Effective connectivity of the anterior hippocampus predicts recollection confidence during natural memory retrieval

Yudan Ren,Simon B Eickhoff,Lei Guo,Saurabh Sonkusare,Tianji Pang,Jinglei Lv,Christine C Guo,Vinh T Nguyen,Michael Breakspear

doi:10.1038/s41467-018-07325-4

Abstract

Human interactions with the world are influenced by memories of recent events. This effect, often triggered by perceptual cues, occurs naturally and without conscious effort. However, the neuroscience of involuntary memory in a dynamic milieu has received much less attention than the mechanisms of voluntary retrieval with deliberate purpose. Here, we investigate the neural processes driven by naturalistic cues that relate to, and presumably trigger the retrieval of recent experiences. Viewing the continuation of recently viewed clips evokes greater bilateral activation in anterior hippocampus, precuneus and angular gyrus than naïve clips. While these regions manifest reciprocal connectivity, continued viewing specifically modulates the effective connectivity from the anterior hippocampus to the precuneus. The strength of this modulation predicts participants’ confidence in later voluntary recall of news details. Our study reveals network mechanisms of dynamic, involuntary memory retrieval and its relevance to metacognition in a rich context resembling everyday life.

Highlights

Human interactions with the world are influenced by memories of recent events
We first show that passive viewing of the news clips that have personal, historical context robustly increases engagement of the anterior hippocampus, as well as a constellation of regions in the default mode network (DMN), executive and control systems and cerebellum
Employing a systematic approach to construct model space based on dynamic causal modelling (DCM), we showed that the effects in the anterior hippocampus, precuneus and angular gyrus could be accounted for by increased, context-specific effective connectivity

Summary

Introduction

Human interactions with the world are influenced by memories of recent events. This effect, often triggered by perceptual cues, occurs naturally and without conscious effort. To improve the ecological validity of experimental paradigms, recent studies have employed naturalistic stimuli to engage and investigate neural processes underlying episodic memory retrieval[19,20] These naturalistic functional magnetic resonance imaging (fMRI) studies, using film and spoken narratives, have further extended our understanding of the role of hippocampus to real-life, dynamic memory processing—interacting with the DMN to support episodic memory retrieval. Few studies have investigated the network mechanisms of the real-life, involuntary memory retrieval and its behavioural relevance To bridge this gap, we designed a paradigm based on news clips: viewing news clips is an almost daily exercise for most people, and implicitly relies upon the involuntary retrieval of information to resume viewing experience following commercial and other breaks in the narrative. Our study addresses the neural mechanism underlying dynamic, involuntary memory retrieval in a naturalistic context resembling the function of memory in real-life

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