Noradrenergic mechanisms of arousal's bidirectional effects on episodic memory.
Arousal's selective effects on cognition go beyond the simple enhancement of emotional stimuli, sometimes enhancing and other times impairing processing of proximal neutral information. Past work shows that arousal impairs encoding of subsequent neutral stimuli regardless of their top-down priority via the engagement of β-adrenoreceptors. In contrast, retrograde amnesia induced by emotional arousal can flip to enhancement when preceding neutral items are prioritized in top-down attention. Whether β-adrenoreceptors also contribute to this retrograde memory enhancement of goal-relevant neutral stimuli is unclear. In this pharmacological study, we administered 40mg of propranolol or 40mg of placebo to healthy young adults to examine whether emotional arousal's bidirectional effects on declarative memory relies on β-adrenoreceptor activation. Following pill intake, participants completed an emotional oddball task in which they were asked to prioritize a neutral object appearing just before an emotional or neutral oddball image within a sequence of 7 neutral objects. Under placebo, emotional oddballs impaired memory for lower priority oddball+1 objects but had no effect on memory for high priority oddball-1 objects. Propranolol blocked this anterograde amnesic effect of arousal. Emotional oddballs also enhanced selective memory trade-offs significantly more in the placebo than drug condition, such that high priority oddball-1 objects were more likely to be remembered at the cost of their corresponding lower priority oddball+1 objects under arousal. Lastly, those who recalled more high priority oddball-1 objects preceding an emotional versus neutral oddball image showed greater increases in salivary alpha-amylase, a biomarker of noradrenergic system activation, across the task. Together these findings suggest that different noradrenergic mechanisms contribute to the anterograde and retrograde mnemonic effects of arousal on proximal neutral memoranda.
Neuroscience Graduate Program, University of Southern California, USA. Electronic address: clewett@usc.edu.
David
D
Clewett
School of Psychology and Clinical Language Sciences, University of Reading, UK.
Michiko
M
Sakaki
Davis School of Gerontology, University of Southern California, USA.
Shawn
S
Nielsen
Neuroscience Graduate Program, University of Southern California, USA; Department of Neurology, University of Southern California, USA.
Giselle
G
Petzinger
Neuroscience Graduate Program, University of Southern California, USA; Davis School of Gerontology, University of Southern California, USA.
Mara
M
Mather
D000319:Adrenergic beta-Antagonists / Q000494:pharmacology*; D001143:Arousal / Q000187:drug effects*; D004644:Emotions / Q000187:drug effects*; D005260:Female; D006801:Humans; D008297:Male; D008568:Memory / Q000187:drug effects*; D061212:Memory, Episodic; D009483:Neuropsychological Tests; D011433:Propranolol / Q000494:pharmacology*; D055291:Salivary alpha-Amylases / Q000032:analysis; D055815:Young Adult
D000319:Adrenergic beta-Antagonists; D011433:Propranolol; D055291:Salivary alpha-Amylases
Arousal; Attention; Emotion; Locus coeruleus; Memory; Norepinephrine