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The Journal of Neuroscience, August 13, 2003, 23(19):7281-7287
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Stress-Related Modulation of Hippocampal Long-Term Potentiation in Rats: Involvement of Adrenal Steroid Receptors
Volker Korz andJulietta U. Frey Department of Neurophysiology, Leibniz-Institute for Neurobiology, D-39118 Magdeburg, Germany
Abstract
Top
Abstract
Introduction
Stress is usually correlated with an increased release of glucocorticoids from the adrenal glands. Within the hippocampus, a structure long known to be involved in spatial learning, two corticosterone-binding receptors are identified: the glucocorticoid receptor (GR) and the mineralocorticoid receptor (MR). Activation of these receptors impairs or facilitates hippocampal long-term potentiation (LTP), respectively. Stress elicited by behavioral manipulations may interfere with cognitive modulations of LTP during learning experiments. Here, we explore the influence of two stress-inducing procedures, handling and swimming, on the maintenance of dentate gyrus LTP in the rat induced by a weak tetanization of the perforant path. Manipulations started 15 min after tetanization. Handling alone resulted in a complete reversal of LTP. Handling followed by a 2 min swim in a water tank elicited prolonged protein synthesis but not-adrenergic-dependent LTP compared with either control or handled animals. Blockade of the GRs but not of the MRs prevented the reversal of LTP by handling. Inactivation of the MRs but not of the GRs hindered LTP prolongation by swimming. Because the activated receptor complexes act as transcription factors, MR- and GR-related proteins may play a role in the maintenance of LTP. The data suggest a complex interplay of corticosterone-binding receptors on modulations of hippocampal LTP and thus, of stress on learning and functional plasticity in general.
Key words: hippocampal long-term potentiation; swim stress; corticosterone; glucocorticoid receptor; mineralocorticoid receptor; dentate gyrus;
Introduction
Stress is well known to modulate hippocampal long-term potentiation (LTP) as well as learning and memory (Kim and Diamond, 2002) and is usually evoked when animals are introduced into an apparatus used for testing spatial cognition (Morris, 1984
Long-term potentiation can be divided into two major phases: protein synthesis-independent early LTP (3-4 hr) and protein synthesis-dependent late LTP with a duration of at least up to 8 hr (Krug et al., 1984
Similar behavioral reinforcements of an electrically induced early LTP in vivo by appetitive or aversive emotional stimuli were found under mild stress conditions (Izquierdo and Medina, 1995
This study aimed to examine stress effects on early DG-LTP within a vulnerable time window, with emphasis on the activation of corticosterone-binding and
Materials and Methods
Electrode and cannula implantation
Male Wistar rats (8 weeks of age) were anesthetized with Nembutal (40 mg/kg, i.p.). A monopolar recording electrode was implanted stereotaxically into the granule cell layer of the dentate gyrus [coordinates: antero-posterior (AP), -2.8; lateral (L), 1.8 from bregma, 3.2-3.5 ventral from dura] and a bipolar stimulation electrode was implanted into the perforant path (coordinates: AP, -6.9; L, 4.1, 2.2-2.5 ventral from dura) of the right hemisphere; coordinates are based on the atlas of Paxinos and Watson (1998Electrophysiological recording
Rats were placed into a recording box (40 x 40 x 40 cm), and the electrodes were connected to a swivel by a flexible cable. This allowed the freely moving animals ad libitum access to food and water. The responses were amplified (differential amplifier, Inh; Science Products, Hochheim, Germany), transformed by an analog-to-digital interface (CED 1401+; Cambridge Electronic Design, Cambridge, UK), and stored on a personal computer. Biphasic constant current pulses (0.1 msec per half wave) were applied to the perforant path to evoke DG field potentials of40% of the maximum PSA. Because the spike is required to induce LTP, the preparation was optimized to obtain a population spike. This influences the dipole of the field EPSP in the hilus, making the recording of the PSA more preferable than that of the EPSP. After registering a stable baseline for 1 hr, LTP was induced by weak tetanic bursts (three bursts of 15 pulses of 200 Hz with 0.2 msec duration of each stimulus and 10 sec interburst interval; same stimulus intensity as for PSA testing). Two minutes and then every 15 min after tetanization, five test stimuli (10 sec interpulse interval) were delivered and the mean values of field potentials were stored for 8 hr. A 24 hr value was obtained the next day. For analysis and presentation, the 15 min recordings were averaged in groups of four to yield 1 hr values. The 2 min value served as control to determine whether a sufficient initial potentiation (with no more than 25% difference between individual animals) had been obtained.
