Action boosts episodic memory encoding in humans via engagement of a noradrenergic system

Abstract

SUMMARYWe are constantly interacting with our environment whilst we encode memories. However, how actions influence memory formation remains poorly understood. Goal-directed movement engages the locus coeruleus (LC), the main source of noradrenaline in the brain. Noradrenaline is also known to enhance episodic encoding, suggesting that action could improve memory via LC engagement. Here we demonstrate, across seven experiments, that action (Go-response) enhances episodic encoding for stimuli unrelated to the action itself, compared to action inhibition (NoGo). Supporting a noradrenergic mechanism underlying this enhancement, functional magnetic resonance imaging, and pupil diameter as a proxy measure for LC-noradrenaline transmission, indicate increased encoding-related LC activity during action. A final experiment confirmed a novel prediction derived from these data that emotionally aversive stimuli, which recruit the noradrenergic system, modulate the mnemonic advantage conferred by Go-responses relative to neutral stimuli. We therefore provide converging evidence that action boosts episodic memory encoding via a noradrenergic mechanism.

Inter‐ and intra‐individual coupling between pupillary, electrophysiological, and behavioral responses in a visual oddball task

“…Response hand was counterbalanced across standard and deviant conditions across blocks, such that every combination of response hand and relative probability for each stimulus was tested for each participant in a separate block. This also helped us control for LC‐NE activity elicited by voluntary movement (e.g., Yebra et al., 2019), as the participant was always responding to every stimulus, counterbalanced across the response hand.…”

Long-term implicit memory for sequential auditory patterns in humans

“…It is difficult to draw strong conclusions from the present experiment about the effect of attention per se. It is possible that the reduced memory effect in the passive condition was driven by issues related to decreased arousal or reward, known to modulate learning (Beste & Dinse, 2013;Braun, Wimmer, & Shohamy, 2018;Polley, Steinberg, & Merzenich, 2006;Yebra et al, 2019), and which likely distinguish active detection (where feedback was provided after each trial) from passive listening.…”

Agency Improves Working Memory and Accelerates Visual and Attentional Processing

“…Moreover, decoupled movements modulate perception 41 and attention 4 . There is also evidence suggesting that unrelated button pressing improves long-term memory encoding, whether the action is time-locked to stimulus onset or not 42 . Our results corroborate a parallel nonpredictive modulation of motor systems over WM.…”

“…Fine temporal coupling between motor acts and their sensory consequences have been depicted to be crucial to visual cortex development 39 and important in perception 1 and attention 40 . However, studies indicate that movements that are made before and after stimuli presentation (hence, the stimuli are not an immediate consequence of the motor act) can also influence perception 41 and even long-term memory performance 42 . This evidence is suggestive of a possible motor-related modulation that is independent of temporal prediction.…”

“…This evidence is suggestive of a possible motor-related modulation that is independent of temporal prediction. Yebra et al (2019) indicated that the noradrenergic system's engagement mediates this motor-related improvement in long-term memory performance during encoding. Since the noradrenergic system massively modulates brain activity, it is possible to speculate an influence at both early sensory and attentional encoding processing levels.…”