Neural Repetition Effects in the Medial Temporal Lobe Complex are Modulated by Previous Encoding Experience

Ciara M Greene,David Soto

doi:10.1371/journal.pone.0040870

Abstract

It remains an intriguing question why the medial temporal lobe (MTL) can display either attenuation or enhancement of neural activity following repetition of previously studied items. To isolate the role of encoding experience itself, we assessed neural repetition effects in the absence of any ongoing task demand or intentional orientation to retrieve. Experiment 1 showed that the hippocampus and surrounding MTL regions displayed neural repetition suppression (RS) upon repetition of past items that were merely attended during an earlier study phase but this was not the case following re-occurrence of items that had been encoded into working memory (WM). In this latter case a trend toward neural repetition enhancement (RE) was observed, though this was highly variable across individuals. Interestingly, participants with a higher degree of neural RE in the MTL complex displayed higher memory sensitivity in a later, surprise recognition test. Experiment 2 showed that massive exposure at encoding effected a change in the neural architecture supporting incidental repetition effects, with regions of the posterior parietal and ventral-frontal cortex in addition to the hippocampus displaying neural RE, while no neural RS was observed. The nature of encoding experience therefore modulates the expression of neural repetition effects in the MTL and the neocortex in the absence of memory goals.

Highlights

The response of the brain to the re-occurrence of past information has been extensively investigated using tasks that require observers to retrieve and match details of past events against current perceptual input
Whole brain analyses were conducted with the goal of assessing regions displaying distinct neural repetition effects in the working memory (WM) and Primed conditions
No significant differences in BOLD response were observed in either direction

Summary

Introduction

The response of the brain to the re-occurrence of past information has been extensively investigated using tasks that require observers to retrieve and match details of past events against current perceptual input. Evidence from functional neuroimaging studies in human and single cell recording in animals has shown that the repetition of stimuli typically results in a reduction of neural activity, a phenomenon termed repetition suppression (RS) [1]. This process is thought to reflect more efficient processing in the brain and has been conceptually linked with behavioural priming mechanisms [2]. Recognition memory tasks typically require participants to make purposeful ‘old/new’ retrieval-based discriminations for test items that may or may not have been previously studied. We hypothesised that the manifestation of repetition-related neural response may be dependent on the nature of previous encoding experience with the stimuli, and that this may be the case even in the absence of memory goals during the assessment of repetition effects

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