Angiotensin II suppresses long-term depression in the lateral amygdala of mice via L-type calcium channels

doi:10.1016/j.neulet.2006.12.040

Neuroscience Letters

Volume 415, Issue 1, 19 March 2007, Pages 68-72

https://doi.org/10.1016/j.neulet.2006.12.040 Get rights and content

Abstract

Previously we have shown that angiotensin II (Ang II) suppresses long-term potentiation (LTP) in the lateral nucleus of the amygdala (LA) of horizontal slices. This study examines the effect of Ang II on long-term depression (LTD) in the LA. Low frequency stimulation (1 Hz, 15 min; LFS) applied to fibers running within the LA induced a long-lasting reduction of the amplitudes of field potentials in the LA of mice. We have previously shown that this LTD is sensitive to the NMDA receptor blocker D-AP5 and is dependent on group II mGlu receptors. Ang II blocked dose-dependent LTD. Losartan, an AT₁ receptor antagonist, blocked the Ang II-induced suppression of LTD, whereas PD 123 319, an AT₂ receptor antagonist, had no effect. Co-administration of nifedipine, an L-type calcium channel antagonist, abolished Ang II-induced suppression of LTD. When applied alone nifedipine reduced the magnitude of LA-LTD. According to our previous results, stimulation of external capsule (EC) fibers in rats did not cause LTD in mice. Similarly, Ang II did not induce long-lasting changes of activity when EC stimulation site was used. The results support the view that angiotensins are involved in mechanisms of learning and memory including the plasticity changes in the LA.

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Acknowledgement

We thank Dr. Herbert Siegmund for expert help in data analysis and Karin Berlin for technical assistance.

