Elsevier

Neuropsychologia

Volume 46, Issue 7, June 2008, Pages 1828-1851
Neuropsychologia

Reviews and perspectives
Top-down and bottom-up attention to memory: A hypothesis (AtoM) on the role of the posterior parietal cortex in memory retrieval

https://doi.org/10.1016/j.neuropsychologia.2008.03.022Get rights and content

Abstract

Recent neuroimaging studies have implicated the posterior parietal cortex in episodic memory retrieval, but there is uncertainty about its specific role. Research in the attentional domain has shown that superior parietal lobe (SPL) regions along the intraparietal sulcus are implicated in the voluntary orienting of attention to relevant aspects of the environment, whereas inferior parietal lobe (IPL) regions at the temporo-parietal junction mediate the automatic allocation of attention to task-relevant information. Here we propose that the SPL and the IPL play conceptually similar roles in episodic memory retrieval. We hypothesize that the SPL allocates top-down attention to memory retrieval, whereas the IPL mediates the automatic, bottom-up attentional capture by retrieved memory contents. By reviewing the existing fMRI literature, we show that the posterior intraparietal sulcus of SPL is consistently active when the need for top-down assistance to memory retrieval is supposedly maximal, e.g., for memories retrieved with low vs. high confidence, for familiar vs. recollected memories, for recognition of high vs. low frequency words. On the other hand, the supramarginal gyrus of IPL is consistently active when the attentional capture by memory contents is supposedly maximal, i.e., for strong vs. weak memories, for vividly recollected vs. familiar memories, for memories retrieved with high vs. low confidence. We introduce a model of episodic memory retrieval that characterizes contributions of posterior parietal cortex.

Introduction

Encoding and retrieval are two fundamental memory operations, the former picking up incoming information and binding it into a memory trace, and the latter assuring that appropriate cues interact with the memory trace, so that memory is recovered and, in the case of explicit memory, delivered to consciousness (Moscovitch, 1992). According to dual-process models of recognition and recall (e.g., Atkinson & Juola, 1974; Jacoby, 1991, Mandler, 1980, Tulving, 1985, Yonelinas, 1994), retrieval operations can be carried out by two independent processes, namely recollection and familiarity (Tulving, 1985, Yonelinas, 1994). Recollection is based on memory for contextual details surrounding the original episode (Dudukovic & Knowlton, 2006; Yonelinas, 2002), and accompanied by a vivid, subjective feeling of reliving the original event (Tulving, 1985; Wheeler, Stuss, & Tulving, 1997), whereas familiarity reflects the global strength of the memory trace without additional qualitative information about the context in which it was acquired (Yonelinas, 1994).

Models of memory retrieval have focused on the medial temporal lobe (MTL) and the prefrontal cortex (see Simons & Spiers, 2003). Typically, in those models, the MTL is concerned with representation of the memory trace, which is supported by an ensemble of MTL and neocortical neurons (Moscovitch, 1992, Moscovitch et al., 2005). At retrieval, the MTL, and the memory trace it mediates, may be accessed directly by a retrieval cue or indirectly via strategic operations mediated by the prefrontal cortex. Various retrieval functions, including initiation and maintenance of retrieval mode, cue specification, monitoring and verification are assigned to different regions of prefrontal cortex (Burgess, Dumontheil, & Gilbert, 2007; Dobbins & Han, 2006; Fletcher & Henson, 2001; Moscovitch and Winocur, 1995, Moscovitch and Winocur, 2002; Wheeler & Buckner, 2003).

The role that attention plays in retrieval is not usually considered in many of these models, the Component Process Model (Moscovitch, 1992, Moscovitch, 1994; Moscovitch & Umiltà, 1991) being an exception. According to that model, during direct retrieval, a (proximal) cue interacts automatically with information stored in memory systems via the MTL. Direct retrieval is thought to be a relatively automatic process, mediated by the MTL, and requiring few attentional resources. In contrast, during indirect retrieval, the target memory is not automatically elicited by the cue, and, therefore, has to be recovered through a strategic search process. Indirect retrieval is mediated by the PFC, and is attention demanding. Accordingly, performance in memory tasks that make demands on indirect retrieval is easily hindered by a concurrent task (e.g., Jacoby, Woloshyn, & Kelley, 1989; Kane & Engle, 2000; Moscovitch, 1994), whereas performance in memory tasks relying on direct retrieval is not. The only time divided attention can interfere with direct tests of memory is when the distracting task competes for the same neocortical representations as the memory task (Fernandes and Moscovitch, 2000, Fernandes and Moscovitch, 2002; but see Carrier & Pashler, 1995). Nevertheless, direct retrieval does inflict costs on the distracting task (e.g., Ciaramelli, Ghetti, & Borsotti, 2008; Craik, Govoni, Naveh-Benjamin, & Anderson, 1996; Fernandes & Moscovitch, 2000). Thus, even when mandatory, episodic memory retrieval usurps attentional resources from ongoing processes.