Tetanization and experimental manipulations were always performed between 10:00 and 11:00 A.M. to avoid interferences with the diurnal rhythm of corticosterone titers.
Stress procedures and experimental groups
The swim stress apparatus was a circular plastic water tank 1.82 m in diameter and 58 cm in height filled with water up to a level of 38 cm. The water temperature was 25 ± 2°C. Water was made opaque by a white latex fluid (Sakret, Giessen, Germany). For behavioral manipulations, all animals were used only once.Control group. Animals in this group received a weak tetanus and were then left undisturbed in the recording chamber.
Swimming group. Rats in the swimming group were placed in the maze 15 min after tetanus for a 2 min swim. They were then dried with a towel and transferred back into the recording chamber. Before swimming, the electrodes were protected from water immersion by petroleum jelly.
Handling group. The handling group was identical to the swimming group in every respect, except that animals were not transferred into the water tank.
Hormone analysis
Blood samples of all groups were collected at the same time of day after decapitation of the animals. Blood samples were taken from parallel groups of animals that had not been implanted with electrodes. However, the experimental and handling procedures were exactly the same as for the implanted animals, with the exception of the absence of recording or LTP induction. Rats were killed 15 min after either swimming or handling. Trunk blood was sampled within 25-30 sec from opening the cache and handling the animal. Blood was allowed to coagulate on ice in an Eppendorf tube. Then the blood was centrifuged, and the serum was stored at -20°C. Samples were analyzed by radioimmunoassay (RIA) within 4-8 weeks. RIA was performed as described previously (Stefanski et al., 2001Pharmacology
Glucocorticoid receptors were blocked by mifepristone, and mineralocorticoid receptors were blocked by spironolactone (150 ng, i.c.v. each; Sigma, St. Louis, MO). Both substances were dissolved in ethanol and then brought up to 1 ml volume with 0.9% saline with a final concentration of 50 ng/µl (2% ethanol). The control solution consisted of 0.9% saline (2% ethanol). The solutions were injected at 1 µl/min to a total volume of 3 µl via a Hamilton syringe. Propranolol (Sigma), aAnisomycin (Sigma), a reversible protein synthesis inhibitor, was first dissolved in 15 µl of 1N HCl solution and then treated with 1N NaOH to create a pH of 7.0. The solution was subsequently made up to a 50 µl volume with 0.9% sodium chloride. After recording of the baseline, the substance (240 µg, i.c.v.; 5 µl over a 5 min period) or the vehicle was applied. After 1 hr, the animals received the weak tetanus.
Statistics
For group comparisons of overall differences in LTP between groups, the general linear model for repeated measures was chosen (slight differences in the degrees of freedom result from a few missing values). Least significant difference multiple-comparison (LSD) post hoc tests were used for multiple group comparisons. Differences in hormone levels were evaluated by the Mann-Whitney U test after an overall comparison with the Kruskal-Wallis H test. The 24 hr values for the drug-treated and vehicle-treated groups were compared by one-way ANOVA and LSD post hoc tests. All tests were two-tailed, and the level of significance was set at p0.05.
Results
Swimming and handling modulated DG-LTP in opposite directions
A 2 min swim subsequent to handling resulted in prolonged LTP, up to 24 hr when compared with control animals (F(1,13) = 7.95; p = 0.014). Handling alone, in contrast, reversed early LTP and led to a suppression of PSA amplitudes below baseline (F(1,13) = 9.07; p = 0.01) (Fig. 1A). This bidirectional modulation of LTP became most obvious when swimming animals were compared with handled animals (F(1,12) = 21.77; p = 0.001). An overall difference, justifying the separate analyses, could be found between all three groups (F(2,19) = 13.97; p < 0.0001). Handling had no effect on baseline values, as indicated by a baseline control group (F(1,12) = 0.20; p > 0.1), whereas swimming slightly depressed baseline values (F(1,10) = 7.71; p < 0.05) (Fig. 1B). No difference could be found between the baseline values for the swimming and the handling group (F(1,10) = 4.59; p > 0.05).
