Abstract

Episodic memory retrieval involves the coordinated interaction of several cognitive processing stages such as mental search, access to a memory store, associative re-encoding, and post-retrieval monitoring. The neural response during memory retrieval is an integration of signals from multiple regions that may subserve supportive cognitive control, attention, sensory association, encoding, or working memory functions. It is particularly challenging to dissociate contributions of these distinct components to brain responses in regions such as the hippocampus, which lies at the interface between overlapping memory encoding and retrieval, and “default” networks. In the present study, event-related functional magnetic resonance imaging (fMRI) and measures of memory performance were used to differentiate brain responses to memory search from subcomponents of episodic memory retrieval associated with successful recall. During the attempted retrieval of both poorly and strongly remembered word pair associates, the hemodynamic response was negatively deflected below baseline in anterior hippocampus and regions of the default network. Activations in anterior hippocampus were functionally distinct from those in posterior hippocampus and negatively correlated with response times. Thus, relative to the pre-stimulus period, the hippocampus shows reduced activity during intensive engagement in episodic memory search. Such deactivation was most salient during trials that engaged only pre-retrieval search processes in the absence of successful recollection or post-retrieval processing. Implications for interpretation of hippocampal fMRI responses during retrieval are discussed. A model is presented to interpret such activations as representing modulation of encoding-related activity, rather than retrieval-related activity. Engagement in intensive mental search may reduce neural and attentional resources that are otherwise tonically devoted to encoding an individual’s stream of experience into episodic memory.

Highlights

  • Functional imaging has the potential to dissect the influences of integrated, but separable, neural processes contributing to successful recall; the challenge remains to identify and isolate such components and dissociate these rapid, transient processes

  • In the present study, negative blood oxygen level dependent (BOLD) signal deflection was observed in anterior hippocampus during the attempted recall of both strongly and poorly remembered word pair associates, and this deactivation was greatest for poorly remembered associations

  • A model of the hemodynamic response in anterior hippocampus was fit to the whole-brain, and a similar pattern of graded deactivation across task conditions was identified in regions associated with the default network

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Summary

Introduction

Functional imaging has the potential to dissect the influences of integrated, but separable, neural processes contributing to successful recall; the challenge remains to identify and isolate such components and dissociate these rapid, transient processes. Regions activated during encoding can be engaged during retrieval of the original memory, suggesting that reactivation of the memory trace and associative re-encoding are additional retrieval sub-processes (Nyberg et al, 2000; Buckner et al, 2001; Woodruff et al, 2005). Distinct elements, such as memory strength and degree of search during memory retrieval attempts, may be highly correlated; studies intending to examine an isolated process may be confounded by these uncontrolled components. Additional investigation is necessary to better identify and understand the neural bases underlying subcomponents of memory retrieval

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