As this brief summary indicates, studies on attention and memory are concerned with whether memory competes for general or material specific resources, or for output pathways. None of them deals with the different components of attention that figure prominently in the literature (e.g., Corbetta & Shulman, 2002). This is all the more surprising since evidence from electrophysiology (Herron & Wilding, 2005; Rugg & Curran, 2007) and functional neuroimaging (fMRI; e.g., Naghavi & Nyberg, 2005; Wagner, Shannon, Kahn, & Buckner, 2005) consistently shows activity in posterior parietal cortex during memory retrieval. Previous research has shown that the posterior parietal cortex supports distinct attentional systems, which mediate different attentional processes (e.g., Behrmann, Geng, & Shomstein, 2004; Colby & Goldberg, 1999; Corbetta & Shulman, 2002). Thus, its involvement in memory retrieval not only lends support to the notion that attention is needed for episodic memory retrieval, but also raises the question of whether different attentional systems would make separate contributions to this process. Accordingly, a careful examination of the literature suggests that the regions of posterior parietal cortex which are implicated during episodic memory retrieval vary with different retrieval processes and the type of memory that is retrieved (Skinner & Fernandes, 2007).

The aim of the present paper is to advance a hypothesis on the role of posterior parietal cortex during memory retrieval based on the evidence that this brain region supports multiple attentional systems, with distinct attentional functions. According to one prominent theory (Corbetta & Shulman, 2002), the superior attentional system, which involves superior parietal lobe (SPL) regions and is centered on the intraparietal sulcus (IPS), mediates the allocation of top-down attention to specific aspects of the environment, according to the subject's goals. On the other hand, the inferior attentional system, which involves inferior parietal lobe (IPL) regions and is centered on the temporo-parietal junction (TPJ), mediates the automatic capture of attention by salient environmental stimuli (Corbetta & Shulman, 2002; see Fig. 1). In Section 2, we review briefly the literature on the role of SPL and IPL in the attentional domain. We next hypothesize that these two regions play conceptually similar roles in the episodic memory domain as they do in the attentional domain, and formulate predictions derived from our hypothesis (Section 3). In the following sections we test these predictions, by comparing activity in the SPL (BAs 7 and 19) vs. IPL (BAs 39 and 40) in the existing fMRI studies on episodic memory retrieval. Given that recent research on attention has focused specifically on the IPS and TPJ regions (Corbetta & Shulman, 2002), for each condition of interest we will report whether these regions are indeed activated, and, if so, whether the loci of activation correspond to those observed in the attentional literature.

Section snippets

Two attentional systems in the brain

Selective attention is the process whereby a subset of the input is selected preferentially for further processing. Such attentional bias can arise either in a top-down fashion, by voluntarily constraining attentional search to stimuli with a specific property, or in a bottom-up fashion, which occurs when stimuli can capture attention relatively automatically (see Corbetta & Shulman, 2002; Fox, Corbetta, Snyder, Vincent, & Raichle, 2006; Mesulam, 1999; Posner & Petersen, 1990). Voluntary and

The attention to memory (AtoM) hypothesis

As we have discussed, SPL regions are activated when observers voluntarily orient attention to specific aspects of the stimuli that are consistent with an attentional set, whereas IPL activity is observed when task-relevant information is automatically detected. We propose that the SPL and the IPL would play a conceptually analogous role in episodic memory retrieval.

We hypothesize that the SPL supports indirect retrieval, by allocating top-down attentional resources to strategic retrieval

Activation in parietal cortex associated with retrieval success

Preliminary to our consideration of parietal retrieval effects, we sought to identify the posterior parietal lobe regions that consistently showed old/new effects. To this end, we reviewed the findings from event-related fMRI studies that (1) used recognition tasks, (2) contained direct comparison of brain activity for hits and correct rejections, and (3) were published by 2006.

General discussion

Studies in cognitive neuroscience have provided converging evidence that MTL and prefrontal regions of the brain are crucial for episodic memory retrieval (see Baldo & Shimamura, 2002; Moscovitch et al., 2005, Petrides, 2005; Simons & Spiers, 2003). More intriguing is the proposal that the posterior parietal cortex is also implicated in memory retrieval. Rugg and colleagues first reported consistent retrieval success effects in parietal cortex in ERP studies (for review, see Rugg & Curran, 2007

Conclusions and a model

We have introduced a dual-process hypothesis of the role of the posterior parietal cortex in memory retrieval, the AtoM hypothesis. A review of the existing fMRI literature provides initial support for our hypothesis. We end by introducing an extension of the Component Process Model (Moscovitch, 1992, Moscovitch, 1994; Moscovitch & Umiltà, 1991; Moscovitch and Winocur, 1995, Moscovitch and Winocur, 2002), that includes the AtoM hypothesis (see Fig. 4).

During direct retrieval, a cue interacts

Acknowledgements

We thank Patrick Davidson and Susanne Ferber for helpful comments on a draft of the paper, Julia Spaniol and Alice Kim for drawing part of the papers to our attention, and Maroquine Aziz for technical support. This research was funded by a Marie Curie individual fellowship to EC and a CIHR (Canada) grant to MM and CG.

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