Effects of inescapable stress on LTP in the amygdala versus the dentate gyrus of freely behaving rats

Abstract

Stress impairs hippocampal long-term potentiation (LTP), a model of synaptic plasticity that is assumed to underlie memory formation. In the amygdala, little is known about the effects of stress on LTP, or about its longevity. Here we assessed the ability of entorhinal cortex (EC) stimulation to induce LTP simultaneously in the basal amygdaloid nucleus (B) and in the dentate gyrus (DG) of freely behaving Wistar rats. We also tested whether LTP persists over days. Once established, we investigated the effects of acute vs. repeated inescapable stressful experiences on LTP in both structures. Results show that B, like DG, sustained LTP for 7 days. Furthermore, a single exposure to moderate stress facilitated LTP in B but did not affect DG LTP. Stress re-exposure inhibited LTP in DG but only long-lasting LTP (>3 days) in B. Behaviourally, animals exhibited a higher immobility when re-exposed to the stressor than with a single/first exposure. These data support a role for B in memory storage. Furthermore, they support a differential involvement of the amygdala and hippocampus in memory formation and storage depending on the emotional characteristics of the experience.

Unraveling the Time Domains of Corticosteroid Hormone Influences on Brain Activity: Rapid, Slow, and Chronic Modes

“…The latter was not seen when the BLA had already been stimulated earlier or when animals had recently experienced stress (Richter-Levin and Maroun, 2010), another example of metaplasticity. In contrast to these findings, most studies agree that stress facilitates LTP in projections to the (baso)lateral amygdala, originating in the entorhinal cortex, external capsule or prelimbic cortex (Vouimba et al, 2004;Rodrí-guez Manzanares et al, 2005;Maroun, 2006; but see .…”

“…Abrari et al (2009) reported facilitated induction of LTP in association with improved memory when rats were treated with a moderately high dose of corticosterone directly after training in a fear conditioning paradigm. However, others found no change after inescapable or cold stress (Shors and Dryver, 1994;Vouimba et al, 2004) or could not link stress-induced changes in LTP/LTD to known corticosteroid receptor types (Spyrka et al, 2011). Stress exposure after LTP induction has also been studied in the dentate gyrus.…”

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

“…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.…”

“…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.…”

“…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).…”