One hundred and sixty-eight male rats of the Sprague Dawley strain (Japan SLC, Hamamatsu City, Japan), weighing between 300 and 380 gm (9-10 weeks old), were used. The animals were housed before experimentation in a soundproof chamber at an ambient temperature of 25°C and 60% relative humidity. The chamber was maintained on a 12 hr light/12 hr dark cycle (lights on at 8 A.M.), and standard laboratory rat chow and water were supplied ad libitum. All animal use procedures were approved by the Animal Care and Use Committee of Osaka Bioscience Institute.
Surgical operation. Under pentobarbital anesthesia (50 mg/kg of body weight) each animal was chronically implanted with electrodes for recording the electroencephalogram and electromyogram as well as with a thermistor probe for monitoring brain temperature, as described previously (Matsumura et al., 1991
0.8; L, 0.0; D, 8.5; midline); L3, in the lateral ventricle (A,
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Figure 1. Schematic sagittal and coronal drawings indicating the seven locations (L1 through L7) for infusing IL-1 into the ventricle and subarachnoid space in the rat brain. Numerals indicate the distance from bregma, the reference point, in the stereotaxic coordinates. L1, In the subarachnoid space of the PGD2-SZ; L2, in the 3V, apposed to the medial preoptic area; L3, in the lateral ventricle; L4, in the subarachnoid space underlying the posterior hypothalamus; L5, in the 3V, near the aqueduct of Sylvius; L6, between the aqueduct of Sylvius and the fourth ventricle, apposed to the locus coeruleus; L7, in the cisterna magna.
Materials. Murine recombinant IL-1
Diclofenac sodium (Sigma, St. Louis, MO) was dissolved in saline and continuously and bilaterally infused at 46 µg (145 nmol) per 6 hr in total (between 11 P.M. and 5 A.M.) into the PGD2-SZ, together with IL-1. Piroxicam (Sigma) and NS-398 (Cayman Chemicals, Ann Arbor, MI) were dissolved separately in dimethyl sulfoxide (DMSO) and further diluted in saline (1:1) before use. Either one (500 µl) was injected intraperitoneally at 3 mg (~9 µmol) per kilogram of body weight 3.2 hr before the commencement of the administration of IL-1.
Experimental procedures. After surgery each rat was allowed a minimum 9 d recovery period in an individual cage before being placed in our originally developed experimental cage (Matsumura et al., 1995
In the first series of experiments (n = 120) a solution of IL-1 was infused into one of the seven locations described above. The total dose of IL-1 that was infused ranged from 0.1 to 100 ng/6 hr, which corresponded to the IL-1 concentration of the test solution from 4.0 × 10
11 to 4.0 × 10
Analysis of data. Duration of wakefulness, SWS, and PS was measured on the generated polygraph recordings, based on the visual judgment by an expert of the sleep-wakefulness states. The minimal scoring interval was set at 0.25 min of recording time. All results were expressed as the mean ± SEM. Statistics were performed by the use of paired Student's t test or ANOVA, depending on the experimental design. The Student-Neuman-Keuls multiple comparison test was used as the post hoc. Differences were considered to be significant at p < 0.05.
RESULTS
Effects of IL-1 at the seven locations in the brain
To determine the site of action of IL-1, we infused 10 ng of IL-1 continuously for 6 hr (between 11 P.M. and 5 A.M.) into seven different locations of the rat brain (Fig. 1). Total amounts of SWS, PS, and food intake plus the average brain temperature during the 6 hr period of IL-1 infusion were compared with corresponding baseline values. The deviations of the experimental values obtained by the IL-1 infusion from corresponding baseline levels were calculated and averaged (Fig. 2).
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Figure 2. Changes in SWS, PS, brain temperature, and food intake from respective baseline levels caused by the 6 hr (from 11 P.M. to 5 A.M.) infusion of IL-1. The difference between the experimental level by the IL-1 infusion and the baseline level (control) under the infusion of saline vehicle was calculated for each rat; each column indicates the mean ± SEM of the differences obtained in this manner in a group of rats (n = 8 each) ascribed to the experiment for one of the seven locations. *p < 0.05, **p < 0.01 by paired Student's t test, compared between the IL-1 experiment and vehicle baseline. §p < 0.05, §§p < 0.01 compared among the changes for the seven locations by Student-Newman-Keuls test following one-way ANOVA, wherein the mark above L1 in the panel for SWS and that above L2 in the panel for
Regardless of the site of infusion, the total amounts of SWS that appeared during the IL-1 infusion period were increased significantly over their corresponding baseline levels. However, the magnitude of these SWS increments differed greatly, in a site-dependent manner. When IL-1 was infused into L1, an extraordinary increase in SWS by 110.7 min (IL-1 was 208.1 ± 14.3 min vs control at 97.4 ± 9.3 min; n = 8; p < 0.01 by paired Student's t test) was attained. In contrast, infusion into any of the other six locations produced only mildly increasing responses (24.1-61.9 min). Thus, the increment attained at L1 was significantly larger than the increments at the other six locations (p < 0.01 by Student-Neuman-Keuls multiple comparison test following one-way ANOVA; F = 6.460; p = 0.0001).
