Endocannabinoid Signaling as a Mediator of the Effects of StressRole of the endocannabinoid system in regulating glucocorticoid effects on memory for emotional experiences
Highlights
▶Glucocorticoid effects on memory require emotion-induced noradrenergic activity. ▶Such glucocorticoid actions are mediated by rapid nongenomic mechanisms. ▶Endocannabinoids might be essential in mediating these rapid glucocorticoid effects.
Section snippets
Glucocorticoid effects on different memory phases: dependence on arousal status
In this section, we describe the effects of glucocorticoids on different memory phases and their interaction with emotional arousal. There is compelling evidence from studies in both animals and humans that glucocorticoids are involved in regulating the consolidation of memory processes (Flood et al., 1978, de Kloet, 2000; Roozendaal, 2000, Roozendaal, 2002; McGaugh and Roozendaal, 2002, Het et al., 2005; Sandi and Pinelo-Nava, 2007, de Quervain et al., 2009, Roozendaal et al., 2009). Memory
Glucocorticoid interactions with arousal-induced noradrenergic activation in the basolateral amygdala
Why do glucocorticoids only modulate memory of emotionally arousing experiences? Our findings suggest that interactions between stress hormones and noradrenergic activity within the amygdala may be key in determining this selectivity. It is well established that emotional experiences that induce the release of adrenal stress hormones also increase amygdala neuronal activity (Pelletier et al., 2005). Extensive evidence from our as well as other laboratories indicates that the enhancing effects
Rapid nongenomic glucocorticoid effects: involvement of the endocannabinoid system
Glucocorticoids are known to modulate cellular function, including learning and memory, through both genomic (slow) and nongenomic (rapid) pathways (de Kloet, 2000, Dallman, 2005). Genomic glucocorticoid effects are mediated by classical steroid mechanisms involving transcriptional regulation. Glucocorticoids can influence transcription through both DNA-binding–dependent and DNA-binding–independent mechanisms (de Kloet, 2000). Although many glucocorticoid actions suit the time frame for a
Role of endocannabinoids in regulating glucocorticoid effects on memory: the model
Endocannabinoid signaling is crucial for certain forms of short- and long-term synaptic plasticity at excitatory and inhibitory synapses, and thereby contributes to various aspects of brain function, including learning and memory (Kano et al., 2009). It has long been recognized, in animals and humans, that endocannabinoids influence different memory phases. Behavioral studies in humans indicate that cannabis consumption as well as synthetic CB1 receptor agonists impair cognitive processes that
Conclusions and future directions
The findings summarized previously indicate that glucocorticoids enhance memory consolidation for emotionally arousing experiences and impair memory retrieval and working memory during emotionally arousing test situations via rapid interactions with arousal-induced noradrenergic mechanisms. The endocannabinoid system might play a crucial role in mediating such rapid glucocorticoid effects on the noradrenergic system. However, there are many fascinating, unanswered questions. First, our model
Acknowledgments
Research was supported by a Jan Kornelis de Cock Foundation Research Grant to P.A. and “Progretti di Ricerca 2010” (Sapienza University of Rome) to P.C.
References (144)
- et al.
Endogenous cortisol elevations are related to memory facilitation only in individuals who are emotionally aroused
Psychoneuroendocrinology
(2006) - et al.
The effects of long-term corticosterone administration on hippocampal morphology and cognitive performance of middle-aged rats
Brain Res
(1994) Catecholamine modulation of prefrontal cortical cognitive function
Trends Cogn Sci
(1998)- et al.
Interactions between anandamide-induced anterograde amnesia and post-training memory modulatory systems
Brain Res
(2004) - et al.
Dose-dependent effects of hydrocortisone on memory in human males
Physiol Behav
(1986) - et al.
Adrenocortical hormones and avoidance behaviour of rats
Int J Neuropharmacol
(1968) - et al.
Autobiographic memory impairment following acute cortisol administration
Psychoneuroendocrinology
(2004) Fast glucocorticoid actions on brain: back to the future
Front Neuroendocrinol
(2005)- et al.
