Factors That Determine the Non-Linear Amygdala Influence on Hippocampus-Dependent Memory

Abstract

ᮀ Stressful experiences are known to either improve or impair hippocampal-dependent memory tasks and synaptic plasticity. These positive and negative effects of stress on the hippocampus have been largely documented, however little is known about the mechanism involved in the twofold influence of stress on hippocampal functioning and about what factors define an enhancing or inhibitory outcome. We have recently demonstrated that activation of the basolateral amygdala can produce a biphasic effect, enhancement or inhibition, of hippocampal synaptic plasticity, depending on the timing of activation (priming or spaced activation). A key question is under which conditions do the effects of amygdala activation on hippocampus dependent memory functions change from improvement to impairment of learning and memory. In this chapter we suggest that hippocampal outcome of amygdala activation may be critically dependent on four main factors: (1) The intensity of amygdala activation, (2) the temporal relation between the activation of the amygdala and the hippocampus dependent memory function, (3) the duration of amygdala activation, and (4) the contextual input during the processing of the information.Keywords: Amygdala, Hippocampus, Plasticity, Stress. A. EMOTIONALLY AROUSING EVENTS ARE MEDIATED BY THE AMYGDALA IN AN INVERTED U-SHAPED FUNCTIONEmotional states range from positive to negative, and both can range from low to high levels of arousal. Research in the field of emotional memories usually focuses on the negative end of emotional experiences due to the profound neurobiological effects of stressful experiences on learning and memory. These effects are believed to be the basis of many cognitive and affective changes in health and disease (McEwen and Sapolsky, 1995).The amygdala is an important brain structure for the recognition of negative, unpleasant emotions, such as fear, and for associating environmental stimuli with emotionally charged, aversive sensory inputs. Most of the evidence points to the basolateral amygdala nucleus (BLA; comprised of the lateral, basal, and accessory basal nuclei) as particularly important in the acquisition, consolidation, and retrieval of emotional information

The anterior medial temporal lobes: Their role in food intake and body weight regulation

“…Furthermore, the same argument can be applied to cues predicting food intake. In this article, we will consequently develop the hypothesis that the amygdala is involved (1) in the relevance processing of food stimuli, including (2) in the detection of cues linked to food intake. Additionally, we will present its role in (3) stress-induced eating, and briefly mention (4) its uncertain role in satiety signals.…”

“…Third, cued conditioning relies on the amygdala, but in the case of a conditioning relying on context, the hippocampus would additionally be recruited [97]. Fourth, a lot of studies have shown that a stimulation of the amygdala enhances hippocampal-dependent memory and modulates the synaptic plasticity in the hippocampus (e.g., [1,2,40,69,93,100,102,104]). Fifth, learning to suppress conditioned responses requires interactions between the hippocampus and the (basolateral) amygdala.…”

Differential expression of molecular markers of synaptic plasticity in the hippocampus, prefrontal cortex, and amygdala in response to spatial learning, predator exposure, and stress‐induced amnesia

“…It is also well-established that stress reduces hippocampal expression of brain-derived neurotrophic factor (BDNF), which has been associated with impaired hippocampus-dependent memory (Radecki et al, 2005;Duman and Monteggia, 2006). In contrast, stress or a fear-provoking experience activates molecular plasticity in the amygdala (Pare, 2003;Monfils et al, 2007;Ilin and Richter-Levin, 2009), which exerts an inhibitory influence on hippocampal plasticity (Akirav and Richter-Levin, 1999;Akirav and Richter-Levin, 2006). Therefore, understanding how stress differentially affects molecular plasticity in the hippocampus, amygdala and PFC could enhance our understanding of the complexity of how stress affects learning and memory.…”

Stress response recruits the hippocampal endocannabinoid system for the modulation of fear memory

“…The hippocampus is one of the memoryrelated targets of these actions, being specifically susceptible to uncontrollable stress through a pathway that involves the amygdala (Kim and Diamond 2002;Akirav and Richter-Levin 2006;Malin and McGaugh 2006). Several convergent studies show that either corticosterone, or the synthetic glucocorticoid dexamethasone, or stress promote the enhancement of memory consolidation (Roozendaal and McGaugh 1996;Roozendaal et al 1999) while impairing retrieval (de Quervain et al 1998;Roozendaal et al 2003).…”