Parietal Lobe Contributions to Episodic Memory Retrieval

Review TRENDS in Cognitive Sciences Vol.9 No.9 September 2005

Parietal lobe contributions to episodic memory retrieval

Anthony D. Wagner1, Benjamin J. Shannon2, Itamar Kahn1 and Randy L. Buckner2

1Department of Psychology and Neurosciences Program, Stanford University 2Howard Hughes Medical Institute, Departments of Psychology, Radiology, and Anatomy & Neurobiology, Washington University in St. Louis

Although the parietal lobe is not traditionally thought to have documented greater activation during hits than support declarative memory, recent event-related fMRI during CRs in posterior parietal cortex (PPC), including studies of episodic retrieval have consistently revealed a inferior and superior parietal lobules, as well as medial range of memory-related influences on activation in structures that extend from precuneus into posterior lateral posterior parietal cortex (PPC) and precuneus cingulate and retrosplenial cortices. extending into posterior cingulate and retrosplenial Beyond simply identifying neural regions that demon- cortex. This article surveys the fMRI literature on PPC strate old/new effects (Box 1), fMRI studies have activation during remembering, a literature that comp- suggested a range of distinct memory-related influences lements earlier electroencephalography data. We con- on parietal activation. For example, activation in PPC sider these recent memory-related fMRI responses modulates based on the perception that information is old within the context of classical ideas about parietal (or familiar) even when that perception is in error [10,11]. function that emphasize space-based attention and PPC activation also increases when recognition is motor intention. We conclude by proposing three accompanied by the recollection of event details [12–15], hypotheses concerning how parietal cortex might and, in forced-choice recognition designs, regions in PPC contribute to memory. are engaged when retrieval is oriented towards recollecting episodic details as compared with detecting item familiarity [13,16,17]. This article surveys these recent fMRI findings of PPC activation during episodic retrieval. Introduction In the course of doing so, we consider how these findings Episodic memory – conscious memory for everyday events from the memory literature relate to classical attention [1] – has long been known to depend on the medial and intention accounts of parietal function. We conclude temporal lobe (MTL) memory system [2,3] and on prefrontal contributions to encoding and retrieval [4,5]. Box 1. Early PET and fMRI observations Although theoretical and experimental emphasis remains on specifying how MTL and prefrontal structures mediate Early PET and fMRI studies that compared extended epochs (blocks) the acquisition, consolidation and retrieval of episodic of episodic retrieval with non-memory control conditions consistently revealed activation in PPC, including during recognition of memories, an emerging body of functional imaging words, sentences, and pictures (e.g. [28,64–66]) and during cued- evidence suggests that a full understanding of episodic recall for words and pictures (e.g. [67–70]). Initial studies emphasized memory might also require specification of parietal retrieval-related activations in the precuneus – although activations contributions to retrieval [6,7].Herewereviewthis often extended to lateral PPC – with one hypothesis being that surprising new literature and develop hypotheses regard- precuneus participates as part of the ‘mind’s eye’ to reinstate visual content during retrieval [71]. Modest debate emerged as retrieval ing how parietal cortex might support remembering. correlates in multiple parietal regions were observed to generalize The basic phenomenon that has sparked interest in across content domains (e.g. [70]). parietal contributions to episodic retrieval is that differ- Other early block-design studies attempted to isolate correlates of ential parietal responses are observed when individuals successful retrieval, either by manipulating the percentage of old correctly recognize previously encountered old items (hits) and new items in retrieval blocks (for review, see [72]) or by varying encoding conditions to elicit differential levels of subsequent as compared with correctly identifying new unstudied retrieval success (e.g. depth-of-processing manipulations; items (correct rejections; CRs). The earliest observations [28,73,74]). Whereas some studies failed to observe modulations in of such ‘old/new’ effects (alternatively labeled ‘retrieval parietal activation as a function of retrieval success (e.g. [28]), others success’ effects; [8]) were obtained with electroencephalo- revealed increased activation during conditions fostering greater retrieval. For example, Tulving et al. [64] observed greater parietal graphy, wherein the magnitude of event-related potentials activation when performing recognition on blocks of predominantly (ERP) differed at left and medial parietal scalp electrode old versus blocks of predominantly new stimuli. Habib and Lepage sites during hits and CRs (for review, see [9]). More [75] performed a meta-analysis that combined these data with four recently, event-related functional MRI (fMRI) studies