Activity and plasticity in the CA1, the dentate gyrus, and the amygdala following controllable vs. uncontrollable water stress

Kavushansky, Alexandra; Vouimba, Rose-Marie; Cohen, Hagit; Richter‐Levin, Gal

doi:10.1002/hipo.20130

Cited by 133 publications

(100 citation statements)

References 44 publications

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“…However, an efficient memory system must retain relevant information selectively, while permitting the decay of irrelevant memory traces (McGaugh 2000). As discussed in the introduction, novelty has been implicated in the selection of hippocampal memory traces to be stored for long or short periods of time, but other factors such as stress and reward are also known to modulate hippocampal memory (McGaugh 2004;Wittmann et al 2005;Adcock et al 2006;Shors 2006), perhaps via their impact on synaptic plasticity (Seidenbecher et al 1995(Seidenbecher et al , 1997Xu et al 1998b;Richter-Levin and Akirav 2003;Diamond et al 2005;Korz and Frey 2005;Ahmed et al 2006;Kavushansky et al 2006). In one variant of this idea, the "synaptic tagging and capture" (STC) hypothesis Morris 1997, 1998;Kelleher III et al 2004), mechanisms underlying the persistence of LTP in the hippocampus involve the intersection of two dissociable events: the local set- …”

Section: Relationship Of These Findings To the Synaptic Tagging And Cmentioning

confidence: 99%

Dopaminergic modulation of the persistence of one-trial hippocampus-dependent memory

O'Carroll¹,

Martin²,

Sandin³

et al. 2006

Learn. Mem.

216

148

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The persistence of new memory traces in the hippocampus, encoded following appropriate activation of glutamatergic receptors and the induction of synaptic plasticity, can be influenced by heterosynaptic activation of neuromodulatory brain systems. We therefore investigated the effects of a hippocampus-specific blockade of dopamine D1/D5 receptors on the persistence of spatial memory encoded in one trial using a delayed matching-to-place (DMP) task in a watermaze in which rats learn a new escape location each day. A within-subjects design was used such that both short (20 min) and long (6 h) retention intervals, and both drug (SCH23390, a D1/D5 receptor antagonist) and vehicle (aCSF) infusions were tested on different days in the same animals. Bilateral intrahippocampal infusion of SCH23390 (5 µg in 1 µL per side) prior to trial 1 (encoding) caused a differential impairment as a function of memory delay-with no effect during trial 2 (memory retrieval) after a 20-min interval, but a block of memory at 6 h. Further experiments revealed that infusion of SCH23390 immediately after trial 1 had no effect on retention 6 h later, and the poor memory seen at long retention intervals when the drug was present at encoding was not due to a state-dependent failure of retrieval. These results suggest that activation of D1/D5 receptors during memory encoding is necessary for the formation of a persistent memory trace in the hippocampus. The complementary effects of D1/D5 receptor blockade on the persistence of LTP and the duration of memory are consistent with the idea that changes in synaptic strength underlie memory.

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Section: Relationship Of These Findings To the Synaptic Tagging And Cmentioning

confidence: 99%

Dopaminergic modulation of the persistence of one-trial hippocampus-dependent memory

O'Carroll¹,

Martin²,

Sandin³

et al. 2006

Learn. Mem.

216

148

View full text Add to dashboard Cite

show abstract

“…The dentate gyrus, as well as the CA1 region of the hippocampus, is vulnerable to stress. Depending on its severity and context, stress has been shown to facilitate or impair the induction of LTP in the dentate gyrus (Shors and Dryver, 1994;Frey, 2003, 2005;Ahmed et al, 2006;Kavushansky et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

Acute Stress Impairs Hippocampal Mossy Fiber-CA3 Long-Term Potentiation by Enhancing cAMP-Specific Phosphodiesterase 4 Activity

Chen

Yang

Huang

et al. 2010

Neuropsychopharmacol

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The mossy fiber synapses onto hippocampal CA3 neurons show unique molecular features and a wide dynamic range of plasticity. Although acute stress has been well recognized to alter bidirectional long-term synaptic plasticity in the hippocampal CA1 region and dentate gyrus, it remains unclear whether the same effect may also occur at the mossy fiber-CA3 synapses. Here, we report that hippocampal slices prepared from adult mice that had experienced an acute unpredictable and inescapable restraint tail-shock stress showed a marked impairment of long-term potentiation (LTP) induced by high-frequency stimulation or adenylyl cyclase activator forskolin. This effect was prevented when animals were submitted to bilateral adrenalectomy or given the glucocorticoid receptor antagonist RU38486 before experiencing stress. In contrast, stress has no effect on synaptic potentiation induced by the nonhydrolysable and membrane-permeable cyclic adenosine 5 0 -monophosphate (cAMP) analog Sp-8-bromo-cAMPS. No obvious differences were observed between control and stressed mice in the basal synaptic transmission, paired-pulse facilitation, or frequency facilitation at the mossy fiber-CA3 synapses. We also found that the inhibitory effect of stress on mossy fiber LTP was obviated by the adenosine A 1 receptor antagonist 8-cyclopentyl-1,3,-dipropylxanthine, the non-specific phosphodiesterase (PDE) inhibitor 3-isobutylmethylxanthine, and the specific PDE4 inhibitor 4-(3-butoxy-4-methoxyphenyl)methyl-2-imidazolidone. In addition, stress induces a sustained and profound increase in cAMP-specific PDE4 activity. These results suggest that the inhibition of mossy fiber LTP by acute stress treatment seems originating from a corticosterone-induced sustained increase in the PDE4 activity to accelerate the metabolism of cAMP to adenosine, in turn triggering an adenosine A 1 receptor-mediated impairment of transmitter release machinery.