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Figure 1. A, Population spike (PS) amplitudes (percentage change from baseline values) over 8 hr and a 24 hr value for rats that were handled 15 min after tetanization compared with unmanipulated animals (p = 0.024, 0.011, 0.016, 0.006, 0.007, 0.021, 0.003, 0.055, 0.021, levels for increasing time points) and for animals that experienced a 2 min swim compared with unmanipulated animals (p = 0.021, 0.012, 0.023, 0.005, 0.05, levels for increasing time points). Comparing the handled animals with the swimming animals reveals significant differences for all time points (p = 0.012, 0.007, 0.004, 0.0001, 0.0001, 0.0001, 0.0001, 0.0001, 0.0001). B, Baseline control groups were used for both behavioral manipulations. Means ± SEM are given. Asterisks indicate significant time point differences. The insets show representative analog traces for a handled and a swimming animal at the indicated time points. Horizontal dashed lines indicate the 100% level.
Blockade of GRs but not of MRs prevented impairment of LTP by handling
We measured the titers of serum corticosterone in animals 15 min after the different behavioral manipulations and found significant overall differences (2 = 18.59; df = 2; p < 0.001). Group comparisons (Fig. 2) revealed that handling caused an increase in corticosterone that was threefold that seen for the control group (U = 0, p < 0.01), whereas swimming augmented the titers nearly sixfold, also with respect to the control group (U = 0; p < 0.01). Handled animals showed significantly lower corticosterone titers than swimming animals (U = 0; p < 0.01). This suggests an impact of corticosterone on the maintenance of LTP, depending on the animals' manipulation.
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Figure 2. Levels of serum corticosterone for unmanipulated animals and for animals 15 min after handling or swimming. Asterisks indicate significant group differences.
The pharmacological analysis of the handling group alone revealed an overall difference between groups treated with a GR-antagonist (GR-ant), an MR-antagonist (MR-ant), or the vehicle (F(2,13) = 11.75; p = 0.001). Application of a GR-ant prevented impairment of LTP compared with vehicle-treated (Fig. 3A) animals (F(1,8) = 18.60; p < 0.01) and led to normal early LTP that was not distinguishable from that in the control group (F(1,12) = 2.71; p > 0.1). Injection of an MR-ant, however, had no effect on the impairment of LTP when compared with vehicle controls (Fig. 3B).
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Figure 3. Population spike (PS) amplitudes (percentage change from baseline values) over 8 hr and a 24 hr value for rats that were handled 15 min after tetanus and injected with a GR-antagonist (A) (n = 6; p = 0.005, 0.004, 0.013, 0.001, 0.012, 0.002, 0.003, 0.001, 0.013, levels for increasing time points) or an MR-antagonist (B) compared with vehicle-treated rats. Rats that experienced a 2 min swim after tetanus and injection of a GR-antagonist showed no differences compared with vehicle-treated rats (C), whereas injection of an MR-antagonist impaired LTP (D) (p = 0.007, 0.007, 0.0001, 0.0001, 0.0001, 0.0001, 0.0001, 0.0001, levels for increasing time points). E, Injection of a mixture of GR-MR-antagonists also impaired LTP (p = 0.008, 0.0001, 0.0001, 0.0001, 0.0001, 0.0001, 0.001, 0.001, levels for increasing time points). F, Baseline control groups were used for both antagonists. Means ± SEM are given. Asterisks indicate significant time point differences. The diagram insets show representative analog traces for GR-ant-treated rats (A) and MR-ant treated rats (D) at the indicated time points. Dashed lines indicate the 100% level.
Inactivation of MRs but not GRs hindered LTP prolongation by swimming
An overall comparison between all drug- and vehicle-treated swim groups (including the anisomycin- and propranolol-treated groups) revealed a significant difference (F(5,36) = 15.12; p < 0.0001). Application of the GR-ant in animals that experienced a 2 min swim had no influence on LTP prolongation (Fig. 3C), whereas an acute blockade of MR receptors completely impaired LTP in swimming rats (F(1,9) = 43.76; p < 0.001), with a significant difference at all time points (Fig. 3D) from the second hour onward. It is known that acute blockade of MRs results in an increased release of corticosterone. This could lead to an overactivation of GRs that would then mask the effect of MR blockade on LTP. For this reason, a group treated with a mixture of the GR-ant and MR-ant was tested. We found no difference between the MR-ant and the GR-ant-MR-ant group (Fig. 3E), but a difference was found between vehicle-treated rats and the GR-ant-MR-ant group (F(1,9) = 20.18; p < 0.01) that was similar to that ascertained between the vehicle-treated rats and the MR-ant group. Mifepristone (F(1,10) = 1.36; p > 0.1) as well as spironolactone (F(1,10) = 0.25; p > 0.1) did not operate on baseline values, as reflected by the lack of effect on a baseline control group (Fig. 3F).The blockade of GRs had no significant effect compared with vehicle controls but displayed a slight enhancement of LTP up to 6 hr. In contrast, the blockade of MRs led to a suppression of early LTP similar to that in handled animals. The MR-ant-treated swimming group exhibited a significantly lower potentiation than control animals (F(1,12) = 20.07; p < 0.01) with significant differences from the second hour onward up to 7 hr (p < 0.01 each; p < 0.05 for the 6 and 7 hr time points).