Plasma catecholamine, corticosterone and glucose responses to repeated stress in rats: effect of interstressor interval length
Physiol Behav
(1990) Stress in the brain
Eur J Pharmacol
(2000)
Corticosteroid hormones in the central stress response: quick-and-slow
Front Neuroendocrinol
Amnestic effect of intrahippocampal AM251, a CB1-selective blocker, in the inhibitory avoidance, but not in the open field habituation task, in rats
Neurobiol Learn Mem
AM251, a selective antagonist of the CB1 receptor, inhibits the induction of long-term potentiation and induces retrograde amnesia in rats
Brain Res
Glucocorticoids and the regulation of memory in health and disease
Front Neuroendocrinol
Cannabinoids and prefrontal cortical function: insights from preclinical studies
Neurosci Biobehav Rev
Clenbuterol administration into the basolateral amygdala post-training enhances retention in an inhibitory avoidance task
Neurobiol Learn Mem
Memory facilitating and anti-amnesic effects of corticosteroids
Pharmacol Biochem Behav
The prefrontal cortex and its relation to behavior
Prog Brain Res
The effects of non-genomic glucocorticoid mechanisms on bodily functions and the central neural system: a critical evaluation of findings
Front Neuroendocrinol
Response of amygdalar norepinephrine to footshock and GABAergic drugs using in vivo microdialysis and HPLC
Brain Res
A meta-analytic review of the effects of acute cortisol administration on human memory
Psychoneuroendocrinology
Rapid elevations in limbic endocannabinoid content by glucocorticoid hormones in vivo
Psychoneuroendocrinology
Stress and emotional memory: a matter of timing
Trends Cogn Sci
Localization of glucocorticoid receptors at postsynaptic membranes in the lateral amygdala
Neuroscience
Activation of the amygdala and anterior cingulate during nonconscious processing of sad versus happy faces
Neuroimage
Effects of oral cortisol treatment in healthy young women on memory retrieval of negative and neutral words
Neurobiol Learn Mem
Adrenocortical suppression blocks the enhancement of memory storage produced by exposure to psychological stress in rats
Brain Res
Effects of chronic corticosterone ingestion on spatial memory performance and hippocampal serotonergic function
Brain Res
Role of adrenal stress hormones in forming lasting memories in the brain
Curr Opin Neurobiol
Memory-enhancing corticosterone treatment increases amygdala norepinephrine and Arc protein expression in hippocampal synaptic fractions
Neurobiol Learn Mem
Functional CB2 type cannabinoid receptors at CNS synapses
Neuropharmacology
Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals
Neuron
Systemic administration of WIN 55,212-2 increases norepinephrine release in the rat frontal cortex
Brain Res
Is lipid signaling through cannabinoid 2 receptors part of a protective system?
Prog Lipid Res
Repeated cannabinoid administration increases indices of noradrenergic activity in rats
Pharmacol Biochem Behav
WIN 55212-2 impairs contextual fear conditioning through the activation of CB1 cannabinoid receptors
Neurosci Lett
Impaired declarative memory for emotional material following bilateral amygdala damage in humans
Learn Mem
Working memory
Science
Glucocorticoids in the prefrontal cortex enhance memory consolidation and impair working memory by a common neural mechanism
Proc Natl Acad Sci U S A
Prelimbic cortex, mediodorsal thalamus, septum, and delayed alternation in rats
Exp Brain Res
Aversive memory reactivation engages in the amygdala only some neurotransmitters involved in consolidation
Learn Mem
The amygdala and emotional memory
Nature
Amygdala activity at encoding correlated with long-term, free recall of emotional information
Proc Natl Acad Sci U S A
Fat-induced satiety factor oleoylethanolamide enhances memory consolidation
Proc Natl Acad Sci U S A
Endocannabinoids in the rat basolateral amygdala enhance memory consolidation and enable glucocorticoid modulation of memory
Proc Natl Acad Sci U S A
Event-related activation in the human amygdala associates with later memory for individual emotional experience
J Neurosci
Enhancing cannabinoid neurotransmission augments the extinction of conditioned fear
Neuropsychopharmacology
Corticosterone enhances adrenocorticotropin-induced calcium signals in bovine adrenocortical cells
Endocrinology
Glucocorticoid therapy-induced memory deficits: acute versus chronic effects
J Neurosci
Glucocorticoid involvement in memory formation in a rat model for traumatic memory
Stress
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