Beta-adrenergic Blockade at Memory Encoding, but Not Retrieval, Decreases the Subjective Sense of Recollection

Abstract

Abstract■ Humans remember emotional events not only better but also exhibit a qualitatively distinct recollective experience-that is, emotion intensifies the subjective vividness of the memory, the sense of reliving the event, and confidence in the accuracy of the memory [Phelps, E. A., & Sharot, T. How (and why) emotion enhances the subjective sense of recollection. Current Directions in Psychological Science, 17, 147-152, 2008]. Although it has been demonstrated that activation of the betaadrenergic system, linked to increases in stress hormone levels and physiological arousal, mediates enhanced emotional memory accuracy, the mechanism underlying the increased subjective sense of recollection is unknown. Behavioral evidence suggests that increased arousal associated with emotional events, either at encoding or retrieval, underlies their increased subjective sense of recollection. Using a double-blind, placebo-controlled, withinsubject design, we showed that reducing arousal at encoding through oral intake of 80-mg of the beta-adrenergic receptor antagonist propranolol decreases the subjective sense of recollection for both negative and neutral stimuli 24 hr later. In contrast, administration of propranolol before memory retrieval did not alter the subjective sense of recollection. These results suggest that the neurohormonal changes underlying increased arousal at the time of memory formation, rather than the time of memory retrieval, modulate the subjective sense of recollection. ■

The role of beta-adrenolytic drugs in treating anxiety disorders

“…Nevertheless, the most recent study conducted by Rimmele et al demonstrates that propranolol has the ability to reduce the effectiveness of memorizing (not the process of retrieval from memory!) of both emotional and more neutral stimuli [63].…”

“…Jak dowodzą badania z zastosowaniem fMRI (ang. functional magnetic resonance imaging), noradrenalina jest istotnym neurotransmiterem oddziałującym na ciało migdałowate -strukturę kluczową w procesie przetwarzania emocjonalnych informacji [61,62,63]. Niemniej jednak najnowsze badanie przeprowadzone przez Rimmele i współ.…”

Suppressing cortisol at encoding reduces the emotional enhancement in subjective sense of recollection

“…Cortisol has been ascribed a modulatory role on arousal-and amygdala-dependent noradrenergic action leading to enhanced emotional memory formation (Okuda, Roozendaal, & McGaugh, 2004;van Stegeren et al, 2007;Kukolja, Klingmuller, Maier, Fink, & Hurlemann, 2011;Segal et al, 2014). While increased arousal during encoding has been specifically related to the increase of the subjective sense of recollection (Ochsner, 2000;Kensinger & Corkin, 2004;Rimmele et al, 2016), it has never been examined whether both cortisol and arousal specifically affect the subjective sense of recollection. Our finding that cortisol suppression particularly reduces the emotional enhancement in subjective sense of recollection suggests that cortisol is necessary for the arousal effects to emerge on enhancing subjective sense of recollection for emotional memories.…”

“…In contrast to the subjective sense of recollection for neutral images which has been linked to increased activation in parahippocampal cortex and better memory for contextual details (Perfect, Mayes, Downes, & Van Eijk, 1996;Gardiner, Ramponi, & Richardson-Klavehn, 1998;Sharot, Delgado, & Phelps, 2004), the subjective sense of recollection for emotional memories is distinctly associated with enhanced activation of the amygdala and better memory for some, but not all kinds of details (Sharot et al, 2004;Phelps & Sharot, 2008;Sharot & Yonelinas, 2008;Rimmele, Davachi, Petrov, Dougal, & Phelps, 2011). In addition, noradrenergic activation of beta-adrenergic receptors contributes to the subjective sense of recollection, as blocking the action of noradrenaline with the beta-adrenergic antagonist propranolol at memory encoding decreases the subjective sense of recollection (Rimmele, Lackovic, Tobe, Leventhal, & Phelps, 2016). Given that emotional enhancement in subjective sense of recollection depends on arousal, amygdala and noradrenaline action (Sharot et al, 2004;Rimmele et al, 2016), and emotional enhancement in memory formation moreover requires cortisol (Roozendaal, Okuda, de Quervain, & McGaugh, 2006;van Stegeren et al, 2007), the question arises whether cortisol plays a role in the increased subjective sense of recollection for emotional events.…”

“…In addition, noradrenergic activation of beta-adrenergic receptors contributes to the subjective sense of recollection, as blocking the action of noradrenaline with the beta-adrenergic antagonist propranolol at memory encoding decreases the subjective sense of recollection (Rimmele, Lackovic, Tobe, Leventhal, & Phelps, 2016). Given that emotional enhancement in subjective sense of recollection depends on arousal, amygdala and noradrenaline action (Sharot et al, 2004;Rimmele et al, 2016), and emotional enhancement in memory formation moreover requires cortisol (Roozendaal, Okuda, de Quervain, & McGaugh, 2006;van Stegeren et al, 2007), the question arises whether cortisol plays a role in the increased subjective sense of recollection for emotional events. Some evidence for cortisol playing a role particularly for subjective sense of recollection comes from a study with a postencoding stressor, where stress-induced cortisol levels during consolidation were associated with increased subjective sense of recollection at a later test (McCullough, Ritchey, Ranganath, & Yonelinas, 2015).…”