Reinforcement of LTP was dependent on protein synthesis but not on
The stress response to swimming leads not only to an increased level of blood corticosterone but also to a release of adrenaline and noradrenaline. These substances do not readily cross the blood-brain barrier. The main source of noradrenaline in the brain is the locus ceruleus, and there are several lines of evidence that the activation of
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Figure 4. Population spike (PS) amplitudes (percentage change from baseline values) over 8 hr and a 24 hr value for rats that experienced a 2 min swim after tetanus and were injected with a
To determine whether the late phase of the LTP reinforced by swimming is protein synthesis dependent, anisomycin, a protein synthesis inhibitor, was applied before behavioral manipulation. Anisomycin prevented the prolongation of early LTP by swimming (Fig. 4B), indicated by a significant difference with the vehicle-treated rats (F(1,10) = 10.09; p = 0.01). Figure 5 gives an overview of the differences at the 24 hr time point between treated rats in the swimming groups. In previous studies from our laboratory, it was shown that propranolol (Seidenbecher et al., 1997
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Figure 5. Differences between the population spike amplitudes at the 24 hr time point for the drug-treated swimming groups. Vehicle post, Injection after tetanization; vehicle pre, injection before tetanization, control for the anisomycin-treated group. Means ± SEM are given. **p < 0.01; *p < 0.05.
Discussion
We found bidirectional effects of behavioral manipulations on the maintenance of hippocampal LTP. Although handling 15 min after induction of early LTP resulted in an impairment of LTP, a 2 min swim, also 15 min after induction, resulted in prolongation of LTP to up to 24 hr. Because both of the behavioral manipulations increased the titers of circulating corticosterone, we studied the role of corticosterone receptors on LTP modulation by behavioral manipulation. The handling-dependent LTP impairment was reversed by blockade of glucocorticoid receptors and left unaffected by blockade of mineralocorticoid receptors. The LTP prolongation observed after swimming, however, was unaffected by blockade of GRs, whereas blockade of MRs resulted in an impairment of LTP comparable with that seen in untreated handled animals.A possible explanation for the pattern of results obtained can be found in the finding by Gesing et al. (2001
The activated corticosterone receptors regulate gene expression in two ways: by transactivation, which requires homodimerization and binding of homodimers to the DNA, and through transrepression, by interaction of receptor monomers with other transcription factors, which does not require DNA binding (Heck et al., 1994
The prolongation of LTP by swimming does not depend on the activation of
The main difference between these reports and our experiments is the highly stressful context in which our study was conducted. Increased extracellular levels of corticosterone within the hippocampus could already be observed a few minutes after the onset of stress (Linthorst et al., 2000
Because we found no evidence for the requirement of
The novelty of the swim situation very likely contributes to our results. It has been found that perception of a novel environment under low-stress conditions prolongs early DG-LTP within a certain time window around a weak tetanus (Straube et al., 2003
It is well established that glucocorticoids modulate spatial learning (Oitzl and De Kloet, 1992
Footnotes
Received Mar. 10, 2003; revised May. 23, 2003; accepted Jun. 12, 2003.This study was supported by the Land Saxony-Anhalt (LSA 3475A/1102M) as well as by the European Union Framework V NAPPY to J.U.F. We are grateful to Drs. D. v. Holst and V. Stefanski for analyzing the blood samples in the Animal Department of Physiology (Bayreuth, Germany). We thank Dr. L. de Hoz for critically reading this manuscript and G. Behnisch and J. Maiwald for technical assistance.
Correspondence should be addressed to Dr. Volker Korz, Leibniz-Institute for Neurobiology, Brenneckestrasse 6, D-39118 Magdeburg, Germany. E-mail: korz{at}ifn-magdeburg.de.
Copyright © 2003 Society for Neuroscience 0270-6474/03/237281-07$15.00/0
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