Locus Coeruleus Activity Strengthens Prioritized Memories Under Arousal

Recent models posit that bursts of locus ceruleus (LC) activity amplify neural gain such that limited attention and encoding resources focus even more on prioritized mental representations under arousal. Here, we tested this hypothesis in human males and females using fMRI, neuromelanin MRI, and pupil dilation, a biomarker of arousal and LC activity. During scanning, participants performed a monetary incentive encoding task in which threat of punishment motivated them to prioritize encoding of scene images over superimposed objects. Threat of punishment elicited arousal and selectively enhanced memory for goal-relevant scenes. Furthermore, trial-level pupil dilations predicted better scene memory under threat, but were not related to object memory outcomes. fMRI analyses revealed that greater threat-evoked pupil dilations were positively associated with greater scene encoding activity in LC and parahippocampal cortex, a region specialized to process scene information. Across participants, this pattern of LC engagement for goal-relevant encoding was correlated with neuromelanin signal intensity, providing the first evidence that LC structure relates to its activation pattern during cognitive processing. Threat also reduced dynamic functional connectivity between high-priority (parahippocampal place area) and lower-priority (lateral occipital cortex) category-selective visual cortex in ways that predicted increased memory selectivity. Together, these findings support the idea that, under arousal, LC activity selectively strengthens prioritized memory representations by modulating local and functional network-level patterns of information processing.

SIGNIFICANCE STATEMENT Adaptive behavior relies on the ability to select and store important information amid distraction. Prioritizing encoding of task-relevant inputs is especially critical in threatening or arousing situations, when forming these memories is essential for avoiding danger in the future. However, little is known about the arousal mechanisms that support such memory selectivity. Using fMRI, neuromelanin MRI, and pupil measures, we demonstrate that locus ceruleus (LC) activity amplifies neural gain such that limited encoding resources focus even more on prioritized mental representations under arousal. For the first time, we also show that LC structure relates to its involvement in threat-related encoding processes. These results shed new light on the brain mechanisms by which we process important information when it is most needed.