other independent PET studies. Anticipating the results of many later studies, their meta-analysis revealed greater activation in left lateral Corresponding authors: Wagner, A.D. ([email protected]), PPC and in precuneus when many old items occurred within a Buckner, R.L. ([email protected]). recognition block as compared with few items. Available online 28 July 2005 www.sciencedirect.com 1364-6613/$ - see front matter Q 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.tics.2005.07.001 446 Review TRENDS in Cognitive Sciences Vol.9 No.9 September 2005 by proposing a set of hypotheses about how parietal cortices might contribute to remembering. (a) IPS The old/new effect – a multi-study analysis IPL Event-related fMRI studies of retrieval have revealed greater PPC activation during hits as compared with CRs. Across experiments, such old/new effects generalize across verbal and visual-object targets (e.g. words and faces, [8,18–20]) and across yes/no recognition, remember/know, recognition confidence, and source recollection paradigms [11,12,14,15,21,22], demonstrating that certain PPC regions are sensitive to, or signal some aspect of, successful retrieval [8,10,12,23]. Although PPC old/new effects are frequently obtained, it is also the case that activation in certain PPC regions does not exclusively (b) track retrieval success, as indexed by old/new effects. For example, although Herron et al. [24] observed old/new effects in portions of left PPC irrespective of the percentage of old items within a recognition test (which varied from 25% to 75%), old/new effects in one region of left superior parietal cortex were probability dependent, only being observed during the 25% old condition. Thus, there may be heterogeneity across parietal cortex in relation to memory. To begin our consideration of parietal retrieval effects, we sought to localize regions consistently showing old/new Figure 1. Convergence analysis of the old/new effect. Consistent old/new effects are effects. To this end, we constructed a multi-study plotted on the (a) lateral and (b) medial cortical surface of the brain, based on their reproducibility across studies using the PALS approach [26]. The left hemisphere is convergence map detailing regions showing old/new illustrated. The inset shows the inferior parietal lobule (IPL) and the intraparietal effects across seven independent retrieval contrasts sulcus (IPS). Old/new effects were identified at a threshold of p!0.001 in seven [8,11,15,25]. The experiments included auditory and separate event-related fMRI contrasts (data included from [8,11,15,25]). All contain direct comparisons of hits and correct rejections (CR) during recognition tasks. visual items, verbal and non-verbal stimuli, and required Voxels independently significant in 4 or more of the 7 contrasts are shown different responses. For each independent contrast, a (yellowZ7 of 7). Clear convergence is observed in lateral parietal cortex (inferior whole-brain activation map was constructed identifying parietal and a small focus in superior parietal), as well as along the medial surface extending from precuneus into posterior cingulate and retrosplenial cortex. The voxels showing an increased hemodynamic response for midline region within the outlined area is not part of the cortical surface and is hitrelativetoCRtrials(thresholdedatp!0.001). therefore masked. Convergence across these maps was assessed by plotting the number of studies demonstrating an old/new effect, memory-gated orienting effects). Recent fMRI data indi- with this convergence projected onto the cortical surface cate that PPC activation can be modulated by (a) the using a novel atlas approach developed by Van Essen and subjective perception that items are old, (b) recollective- as colleagues [26] (using Caret software [27]). Strikingly, compared with familiarity-based recognition, and (c) prominent old/new effects were obtained in precuneus retrieval oriented towards the recollection of episodic extending into posterior cingulate and retrosplenial details versus detecting differential stimulus familiarity. cortices, as well as in left lateral parietal cortex in 100% (7 of 7) of the included contrasts (Figure 1). Identified The subjective perception that information is old lateral parietal regions included an expanse of inferior Figure 1 highlights regions showing greater responses parietal cortex, notably in intraparietal sulcus (IPS) and when subjects correctly identify old information as old laterally in inferior parietal lobule (IPL), and a more focal (hits) and new information as new (CRs). What about region in superior parietal cortex. memory errors? People often fail to recognize previously encountered items (misses), and sometimes mistakenly Factors that modulate parietal responses at retrieval claim to recognize new items (false alarms). Examining PPC regions show old/new effects that generalize across memory errors can provide evidence regarding whether different item modalities, variable response conditions, parietal old/new effects are associated with the conscious and multiple data samples across laboratories (Figure 1), perception that an item was previously encountered or, suggesting that these regions consistently track processes alternatively, with the item’s history