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A novel form of capsaicin-modified amygdala LTD mediated by TRPM1
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Citation Excerpt :
For removing out-of-focus blur, deconvolution with a constrained iterative (CI) algorithm (CellSens Dimension, Olympus, Germany) was used. Previous studies in horizontal slices of the LA have shown that the application of low-frequency stimulation (LFS, 900 pulses at 1 Hz) elicits a strong LTD when stimulating presynaptic fibers within the LA (intranuclear; IN) (Muller et al., 2009; Tchekalarova & Albrecht, 2007), but not when stimulating the EC (Muller et al., 2009) (Fig. 1A). In this investigation we show that paired-pulse low-frequency stimulation (PP-LFS) with an interstimulus time of 40 ms reliably produces LA-LTD even when stimulating the EC.
Recently we have shown that capsaicin attenuates the strength of LTP in the lateral amygdala (LA) and demonstrated that this effect is mediated by the transient receptor potential (TRP) channel TRPV1. Here we further show that capsaicin, which is thought to act primarily through TRPV1, modifies long term depression (LTD) in the LA. Yet the application of various TRPV1 antagonists does not reverse this effect and it remains in TRPV1-deficient mice. In addition, voltage gated calcium channels, nitric oxide and CB1 receptors are not involved. Using pharmacology and TRPM1^−/− mice, our electrophysiological data indicate that capsaicin-induced activation of TRPM1 channels contribute to the induction of LA-LTD. Whereas LA-LTD in general depends on the acitvation of NMDA receptors- and group II metabotropic glutamate receptors (mGluR), the modifying effect of capsaicin on LA-LTD via TRPM1 appears to be specifically mediated by group I mGluRs and in interaction with another member of the TRP family, TRPC5. Additionally, intact GABAergic transmission is required for the capsaicin-effect to take place. This is the first documentation that beside their function in the retina TRPM1 proteins are expressed in the brain and have a functional relevance in modifying synaptic plasticity.
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Central administration of angiotensin IV rapidly enhances novel object recognition among mice
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Citation Excerpt :
While Ang IV has high affinity for a distinct binding site referred to as the AT4 receptor, recent findings suggest that Ang IV may also have important actions at AT1 receptors that mediate working memory (De Bundel et al., 2010). However, activation of AT1 receptors (by Ang II itself) has been found to inhibit synaptic LTP (Wayner et al., 1993) and inhibit long-term depression (LTD; Tchekalarova and Albrecht, 2007). The present finding that pharmacological blockade of AT4 receptors with the putative antagonist divalinal-Ang IV (Coleman et al., 1998; Krebs et al., 1996) significantly reduced object recognition supports a procognitive mechanism for Ang IV that is mediated; albeit not exclusively, by AT4 receptors.
Angiotensin IV (Val¹-Tyr²-Ile³-His⁴-Pro⁵-Phe⁶) has demonstrated potential cognitive-enhancing effects. The present investigation assessed and characterized: (1) dose-dependency of angiotensin IV's cognitive enhancement in a C57BL/6J mouse model of novel object recognition, (2) the time-course for these effects, (3) the identity of residues in the hexapeptide important to these effects and (4) the necessity of actions at angiotensin IV receptors for procognitive activity. Assessment of C57BL/6J mice in a novel object recognition task demonstrated that prior administration of angiotensin IV (0.1, 1.0, or 10.0, but not 0.01 nmol, i.c.v.) significantly enhanced novel object recognition in a dose-dependent manner. These effects were time dependent, with improved novel object recognition observed when angiotensin IV (0.1 nmol, i.c.v.) was administered 10 or 20, but not 30 min prior to the onset of the novel object recognition testing. An alanine scan of the angiotensin IV peptide revealed that replacement of the Val¹, Ile³, His⁴, or Phe⁶ residues with Ala attenuated peptide-induced improvements in novel object recognition, whereas Tyr² or Pro⁵ replacement did not significantly affect performance. Administration of the angiotensin IV receptor antagonist, divalinal-Ang IV (20 nmol, i.c.v.), reduced (but did not abolish) novel object recognition; however, this antagonist completely blocked the procognitive effects of angiotensin IV (0.1 nmol, i.c.v.) in this task. Rotorod testing demonstrated no locomotor effects with any angiotensin IV or divalinal-Ang IV dose tested. These data demonstrate that angiotensin IV produces a rapid enhancement of associative learning and memory performance in a mouse model that was dependent on the angiotensin IV receptor.
Inhibition of central angiotensin II enhances memory function and reduces oxidative stress status in rat hippocampus
2013, Progress in Neuro-Psychopharmacology and Biological Psychiatry
Citation Excerpt :
It has been also reported that Ang II receptor blockers could facilitate long term potentiation (LTP), in the hippocampus of AD mice (Manschot et al., 2003), while it was previously demonstrated that Ang II blocks long-term potentiation in both hippocampus (Armstrong et al., 1996) and amygdala (von Bohlen und Halbach and Albrecht, 1998). Still, the effects of losartan vs PD 123319 on this kind of specific forms of synaptic plasticity could be extremely different, as showed by Tchekalarova and Albrecht, 2007. Additionally, it was demonstrated that the administration of telmisartan, an AT1 receptor blocker, significantly decreased some hypertension-induced learning and memory deficits in the water maze task (Sharma and Singh, 2012).
While it is now well established that the independent brain renin–angiotensin system (RAS) has some important central functions besides the vascular ones, the relevance of its main bioactive peptide angiotensin II (Ang II) on the memory processes, as well as on oxidative stress status is not completely understood.
The purpose of the present work was to evaluate the effects of central Ang II administration, as well as the effects of Ang II inhibition with either AT1 and AT 2 receptor specific blockers (losartan and PD-123177, respectively) or an angiotensin-converting enzyme (ACE) inhibitor (captopril). These effects were studied on the short-term memory (assessed through Y-maze) or long-term memory (as determined in passive avoidance) and on the oxidative stress status of the hippocampus.
Our results demonstrate memory deficits induced by the administration of Ang II, as showed by the significant decrease of the spontaneous alternation in Y-maze (p = 0.015) and latency-time in passive avoidance task (p = 0.001) when compared to saline. On the other side, the administration of all the aforementioned Ang II blockers significantly improved the spontaneous alternation in Y-maze task, while losartan also increased the latency time as compared to saline in step-through passive avoidance (p = 0.042).
Also, increased oxidative stress status was induced in the hippocampus by the administration of Ang II, as demonstrated by increased levels of lipid peroxidation markers (malondialdehyde-MDA concentration) (p < 0.0001) and a decrease in both antioxidant enzymes determined: superoxide dismutase-SOD (p < 0.0001) and glutathione peroxidase-GPX (p = 0.01), as compared to saline. Additionally, the administration of captopril resulted in an increase of both antioxidant enzymes and decreased levels of lipid peroxidation (p = 0.001), while PD-123177 significantly decreased MDA concentration (p > 0.0001) vs. saline.
Moreover, significant correlations were found between all of the memory related behavioral parameters and the main oxidative stress markers from the hippocampus, which is known for its implication in the processes of memory and also where RAS components are well expressed.
This could be relevant for the complex interactions between Ang II, behavioral processes and neuronal oxidative stress, and could generate important therapeutic approaches.

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Angiotensin II suppresses long-term depression in the lateral amygdala of mice via L-type calcium channels

Abstract

Section snippets

Acknowledgement

Peptides

Neuroscience

Brain Res.

Neurobiol. Learn. Mem.

Front. Neuroendocrinol.

Neuroscience

Brain Res.

J. Neurosci. Methods

Peptides

Neurosci. Lett.

Neurosci. Biobehav. Rev.

Angiotensin II and the amygdala

Ann. N. Y. Acad. Sci.

The renin angiotensin system and Alzheimer's disease

Ann. N. Y. Acad. Sci.

Input-specific LTP and depotentiation in the basolateral amygdala

Neuroreport