Affective Enhancement of Episodic Memory Is Associated With Widespread Patterns of Intrinsic Functional Connectivity in the Brain Across the Adult Lifespan

Abstract

Subjectively arousing experiences tend to be better remembered than neutral ones. While numerous task-related neuroimaging studies have revealed the neural mechanisms associated with this phenomenon, it remains unclear how variability in the extent to which individuals show superior memory for subjectively arousing stimuli is associated with the intrinsic functional organization of their brains. Here, we addressed this issue using functional magnetic resonance imaging data collected at rest from a sample drawn from the Cambridge Centre for Ageing and Neuroscience cohort (N = 269, 18–86 years). Specifically, we performed multi-voxel pattern analysis of intrinsic functional connectivity, an unbiased, data-driven approach to examine whole-brain voxel-wise connectivity patterns. This technique allowed us to reveal the most important features from the high-dimensional, whole-brain connectivity structure without a priori hypotheses about the topography and direction of functional connectivity differences. Behaviorally, both item and associative memory accuracy were enhanced for trials with affectively arousing (positive or negative) stimuli than those with neutral ones. Whole-brain multi-voxel pattern analysis of functional connectivity revealed that the affective enhancement of memory was associated with intrinsic connectivity patterns of spatially distributed brain regions belonging to several functional networks in the cerebral cortex. Post hoc seed-based brain-behavior regression analysis and principal component analysis of the resulting correlation maps showed that these connectivity patterns were in turn primarily characterized by the involvement of heteromodal association and paralimbic (dorsal attention, salience, and default mode) networks of the cerebral cortex as well as select subcortical structures (striatum, thalamus, and cerebellum). Collectively, these findings suggest that the affective enhancement of episodic memory may be characterized as a whole-brain phenomenon, possibly supported by intrinsic functional interactions across several networks and structures in the brain.