irrespective of its correlated with the successful retrieval of episodic perceived memory status. information. However, comparisons between hits and Two recent fMRI studies addressed this important CRs do not specify the particular mnemonic attributes issue, measuring parietal activation not only during that give rise to the observed activation differences, accurate responses but also during memory errors because the processing of hits and CRs can differ along [10,11]. Inclusion of misses and false alarms allowed several dimensions (e.g. old/new differences could reflect determination of whether activation tracked item history recollection, item familiarity, repetition priming, or (i.e. missesOfalse alarms, which would support a www.sciencedirect.com Review TRENDS in Cognitive Sciences Vol.9 No.9 September 2005 447 repetition priming account of old/new effects) or perceived Box 2. Dual-process models of recognition recognition (i.e. false alarmsOCRs). Wheeler and Buckner [10] and Kahn et al. [11] both observed strong activation in Dual-process theories of recognition suggest that two types of left inferior parietal cortex to false alarms consistent with a mnemonic information can support recognition decisions. As one basis for recognition, the test probe can be used to retrieve perceived recognition account (Figure 2). Intriguingly, Kahn contextual details regarding the previous encounter with the et al. further observed that this region, although modulated stimulus, yielding recollection of the past event (the essence of by perceived oldness, was not modulated by the recollection episodic memory; [1]). Alternately, a test probe might be recognized of episodic details, raising the question of how left PPC because it yields a perception of a recent encounter, or item activation relates to recollection and familiarity (Box 2). familiarity, despite the fact that no contextual details are recollected [63,76,77]. Recollection and familiarity are often measured using ‘remember/know’ and source-memory tasks. The remember/know Recollection versus familiarity procedure is posited to reveal differential reliance on recollection and Several event-related fMRI studies have explored whether familiarity, such that subjects respond ‘remember’ to items recognized based on conscious recollection of contextual details and parietal activation varies according to whether recognition ‘know’ when there is a sense that the item was previously is accompanied by recollection or familiarity. Initial data encountered but an absence of recollection (e.g. [78,79]; but see, indicate that, when sorting retrieval trials by remember/ [59]). In source paradigms, subjects discriminate between previously know, source recollection, and study-depth status, recollec- studied and new items, and try to recollect a particular (source) detail tion-sensitive activation is observed in certain medial and about each studied item’s past encounter; recollection is essential to accurate source memory [55]. Accordingly, neural correlates of lateral parietal regions [12–15,22]. A convergence analysis recollection are operationalized as the contrast between hits across studies from our laboratories identified recollection- accompanied by remember versus know responses or the contrast sensitive parietal foci in precuneus, extending into between Source–Hit and Source–Miss trials. Anticipating findings in posterior cingulate and retrosplenial cortex, and in left- fMRI studies, the ERP literature has revealed parietal-situated lateralized PPC (excluding the IPS) (Figure 3). old/new effects (400–800 ms post-stimulus onset) that track the presence or absence of recollection in remember/know and source Although Figure 3 points to some convergence, evidence memory paradigms (for review, see [80]). from studies examining the consequences of depth of

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Figure 2. Parietal activation tracks the perception that an item is old. (a) Statistical parametric maps from Kahn et al. [11] show increased activation during hits vs. CR and during false alarm (FA) vs. CR responses. (b) Activity associated with correct and incorrect responses are plotted from two recognition experiments [10,11]. The mean signal magnitude (bar graphs) across response types is plotted from a targeted left inferior parietal region showing old/new effects (axial plane). Crucially, in both experiments, incorrect responses (MISS, old items endorsed as new; FA, new items endorsed as old) were accompanied by activity magnitudes that fell between those elicited by correct responses (HIT and CR). www.sciencedirect.com 448 Review TRENDS in Cognitive Sciences Vol.9 No.9 September 2005

