Bidirectional Modulation of Hippocampal Long-Term Potentiation under Stress and No-Stress Conditions in Basolateral Amygdala-Lesioned and Intact Rats

Abstract

Hippocampal long-term potentiation (LTP) is widely considered as a cellular model for learning and memory formation. We have shown previously that protein synthesis-independent, early dentate gyrus (DG) LTP, lasting ϳ4 -5 h, can be transformed into a late-LTP with a duration of Ն24 h by a brief acute swim stress experience (high-stress condition). This reinforcement requires the activation of mineralocorticoid receptors and protein synthesis. The basolateral amygdala (BLA) is known to modulate glucocorticoid effects on the consolidation of spatial/contextual memory via a ␤-adrenergic mechanism. Interestingly, hippocampal DG-LTP can also be indirectly modulated by ␤-adrenergic and cholinergic/muscarinergic processes. Here, we show that the reinforcement of early-DG-LTP under high-stress conditions depends on the processing of novel spatial/contextual information. Furthermore, this reinforcement was blocked in BLA-lesioned animals compared with sham-operated and intact controls; however, it was not dependent on ␤-adrenergic or cholinergic/muscarinergic receptor activation. In contrast, under low-stress conditions, the induction of late-LTP in BLA-lesioned animals is facilitated, and this facilitation, again, was dependent on ␤-adrenergic activation. The data suggest that DG-LTP maintenance can be influenced by the BLA through different mechanisms: a short-lasting corticosterone-dependent and ␤-adrenergic-independent mechanism and a long-lasting mechanism that facilitated hippocampal ␤-adrenergic mechanisms.

Severe Early Life Stress Hampers Spatial Learning and Neurogenesis, but Improves Hippocampal Synaptic Plasticity and Emotional Learning under High-Stress Conditions in Adulthood

“…However, Champagne et al (2008), using a similar fear conditioning protocol, showed that animals with a history of low maternal care have a better memory of the fearful context. Possibly, amygdalar influences on DG network activity (Akirav and Richter-Levin, 1999;Kim and Diamond, 2002;Korz and Frey, 2005) are lastingly affected by early environment, amplified by differences in corticosterone responsiveness in the DG itself as found in our in vitro studies. In addition, differences in corticosterone responsiveness due to early experience in other subregions such as the CA1 can also be expected (Champagne et al, 2008).…”

Glucocorticoid enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala

“…Previous findings have shown that the infusion of either a glucocorticoid receptor agonist or ␤-adrenoceptor agonist into the hippocampus enhances memory of such training (50,51). Furthermore, it has been reported that hippocampal excitability (52), as well as the stress-induced modulation of long-term potentiation in the hippocampus, depends on both glucocorticoid and ␤-adrenergic influences (53)(54)(55). However, glucocorticoid effects in the hippocampus on memory consolidation of contextual͞spatial training also require concurrent noradrenergic activity within the BLA (12).…”

The Basolateral Nucleus of the Amygdala Is Necessary to Induce the Opposing Effects of Stressful Experience on Learning in Males and Females

“…The hippocampus exhibits morphological and excitability changes in response to stress (Galea et al, 1997;Kim et al, 2001;Shors et al, 2001) as well as eyeblink conditioning (Geinisman et al, 2001;Moyer et al, 1996). The BLA modulates neuronal activity within the hippocampus in response to stress exposure (Kim et al, 2001;Korz and Frey, 2005) and many learning tasks, including eyeblink conditioning (Pare, 2003;Huff and Rudy, 2004;Blankenship et al, 2005;McIntyre et al, 2005). The hippocampus is sensitive to fluctuating estrogen levels (Woolley et al, 1990;Yankova et al, 2001); whether estrogen levels directly influence BLA-hippocampal interactions during stress exposure and eyeblink conditioning is unknown.…”

“…Similarly, a stress-induced enhancement of contextual fear conditioning was abolished by intra-amygdala administration of the GABA agonist midazolam before stress exposure (Rodríguez Manzanares et al, 2005). In tasks such as passive avoidance, the BLA positively modulates memory consolidation Roozendaal et al, 2002) and also modulates activity in the hippocampus during learning and stress (Vazdarjanova and McGaugh, 1999;Kim et al, 2001;Huff and Rudy, 2004;Blankenship et al, 2005;Korz and Frey, 2005). In general, an intact amygdala is necessary for stress-induced facilitation of classical fear and eyeblink conditioning Neufeld and Mintz, 2001;Rodríguez Manzanares et al, 2005).…”