Posterior parietal cortex and episodic retrieval: Convergent and divergent effects of attention and memory

Functional neuroimaging studies of humans engaged in retrieval from episodic memory have revealed a surprisingly consistent pattern of retrieval-related activity in lateral posterior parietal cortex (PPC). Given the well-established role of lateral PPC in subserving goal-directed and reflexive attention, it has been hypothesized that PPC activation during retrieval reflects the recruitment of parietal attention mechanisms during remembering. Here, we evaluate this hypothesis by considering the anatomical overlap of retrieval and attention effects in lateral PPC. We begin by briefly reviewing the literature implicating dorsal PPC in goal-directed attention and ventral PPC in reflexive attention. We then discuss the pattern of dorsal and ventral PPC activation during episodic retrieval, and conclude with consideration of the degree of anatomical convergence across the two domains. This assessment revealed that predominantly divergent subregions of lateral PPC are engaged during acts of episodic retrieval and during goal-directed and reflexive attention, suggesting that PPC retrieval effects reflect functionally distinct mechanisms from these forms of attention. Although attention must play a role in aspects of retrieval, the data reviewed here suggest that further investigation into the relationship between processes of attention and memory, as well as alternative accounts of PPC contributions to retrieval, is warranted.Episodic memory—declarative memory for events—has long been known to depend on the medial temporal lobe and, to a lesser extent, the prefrontal cortex (Squire 1992; Shimamura 1995; Wheeler et al. 1995; Gabrieli 1998; Eichenbaum and Cohen 2001; Squire et al. 2004). Recently, an explosion of functional neuroimaging studies has revealed that episodic retrieval is also consistently associated with activity in lateral posterior parietal cortex (PPC), including in the intraparietal sulcus and inferior parietal lobule (Figs. 1, ​,2;2; for detailed review, see Wagner et al. 2005; Cabeza 2008; Cabeza et al. 2008; Ciaramelli et al. 2008; Vilberg and Rugg 2008b; Olson and Berryhill 2009). This unexpected finding raises the possibility that parietal mechanisms may be more central to episodic retrieval than previously thought.Open in a separate windowFigure 1.Anatomy of posterior parietal cortex (PPC). A posterior-lateral view of human PPC is depicted, with PPC separated into dorsal and ventral portions by the intraparietal sulcus (IPS). Dorsal PPC includes the superior parietal lobule (SPL) and IPS. Ventral PPC includes inferior parietal lobule (IPL) and its subregions: supramarginal gyrus (SMG), temporoparietal junction (TPJ), and angular gyrus (AnG).Open in a separate windowFigure 2.Left lateral PPC activity during episodic retrieval. (A) A comparison of hits relative to correct rejections reported by Kahn et al. (2004) revealed “old/new” effects in dorsal PPC, inclusive of IPS. Average signal change within IPS was greater for items perceived as old (hits and false alarms) vs. those believed to be new (misses and correct rejections). (B) A comparison of successful, relative to unsuccessful, cued recall by Kuhl et al. (2007) revealed greater activity in AnG, compatible with the broader literature on recollection success effects (see Fig. 4). In addition, effects were observed in more anterior aspects of ventral PPC (SMG), as well as in dorsal PPC (principally SPL) (see Discussion). (C) Orienting to memory in attempts to recollect, independent of recollection success, is often associated with activity in dorsal PPC. For example, comparison of temporal recency judgments to novelty-based decisions elicited greater IPS activity (Dudukovic and Wagner 2007).At the neuropsychological level, human lesion evidence regarding the necessity of lateral PPC mechanisms for episodic retrieval is limited and mixed (Berryhill et al. 2007; Davidson et al. 2008; Haramati et al. 2008; Simons et al. 2008). By contrast, other neuropsychological data indicate that lateral PPC is unambiguously associated with another cognitive domain—attention (Posner et al. 1984; Mesulam 1999; Parton et al. 2004). This latter lesion literature is further complemented by rich functional neuroimaging evidence implicating dorsal and ventral PPC in goal-directed and reflexive attention, respectively (for review, see Corbetta and Shulman 2002; Corbetta et al. 2008).Drawing from the rich literature linking attention to lateral PPC, memory researchers have recently proposed that lateral PPC activity during episodic retrieval tasks reflects the engagement of attention mechanisms during remembering (Cabeza 2008; Cabeza et al. 2008; Ciaramelli et al. 2008; Olson and Berryhill 2009). Specifically, it has been hypothesized that: (1) Dorsal PPC activity during retrieval may reflect the recruitment of goal-directed attention in service of performing retrieval tasks and (2) ventral PPC engagement during retrieval may mark the reflexive capture of attention by mnemonic representations. While prior comprehensive reviews of the neuroimaging literature on parietal correlates of episodic retrieval have documented functional dissociations along the dorsal/ventral axis of lateral PPC, which qualitatively parallel those seen in the attention literature, evaluation of the hypothesis that PPC retrieval activity reflects attention mechanisms further requires an assessment of the degree to which attention and retrieval effects co-localize. Here we review lateral PPC correlates of both episodic retrieval and attention, with the goal of directly assessing to the degree of anatomic overlap.It should be noted from the outset that the aim of the present review is to evaluate the hypothesis that lateral PPC episodic retrieval effects can be explained in terms of goal-directed and reflexive attention mechanisms. As such, we a priori imposed three constraints that served to focus our treatment of these two substantial literatures. First, while both the dual-attention and memory retrieval literatures focus on effects on the lateral parietal surface, retrieval effects are predominantly left lateralized. Thus, we constrained our analysis of attention and retrieval findings to left lateral PPC.⁵ Second, because prior retrieval reviews focused theoretical discussion on dual-attention accounts, here we similarly constrained our treatment of the extensive attention literature to include only those effects relevant to dual-attention theory. Finally, because the preponderance of evidence offered in support of dual-attention theory''s proposed dorsal attention network derives from studies of visual attention, the present review of the dorsal network is also confined to visual attention. As such, the present review should not be viewed as a comprehensive review of the entire attention literature.We first survey the functional neuroimaging literature on parietal correlates of goal-directed and reflexive attention, and then discuss how these correlates converge and diverge with the patterns of lateral PPC activity present during episodic retrieval. We conclude by considering theoretical frameworks that focus on the role of attention in episodic retrieval, as well as nonattention-based accounts of PPC activity during retrieval, and we highlight open questions that await further investigation.