Wheeler and Buckner [15] identified a region along the (a) banks of the IPS that showed similarly increased activity IPS for remember and know responses compared with CRs, IPL thus showing an effect that tracked item familiarity. Earlier remember/know studies also revealed that left IPS is insensitive to recollection [12,30], and source memory studies demonstrated similarly increased activity in left IPS during Source-Hits and Source-Misses compared with CRs [11,22]. In contrast to IPS, Wheeler and Buckner [15] identified two additional left PPC regions, lateral and posterior to the IPS, that responded preferentially to remember decisions (see also, [31]). Again, earlier Remember/Know studies also observed selective increases during remember responses in similar left lateral PPC (b) regions [12,14,15]. Our convergence maps lend further support for this anatomic distinction, revealing consistent old/new effects in left IPS (see Figures 1 and 2) but recollection-sensitive effects in more lateral inferior parietal regions (Figure 3). Although not apparent in Figure 3, source retrieval studies also point to an additional region – near left superior parietal cortex – that is responsive to recollection outcome, as evidenced by increased activation during Source-Hits compared with Source-Misses [11,13,24,32]. Collectively, it appears that multiple distinct foci in PPC can be modulated by recollective experience: lateral and Figure 3. Convergence analysis of successful recollection. Activity is shown on (a) lateral and (b) medial cortical surfaces, as in Figure 1, reflecting convergence across posterior inferior parietal regions (lateral to IPS), medial event-related fMRI conditions that contrast remember vs. know recognition trials regions near precuneus, and (to a lesser extent) superior [15], Source-Hit vs. Source-Miss recognition trials [11,13], and recognition following Deep vs. Shallow encoding [25]. All contain direct comparisons of hits parietal cortex [11–15,25]. Responses in left IPS, by accompanied by high levels of recollection as compared with hits based contrast, appear to correlate with item familiarity rather preferentially on familiarity. Voxels independently significant in 2 or more of the than recollection. 4 contrasts are shown (yellowZ4of4). processing during encoding for subsequent recognition- Retrieval orientation related parietal activation is mixed. For example, Although parietal responses are influenced by the Shannon and Buckner [25] observed greater parietal mnemonic status (or perceived status) of the recognition activation during recognition following deep encoding probe, recent data indicate that PPC activation also than following shallow encoding. By contrast, Kahn modulates based on the type of mnemonic information to which subjects orient during attempts to remember et al. [11] observed comparable activation following deep (‘retrieval orientation’; e.g. [13,16,32–38]). Important and shallow encoding (see also, [28]), with activation data come from fMRI studies of forced-choice recognition, tracking whether subjects recollected having performed wherein retrieval orientation was manipulated by varying the shallow task. It is unclear whether these divergent whether the retrieval task required recollective- (source findings partly reflect a difference in the size of the study decisions) or familiarity-based (item novelty and temporal depth effect (0.38 in Shannon and Buckner compared with recency decisions) information, holding the mnemonic 0.17 in Kahn et al.), the encoding tasks (abstract/concrete history of the test probes constant ([13,16,17], see also [39]). and uppercase/lowercase vs. meaning-based imagery and Initial evidence for retrieval orienting effects was orthographic-to-phonological transformation), or type of obtained by Dobbins et al. [13], who compared activation recognition test (yes/no vs. source recognition). during source recollection decisions with that during The sensitivity of some parietal regions to recollection temporal recency decisions. Whereas greater MTL acti- is also, on first glance, difficult to reconcile with other vation was observed during source vs. recency judgments, observations of old/new effects that are almost surely with hippocampal activation tracking source recollection correlated with familiarity-based decisions. For example, success, increased left PPC activation was present during parietal old/new effects can occur (i) following repetitive recollective-orienting independent of recollection success shallow encoding designed to maximize familiarity-based (i.e. activation did not differ between successful vs. responding [29], (ii) for both fast and slow recognition unsuccessful source decisions). This pattern suggests responses [23], and (iii) when comparing know responses that specific parietal mechanisms may be recruited during with CRs (e.g. [12,15,30]). Possible resolution of this attempts to selectively retrieve event-specific details, apparent inconsistency is suggested by recent evidence consistent with an ‘attention to memory’ (or internal that functionally distinct PPC subregions are differen- representations) hypothesis (see below). tially sensitive to recollection success and perceived Two subsequent studies explored the generalizability of familiarity [15,31]. recollective-orienting effects in left PPC [16,17], www.sciencedirect.com Review TRENDS in Cognitive Sciences Vol.9 No.9 September 2005 449 contrasting source recollection to item novelty decisions have motivated the space-based attention and motor using three-alternative forced-choice with words or intention theories of parietal function [44,45]. An import- pictures. Dobbins and Wagner [17] included two source ant question is whether memory-related parietal recollection conditions – one requiring attempts to recover responses can be explained in terms of these classical perceptual