Infusion of IL-1 into L2 caused a significant decrease in the total amount of PS (IL-1 was 7.0 ± 2.1 min vs control at 19.6 ± 1.8 min; n = 8; p < 0.01 by paired Student's t test), whereas infusion into the other locations resulted in marginal changes.
Infusion of IL-1 also caused fever and anorexia at all seven locations that were examined. Fever was induced most severely at L2 among the seven locations (p < 0.01 by Student-Neuman-Keuls multiple comparison test following one-way ANOVA; F = 11.345; p = 0.0001). The degree of anorexia caused by the infusion of IL-1 into L2 was also significantly more severe than that seen under infusion into L1 or L7 (p < 0.05 by Student-Neuman-Keuls multiple comparison test following one-way ANOVA; F = 11.345; p = 0.0167).
Comparisons of the effects between L1 and L2
Because SWS was promoted most effectively by IL-1 at L1, whereas L2 was the site for the most severe fever and anorexia, dose-dependent (Fig. 3) and time-dependent (Fig. 4) responses were examined further at these two locations.
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Figure 3. Changes in SWS, PS, brain temperature, and food intake caused by the 6 hr infusion of IL-1 at different doses from respective baseline (control) levels. See Figure 2 for the method of calculation. Each datum point represents the mean ± SEM of eight rats. , Results by IL-1 infused into L2;
, results by IL-1 infused into L1. *p < 0.05, **p < 0.01 by paired Student's t test, compared between the IL-1 experiment and the baseline under saline infusion. §§p < 0.01 by repeated two-way ANOVA between L1 and L2.
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Figure 4. The 24 hr profiles of SWS, PS, brain temperature, and food intake in rats that received IL-1 into L1 and L2.
Dose-related responses
Infusion of IL-1 into L1 and L2 caused similar dose-dependent increases in SWS, with respective maximum levels at 10 ng/6 hr of infusion (Fig. 3). However, the magnitude of the overall responses was significantly larger at L1 when compared with that at L2 (F = 13.932; p = 0.0004 by repeated two-way ANOVA). Furthermore, at a rate of 0.1 ng/6 hr the infusion of IL-1 into L1 increased SWS from the baseline by 15.1 min with statistical significance (p < 0.05 by paired Student's t test), whereas infusion into L2 caused no significant change. The infusion of IL-1 into L1 apparently increased PS at 0.1-1 ng/6 hr but decreased it at 10-100 ng/6 hr, with statistical significance at 100 ng/6 hr (p < 0.01 by paired Student's t test). On the other hand, PS was dose-dependently suppressed at 0.1 ng/6 hr and above when IL-1 was infused into L2. These profiles of PS for L1 and L2 differed significantly from each other (F = 4.342; p = 0.0409 by repeated two-way ANOVA). Infusion of IL-1 also raised the brain temperature at 0.1 ng/6 hr and above, regardless of the site of infusion at L1 or L2. However, site L2 appeared to be more sensitive than L1 in raising the temperature (F = 14.704; p = 0.0003 by repeated two-way ANOVA). Significant decreases in food intake were observed under the infusion of IL-1 into both L1 and L2 at 1 ng/6 hr and above. However, the dose-dependent decrease for L2 was significantly more severe than that for L1 (F = 10.733; p = 0.0017 by repeated two-way ANOVA).The 24 hr profiles
In the time-dependent profiles of SWS (Fig. 4) the amount of SWS during the first hour of the IL-1 infusion was not increased greatly from the corresponding baseline levels in either L1 or L2 profile; i.e., the duration of latency before the increase in SWS was not greatly different between the two locations. However, from the second hour of IL-1 infusion the hourly mean SWS reached its maximum level in the profile for L1, whereas the maximum level was attained only at the last hour of the infusion in the profile for L2. It is notable that, when IL-1 was infused into L1, the hourly SWS level increased to a level comparable to that of daytime SWS, which is the physiological maximum. Incidentally and interestingly, the rebound decrease in SWS appeared to be more severe in the profile for L2 during the light period after the IL-1 