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“…First, the impact of this drug on glutamatergic synaptic currents differs between the hippocampus and amygdala. Second, this region-specific difference is significant in light of earlier studies reporting opposite effects of chronic stress on these two brain areas (Kavushansky et al, 2006;Vouimba et al, 2004Vouimba et al, , 2006Vyas et al, 2002). Repeated stress causes hippocampal dendritic atrophy, which in turn depends on NMDA receptors.…”

Section: Tianeptine Blocks Chronic Stress-induced Dendritic Hypertropmentioning

confidence: 90%

“…physiological actions of tianeptine in the amygdala, we were guided by earlier reports on the efficacy of tianeptine in preventing hippocampal dendritic atrophy and impaired learning and memory caused by stress (Conrad et al, 1996;McEwen et al, 1997). As the effects of chronic stress on the amygdala are quite different from the hippocampus (Kavushansky et al, 2006;Roozendaal et al, 2009;Vouimba et al, 2004), we tested if the contrasting in vitro effects of tianeptine in the two areas also lead to functional benefits in the intact animal against stress. Indeed, systemic administration of tianeptine prevents stress-induced facilitation of anxiety-like behavior and BLA dendritic growth.…”

Section: Discussionmentioning

confidence: 99%

“…Indeed, little is known about how antidepressants affect amygdalar neurons. The need to look beyond the hippocampus is also highlighted by growing evidence that rodent models of stress elicit contrasting patterns of structural plasticity in the hippocampus vs amygdala (Kavushansky et al, 2006;Roozendaal et al, 2009;Vouimba et al, 2004). For example, the same chronic stress that triggers dendritic atrophy in the hippocampus causes dendritic growth in the basolateral amygdala (BLA) (McEwen, 1999;Vyas et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

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The Same Antidepressant Elicits Contrasting Patterns of Synaptic Changes in the Amygdala vs Hippocampus

Pillai

Anilkumar

Chattarji

2012

Neuropsychopharmacol

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As depression-like symptoms are often precipitated by some form of stress, animal models of stress have been used extensively to investigate cellular mechanisms of depression. Despite being implicated in the emotional symptoms of depression, the amygdala has received little attention compared to the hippocampus in the past studies of antidepressant action. Further, these investigations have not taken into account the contrasting effects of chronic stress on the hippocampus vs amygdala. If an antidepressant is to be equally effective in countering the differential effects of stress on both brain areas, then it is faced with the challenge of eliciting contrasting effects in these two structures. We tested this prediction by examining the impact of tianeptine, an antidepressant with proven clinical efficacy, on neurons of the lateral amygdala (LA) and hippocampal area CA1. Tianeptine reduces N-methyl-D-aspartate (NMDA)-receptor-mediated synaptic currents, without affecting a-amino-3-hydroxy-5-methyl-4-isoxazole propionate (AMPA) currents, in LA neurons. By contrast, tianeptine enhances both NMDA and AMPA currents in area CA1. Tianeptine also lowers action potential firing in LA neurons. As tianeptine modulates cellular metrics that, in addition to mediating amygdalar behavioral output, are also affected by stress, we tested if tianeptine succeeds in countering stress effects in the intact animal. We find that tianeptine prevents two important functional consequences of chronic stress-induced plasticity in the amygdalaFdendritic growth and enhanced anxiety-like behavior. These results provide evidence for antidepressant action on amygdalar neurons that are not only distinct from the hippocampus, but also protect against the debilitating impact of stress on amygdalar structure and function.

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Activity and plasticity in the CA1, the dentate gyrus, and the amygdala following controllable vs. uncontrollable water stress

Cited by 133 publications

References 44 publications

Dopaminergic modulation of the persistence of one-trial hippocampus-dependent memory

Dopaminergic modulation of the persistence of one-trial hippocampus-dependent memory

Acute Stress Impairs Hippocampal Mossy Fiber-CA3 Long-Term Potentiation by Enhancing cAMP-Specific Phosphodiesterase 4 Activity

The Same Antidepressant Elicits Contrasting Patterns of Synaptic Changes in the Amygdala vs Hippocampus

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