episodic details and the other requiring ideas. For example, given that eye movements [46] and attempts to recover conceptual episodic details. Both response times often vary between old and new items, studies revealed greater left PPC activation during source might old/new effects in IPS and superior parietal lobule recollection as compared with novelty detection attempts reflect attentional or intentional processes differentially [16,17], with a convergence analysis revealing high engaged as a result of perceived familiarity? across-experiment overlap in left IPL and IPS (Figure 4). This possibility was recently tested by Shannon and Thus, recollective-orienting effects in left PPC generalize Buckner [25], who demonstrated that old/new effects in across word and picture stimuli, and across attempts to left and medial parietal regions persist across manipula- recollect conceptual and perceptual episodic details. tions designed to affect visuospatial attention and motor Moreover, these left PPC recollective-orienting effects planning (Figure 5). For example, PPC old/new effects converge with other observations of differential left were observed when test materials were natural sounds parietal activation when comparing source with item (e.g. a dog barking) as well as visual pictures. Assuming recognition [40,41]. that old and new sounds are unlikely to elicit differential Given the apparent overlap between the IPS and IPL attention to specific spatial locations, these findings regions sensitive to recollective-orienting (Figure 4) and suggest that a spatial attention account cannot fully those showing old/new effects (Figure 1), intriguing handle memory-related PPC effects (for related recollec- questions arise regarding how to understand the tive-orienting results, see [17]). In a second study, functional contributions of left PPC during retrieval. Shannon and Buckner manipulated response contingen- One possibility is that recollective-orienting effects may cies. In one condition, standard old/new recognition be superimposed on old/new effects, although presumably decisions were made, whereas in two other conditions, familiarity-based old/new effects did not differ across the subjects either responded only to the old items or only to recollective- and familiarity-orienting conditions in these the new items. All three conditions yielded PPC old/new experiments because the mnemonic history of the test effects, including increased activation to old items even probes was held constant. To the extent that this account when responses were made only to new items. These data has merit, it raises the possibility that some PPC old/new suggest that PPC old/new effects are unlikely to pre- effects may reflect memory-gated engagement of PPC dominantly reflect memory modulation of motor intention selective attention mechanisms that support strategic mechanisms. orienting to memory. We return to this, and other possibilities, below in the course of proposing hypotheses Understanding parietal contributions to retrieval regarding PPC contributions to retrieval. Clues about parietal contributions to memory come from anatomy. Lateral parietal, retrosplenial, and posterior Relation to classical accounts of parietal function cingulate cortices are connected directly or indirectly to Lesions to parietal cortex can result in neglect, an the MTL [47–49]. Monkey IPL has direct reciprocal attentional deficit, or apraxia, a deficit in planning projections to parahippocampal cortex [48,50] and direct motor movements [42,43]. Such observations, together projections to hippocampus [51]. Along the midline, with data from single-unit recording studies in monkeys, afferent connections to retrosplenial cortex are dominated

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Figure 4. Convergence analysis of recollection orienting. (a) Using a format similar to Figure 1, the convergence across three forced-choice recognition experiments contrasting conceptual source recollection vs. item recency decisions [13], conceptual source recollection vs. novelty detection [16], and both perceptual and conceptual source recollection vs. novelty detection [17] is shown. Across all three contrasts, the items are held constant with the retrieval instructions differentially orienting the subjects to recollection. Voxels independently signiﬁcant in 1 or more of the 3 contrasts are shown (yellowZ3 of 3). Consistent effects were observed in IPS and laterally in IPL. (b) The peak signal magnitudes in left IPS are plotted for the conceptual source recollection, perceptual source recollection, and novelty detection conditions of Dobbins and Wagner [17]. Above baseline percentage signal change was comparable during both recollection conditions, whereas orienting to novelty did not markedly deviate from baseline. www.sciencedirect.com 450 Review TRENDS in Cognitive Sciences Vol.9 No.9 September 2005

impairments – a phenomenon termed ‘retrosplenial (a) (b) amnesia’ [52]. Reviewing case studies of retrosplenial 0.3 lesions, Kobayashi and Amaral note that memory pro- blems can occur even following relatively circumscribed lesions [49]. Second, Alzheimer’s disease, with its hall- mark memory impairment early in disease progression, is 0.2 associated with metabolic disturbances in medial and lateral parietal regions that overlap fMRI old/new effects, and similar parietal metabolic changes have been reported