infusion, in contrast to the marginal rebound in the profile for L1, in which significant rebound was observed transiently only between 9 and 10 A.M. Thus, in the profile for L2 in comparison with that for L1, the smaller increase in SWS by IL-1 was followed by a larger decreasing rebound. With regard to PS, brain temperature, and food intake (Fig. 4), their responses were more outstanding in the profiles for L2 than in those for L1 from the viewpoints of latency before the onset of marked responses and the magnitude of the responses. In these profiles no rebound phenomena were noticeable, at least within the time duration shown in Figure 4.Analyses of SWS episodes
The state of SWS is composed of episodes, with each duration varying from several seconds up to several minutes. The duration of all SWS episodes was measured, and the values were averaged on an hourly basis (Fig. 5L1-A,L2-A). Under the IL-1 infusion into L1 (Fig. 5L1-A) the average episode duration for the second hour of the infusion period was prolonged significantly when compared with the corresponding average value calculated from the baseline-day recording (mean duration of SWS episodes for IL-1 experiment was 2.21 ± 0.17 min vs baseline at 1.48 ± 0.20 min; n = 8; p < 0.01 by paired Student's t test). A histogram comprising the numbers of SWS episodes with lengths within respective ranges is shown for this hour (Fig. 5L1-B). It indicates that the numbers of episodes were increased irrespective of their length. It is notable that the number of SWS episodes with a duration >3 min or even the number of those episodes >6 min was increased greatly by IL-1 and that the number of SWS episodes of shorter duration also was increased. In contrast, the infusion of IL-1 into L2 shortened the average duration of SWS episodes during the fourth and fifth hour after the commencement of IL-1 infusion (Fig. 5L2-A). The histogram for the SWS episodes during the fourth hour (mean duration of SWS episodes for IL-1 experiment was 0.96 ± 0.08 min vs baseline at 1.29 ± 0.11 min; n = 8; p < 0.01 by paired Student's t test) indicates that the numbers of episodes <2 min were increased but that episodes with longer duration were suppressed mainly by the infusion of IL-1 into L2 (Fig. 5L2-B).
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Figure 5. Changes in the hourly mean of SWS episode duration caused by the IL-1 infusion. L1-A, The 24 hr profiles of the hourly mean of the SWS episode duration on the baseline day (
Incidentally, it is also notable that the average duration of SWS episodes was shortened markedly during the light period that followed the IL-1 infusion. This shortening of SWS episodes appeared to be longer lasting in the profile for L2 (Fig. 5L2-A) than in that for L1 (Fig. 5L1-A). It is likely that the rebound decreases in SWS in Figure 4 were caused, at least in part, by the shortening of SWS episodes.
Effect of COX inhibitors on the SWS promotion
Coadministration of the nonselective COX inhibitor diclofenac (46 µg/6 hr) with IL-1 (10 ng/6 hr) to L1 resulted in the disappearance of the SWS-promoting effect of IL-1 (Figs. 6A vs 4L1) as well as in that of its effects on brain temperature and food intake (data not shown). The rebound decrease in SWS during the light period that followed the IL-1 infusion (Fig. 4L1) was not visible, either, after this coadministration. Neither the elongation of the average SWS episode during the second hour of the IL-1 infusion period nor the shortening of SWS episodes during the rebound phase after the IL-1 infusion (Fig. 5L1-A) became visible (Fig. 6B). Thus, those changes in SWS and SWS episodes produced by IL-1 infusion completely disappeared by the addition of diclofenac.
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Figure 6. Effect of COX inhibitors on the SWS-promoting effect of IL-1 in L1. Shown are the 24 hr profiles of the hourly amount of SWS (A) and those of the hourly mean of the SWS episode duration (B) in rats that received the coinfusion into L1 of IL-1 (10 ng/6 hr) and diclofenac sodium (46 µg/6 hr) between 11 P.M. and 5 A.M. (indicated by the shaded area).