HITÐCR in amnesia following MTL damage (for review, see [53]). 0.1 Thus, although a gap exists between neuropsychological

signal difference (%) signal difference and imaging data, there are hints that at least some of the parietal regions modulated during memory retrieval may be relevant to clinical impairment, perhaps as functional 0.0 components interconnected with the MTL. Pic Snd Old New As a guide for subsequent investigation and debate, we Modality Response conclude by speculating about possible ways in which PPC

TRENDS in Cognitive Sciences could contribute to episodic retrieval, entertaining three hypotheses. We emphasize that these proposals are Figure 5. Parietal regions showing mnemonic effects do so across manipulations of speculative, as too little is presently known to develop visuospatial attention and motor intention. Regions selective for old/new effects are plotted across manipulations of (a) modality of retrieval cue and (b) response target specific models. Additional forms of data, including single- during old/new recognition paradigms. Data are from Shannon and Buckner [25]. unit recordings in monkeys performing recognition, will The mean signal magnitudes represent the difference between HITs and CRs in be required to refine and test these ideas. each of the four conditions. In (a) the modality of the test cues is manipulated between pictures (Pic) and sounds (Snd). In (b) the response is manipulated between responding only to Old item targets or only to New item targets. In all Attention to internal representations hypothesis conditions, HITs show greater activity than CRs suggesting a contribution to PPC regions may be part of a network that supports mnemonic processes that cannot be explained by differences in visuospatial attention and motor planning. attention directed at internal, mnemonic representations. In many situations external cues provide the dominant by MTL projections. Kobayashi and Amaral [49] specu- constraints that drive perception and action, and net- late, based on this anatomy, that retrosplenial cortex acts works including specific PPC regions participate in as an interface zone between the working memory stimulus-driven attention [54]. Shannon and Buckner (executive) functions enabled by prefrontal cortex and [25] provide evidence arguing against the interpretation the declarative memory functions subserved by the MTL that mnemonic modulation of activation in all PPC regions (see also, [52]). Although homologies between human and is a marker of stimulus-directed visuospatial attention. macaque anatomy must be considered cautiously, there However, memory tasks typically demand attentional are likely to be anatomical projections that provide a route shifts to representations that rely on derived internal for MTL to interact with parietal cortex in the service of information. PPC regions might contribute to shift declarative memory. PPC and retrosplenial cortex might attention to, or maintain attention on, internally gener- reflect major pathways through which the MTL influences ated mnemonic representations. Given the apparent cortical information processing. sensitivity of some PPC responses to episodic retrieval, A natural question to ask is why parietal lesions are not including recollective-orienting, these regions may be generally associated with robust episodic memory deficits. constrained to directing attention to a limited set of At present, the source of the divergence between imaging internal representations – perhaps those dependent on correlates of retrieval and lesion consequences for the MTL [55,56]. Indeed, it would not be surprising if remembering remains unclear. One possibility is that, there were attentional networks specialized for directing although PPC regions are modulated by retrieval information processing to emphasize medial-temporal demands, these regions do not contribute to episodic dependent processes, much as attention can serve to memory in a manner that is important for memory enhance processing in ventral and dorsal visual pathways. expression. On this account, the observations reviewed here are epiphenomenal – that is, PPC does not make Mnemonic accumulator hypothesis direct contributions to retrieval. Alternatively, subtle and A second possibility anchors on the observed relation as yet undetected mnemonic deficits may follow PPC between recognition decisions and activation levels in lesions, deficits that might be revealed only under PPC. Activation in some parietal regions correlates with restricted circumstances. Studies of patients with focal successful memory retrieval and with memory errors lesions of the specific parietal regions identified by fMRI or [10,11], raising the possibility that the strength of transient disruption of these regions with transcranial activation contributes to the eventual decision [31]. Such magnetic stimulation are required to determine whether a property is reminiscent of other proposed forms of mild but reliable memory deficits follow focal parietal information accumulation within PPC regions. For dysfunction. example, monkey area LIP plays a role in integrating A few related observations are worth considering. First, sensory signals about motion in the service of eye lesions to parietal midline structures do produce memory movements. Shadlen and Newsome [57] have proposed www.sciencedirect.com Review TRENDS in Cognitive Sciences Vol.9 No.9 September 2005 451 that ‘Sensory data must be interpreted to execute, revise, orientation, although it less readily explains why atten- or delay pending action’ ([57], p. 1916). By their view, LIP tional resources would be deployed in an uneven manner participates to accumulate, or temporally integrate, between successful and failed memory retrieval attempts. opposing sensory signals until a criterion is reached that In this latter regard, one possibility is that rapidly leads to the decision. emerging mnemonic information gates parietal atten- Recognition memory decisions are likely to require a tional mechanisms, providing a means to control retrieval parallel accumulation of evidence about the history of a processing strategies [11]. By contrast, the accumulator stimulus. For example, Ratcliff [58] has proposed that hypothesis suggests a form of strength theory that maps memory retrieval is accomplished by a diffusion process parietal processes to memory decisions. To the extent that during which evidence for or against a memory decision is the left inferior parietal regions that show recollection accumulated. Similarly, an accumulator hypothesis is effects perform such an accumulation process, this finding consistent with models proposing that recognition would appear to diverge from high-threshold models of decisions are based on a signal-detection process that recollection (e.g. [63]), lending support to signal detection compares a single memory-strength signal with a decision models that operate on continuous measures of recollec- criterion [59] or that compares the integration of two tive information [55,60]. Importantly, the observation of continuous signals – one recollective- and one familiarity- functionally dissociable PPC subregions raises the possi- based – with a decision criterion [60]. bility that these distinct PPC structures contribute We view it as an exciting possibility that subsequent differently to episodic retrieval, and therefore are best research will establish a more direct link between explained by alternative hypotheses. Moreover, we note responses in specific PPC regions and the accumulation that the possibilities are not restricted to the three of mnemonic evidence – perhaps through interactions with the MTL. Within such a view, parietal cortex contains alternatives advanced here (e.g. it is also possible that a set of contiguous areas that perform loosely similar PPC could support a mnemonic reference frame). integration functions, but differ depending on the input– Although we do not know what will emerge from these output structures. Area LIP might gain its properties from speculative ideas, the hope is that they will help constrain, connections to extrastriate visual regions and projections or even alter, current models of episodic remembering and to frontal regions involved in eye movement preparation. parietal function (see also Box 3). Other PPC areas might perform similar integrative functions but gain distinct properties via their connections. Relevant to memory, regions in lateral PPC might Box 3. Questions for future research perform analogous computations on inputs from the MTL, † contributing to decision processes that concern an item’s Data support the view that IPS and IPL are sensitive to retrieval success and recollective-orienting. Are these perspectives mutually mnemonic status. exclusive or do orienting effects mark modulatory processes that operate independent of (or interactively with) PPC contributions to Output buffer hypothesis retrieval success? A third possibility is that PPC regions dynamically † fMRI data regarding parietal contributions to memory predominantly derive from recognition and source-judgment tasks, and represent retrieved information in a form accessible to related variations. Will studies using generative memory paradigms decision-making processes, analogous to Baddeley’s pro- – e.g., free recall and cued recall – provide additional important posed active (working) memory buffers [61]. Indeed, constraints on models of PPC memory function? evidence from lesion and functional studies implicate left † As might be predicted by the accumulator hypothesis, does neural parietal regions in phonological storage, although the activity in parietal cortex track the timing of recognition decisions? For example, do recognition reaction times correlate with the precise relation of these parietal regions to those active magnitude of evoked potentials/fields in IPS and IPL? Do the during episodic retrieval is unclear. From this perspective, temporal profiles of IPS and IPL responses differ for recollection- although long-term memories (the ‘engrams’) are not and familiarity-based decisions? stored in neuronal firing patterns, to influence decision- † Do lateral and medial parietal cortices make necessary contri- making, such memories must be expressed in active butions to episodic retrieval, such that focal lesions or TMS-induced transient disruption of these structures result in retrieval deficits that neuronal response