The SWS-promoting effect of IL-1 (Fig. 6C) as well as its effects on brain temperature and food intake (data not shown) also were blocked by NS-398 and by piroxicam, which are said, respectively, to possess high and relative specificity for the COX-2 enzyme (Futaki et al., 1994
DISCUSSION
Site of action
Among the seven locations that were examined, L1 appeared to be the most effective in promoting SWS (see Fig. 2), a region that previously was reported by our group to be the site of action for the SWS-promoting effect of PGD2 (Matsumura et al., 1994
In contrast to the SWS response, other parameters were found to be affected most markedly by the infusion of IL-1 into L2 among those sites that were examined (see Fig. 2). The PS response varied according to the site of infusion from L1 through L7, but a statistically significant change from the baseline was attained only at L2. Thus, it is likely that IL-1 inhibited PS by acting at the region adjacent to the 3V.
The pyrogenic and anorectic effects of IL-1 also were outstanding when IL-1 was infused into L2. The anorectic effect was concordant with those previous results that were demonstrated with continuous infusion of IL-1 into the 3V (Plata-Salamán, 1994
Effect of IL-1 on SWS episodes
During the increase in SWS that was caused by IL-1 infusion into L1, the number of SWS episodes increased regardless of the length range of the episodes (see Fig. 5L1-B); i.e., both long and short episodes increased in number. This feature was strikingly different from the feature observed in the SWS increase brought about by IL-1 infusion into L2 (see Fig. 5L2-B), wherein episodes with short duration increased but those with long duration were suppressed. Because IL-1 activates both the hypothalamic-pituitary-adrenal system (Sapolsky et al., 1987
Involvement of COX in the effects of IL-1
It is postulated that COX in the brain plays a critical role in the central actions of IL-1 such as fever (Dinarello et al., 1983
In the current study, however, not only IL-1-induced fever and anorexia (data not shown) but also SWS promotion were all blocked completely by COX inhibitors (see Fig. 6). The blocking of the SWS-promoting effect of IL-1 by the COX inhibitor also became manifest from the finding that, not only during the IL-1 infusion but also during the expected rebound phase after IL-1 infusion, IL-1-induced changes in the length of SWS episodes were abolished by the addition of diclofenac (see Figs. 6B vs 5L1-A).
We infer that in the study of Krueger and colleagues (1982)
Diclofenac is a general inhibitor of COX regardless of subtypes of the enzyme, i.e., COX-1 and COX-2, whereas inhibitors NS-398 and piroxicam, respectively, are said to possess high and relative specificity for the COX-2 (Futaki et al., 1994
There was a time lag between the commencement of IL-1 infusion and the onset of the increase in SWS, which was calculated to be ~55 min. In a previous study of our group (Matsumura et al., 1994
Role of PGs in the promotion of SWS
At this moment there is no report on whether PGD2 production is augmented by an IL-1 challenge in vivo, but the PGE2 level reportedly rose in response to intravenous injection of IL-1 in some brain areas, including the OVLT (Komaki et al., 1992
It was shown previously that PGE2 possessed a wakefulness-promoting potency in rats and monkeys, which was brought about by its action in the diencephalon (Matsumura et al., 1988
also promoted SWS in the same study. Thus, these three PGs were all SWS-promoting in the zone; therefore, it is plausible without any contradiction that hyperproduction of PGH2 is an important step in the promotion of SWS triggered by the infusion of IL-1 into this zone of the rostral basal forebrain.
Type 1 IL-1 receptor (Ericsson et al., 1995
FOOTNOTES Received Jan. 16, 1998; revised June 1, 1998; accepted June 4, 1998.
This work was supported in part by funding from the program Grants-in-Aid for Scientific Research of the Ministry of Education, Science, and Culture of Japan and from the Special Coordination Funds for Promoting Science and Technology of the Science and Technology Agency of the Japanese Government, as well as by Grant 8A-6 from the program Research Grants for Nervous and Mental Disorders of the Ministry of Health and Welfare and by a grant from the Naito Foundation. A.T. was supported by a fellowship of the Japan Society for Promotion of Science. We are grateful to Drs. Kiyoshi Matsumura, Chunyu Cao, Shinsuke Satoh, Yoshihiro Urade, and Osamu Hayaishi (Osaka Bioscience Institute) for valuable discussions and Dr. Larry D. Frye for critical reading of this manuscript. We also thank Tomoko Nakajima, Keiko Kasahara-Orita, Nobuko Konishi, and Miyako Matsumura for their excellent technical assistance.
Correspondence should be addressed to Dr. Hitoshi Matsumura, Department of Neuropsychiatry, Osaka Medical College, 2-7 Daigakumachi, Takatsuki City, Osaka 569-8686, Japan.
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