patterns. PPC could act as the buffer are distinguishable from encoding deficits? To the extent that PPC into which stored information is transferred. Importantly, regions are necessary for intact retrieval performance, does lesion such active representations are not likely to be restricted evidence support the fMRI-suggested functional dissociation to PPC. The phenomenon of reinstantiation (or re- between IPS and IPL? † capitulation), in which memory retrieval activates How do PPC regions interact with medial temporal lobe mechanisms that support episodic retrieval? Do PPC regions gate engage- modality-specific sensory areas, suggests that at least ment of strategic retrieval processes subserved by the prefrontal part of the retrieved information is represented in the cortex and known to be crucial for successful episodic recollection? corresponding sensory areas [11,62]. Nevertheless, PPC † Can we document anatomical connections between PPC and MTL in might be centrally involved in the representation process. humans using functional connectivity and white matter track tracing methods? Although studies of monkeys have documented connections between PPC and MTL regions, inferring functional homology Relation to the data between humans and non-human primates is not foolproof. Can we Each of our speculative hypotheses would appear to establish across-species functional homologies, perhaps through account for particular portions of the data. For example, single-unit recording and fMRI studies of monkeys performing the attention to internal representations hypothesis recognition memory tasks comparable with those studied in humans? suggests ways to understand the effects of retrieval www.sciencedirect.com 452 Review TRENDS in Cognitive Sciences Vol.9 No.9 September 2005

Conclusions 10 Wheeler, M.E. and Buckner, R.L. (2003) Functional dissociation As surveyed here, fMRI studies have revealed the among components of remembering: Control, perceived oldness, and surprising (but remarkably consistent) finding that content. J. Neurosci. 23, 3869–3880 11 Kahn, I. et al. (2004) Functional-neuroanatomic correlates of specific parietal regions are active during episodic recollection: Implications for models of recognition memory. retrieval tasks. The basic observations can be summarized J. Neurosci. 24, 4172–4180 as follows: 12 Henson, R.N.A. et al. (1999) Recollection and familiarity in recognition (1) Multiple parietal regions are active during episodic memory: An event-related functional magnetic resonance imaging retrieval, including regions within the intraparietal study. J. Neurosci. 19, 3962–3972 13 Dobbins, I.G. et al. (2003) Memory orientation and success: Separable sulcus extending laterally to the inferior parietal neurocognitive components underlying episodic recognition. Neuro- lobule, as well as midline structures that extend from psychologia 41, 318–333 the retrosplenial cortex and posterior cingulate to the 14 Eldridge, L.L. et al. (2000) Remembering episodes: A selective role for precuneus. the hippocampus during retrieval. Nat. Neurosci. 3, 1149–1152 (2) During episodic retrieval, parietal regions show 15 Wheeler, M.E. and Buckner, R.L. (2004) Functional-anatomic correlates of remembering and knowing. Neuroimage 21, 1337–1349 increased activity to recognized old items (hits) and 16 Dobbins, I.G. et al. (2002) Executive control during episodic retrieval: mistakenly recognized new items (false alarms) as Multiple prefrontal processes subserve source memory. Neuron 35, compared with correctly rejected new items and 989–996 forgotten old items (misses). This observation general- 17 Dobbins, I.G. and Wagner, A.D. (2005) Domain-general and domain- izes across different materials, response conditions, and sensitive prefrontal mechanisms for recollecting events and detecting novelty. Cereb. Cortex (e-pub ahead of print) task formats. 18 McDermott, K.B. et al. (2000) Retrieval success is accompanied by (3) Some lateral and medial parietal regions correlate enhanced activation in anterior prefrontal cortex during recognition with the phenomenological experience of remembering memory: An event-related fMRI study. J. Cogn. Neurosci. 12, 965–976 – activation increases when the subject reports 19 Henson, R.N. et al. (2002) Face repetition effects in implicit and recollecting the earlier event or recollecting source explicit memory tests as measured by fMRI. Cereb. Cortex 12, 178–186 20 Leube, D.T. et al. (2003) Successful episodic memory retrieval of newly details surrounding the event, even when memory learned faces activates a left fronto-parietal network. Brain Res. Cogn. errors are made. Brain Res. 18, 97–101 (4) Some parietal regions are sensitive to whether 21 Henson, R.N.A. et al. (2000) Confidence in recognition memory for retrieval is oriented in an attempt to recollect or to words: Dissociating right prefrontal roles in episodic retrieval. detect item novelty/familiarity, even when holding the J. Cogn. Neurosci. 12, 913–923 22 Cansino, S. et al. (2002) Brain activity underlying encoding and mnemonic history of the test materials constant. retrieval of source memory. Cereb. Cortex 12, 1048–1056 Taken collectively, these findings encourage consider- 23 Donaldson, D.I. et al. 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