Neurobiology of Learning and Memory

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1 Neurobiology of Learning and Memory 91 (2009) Contents lists available at ScienceDirect Neurobiology of Learning and Memory journal homeage: Some surrising findings on the involvement of the arietal lobe in human memory Ingrid R. Olson *, Marian Berryhill Deartment of Psychology, Temle University, 1701 N. 13th Street, Philadelhia, PA 19122, USA Center for Cognitive Neuroscience, University of Pennsylvania, USA article info abstract Article history: Received 9 July 2008 Revised 8 Setember 2008 Acceted 9 Setember 2008 Available online 31 October 2008 Keywords: Parietal lobe Balint s syndrome Short-term memory Working memory Eisodic memory Satial rocessing Retrieval Eisodic buffer Meta-memory The osterior arietal lobe is known to lay some role in a far-flung list of mental rocesses: linking vision to action (saccadic eye movements, reaching, grasing), attending to visual sace, numerical calculation, and mental rotation. Here, we review findings from humans and monkeys that illuminate an untraditional function of this region: memory. Our review draws on neuroimaging findings that have reeatedly identified arietal lobe activations associated with short-term or working memory and eisodic memory. We also discuss recent neurosychological findings showing that individuals with arietal lobe damage exhibit both working memory and long-term memory deficits. These deficits are not ubiquitous; they are only evident under certain retrieval demands. Our review elaborates on these findings and evaluates various theories about the mechanistic role of the osterior arietal lobe in memory. The available data oint towards the conclusion that the osterior arietal lobe lays an imortant role in memory retrieval irresective of elased time. However, the available data do not suort simle dichotomies such as recall versus recognition, working versus long-term memory. We conclude by formalizing several oen questions that are intended to encourage future research in this raidly develoing area of memory research. Ó 2008 Elsevier Inc. All rights reserved. 1. Introduction If you were to eruse any textbook on memory or neuroscience, you would be hard-ressed to find the terms memory and arietal lobe together. How then, do we exlain the large number of neuroimaging findings reorting arietal lobe activations to various mnemonic demands? The sheer volume of these findings raises the question of whether the arietal lobe lays a functional role in mnemonic rocessing that has been overlooked. To address this question, we review evidence linking the arietal lobe to memory. We focus on visual short-term or working memory (WM) and eisodic memory for the simle reason that there is now sufficient material in these literatures to rovide some nascent consensus. We note that links between verbal WM and arietal lobe function has recently been reviewed elsewhere (Buchsbaum & D Esosito, 2008). Our first iece of evidence that the arietal lobe may have some role in memory comes from white matter tractograhy revealing close anatomical linkages between the arietal lobe and frontal and medial temoral lobe areas. Subsequent sections describe exerimental evidence from visual WM, object WM and eisodic memory studies. We exlore various hyotheses describing the * Corresonding author. address: iolson@temle.edu (I.R. Olson). mechanism of arietal involvement in memory and conclude with a series of oen questions meriting further research. 2. Anatomy and connectivity of the osterior arietal cortex Because in vivo axon tracing techniques cannot be alied to humans, much of our knowledge of the connectivity of the arietal lobe is drawn from work in non-human rimates. This resents us with a significant intellectual hurdle, since the extent of inter-secies homology is unclear (Culham & Kanwisher, 2001; Glover, 2004), but see (Rushworth, Behrens, & Johansen-Berg, 2006). The human arietal lobe is nearly 20 times larger than that of the macaque. This ratio is markedly higher than the same comarison made between human and macaque temoral (9 times larger), or occiital (2 times larger) cortices (Van Essen et al., 2001). The size difference is artially exlained by the exansion of the human inferior arietal lobe. Indeed, there aears to be no equivalent of the human suramarginal gyrus (BA 39) in monkeys (Karnath, Ferber, & Himmelbach, 2001). Desite this roblem, there are some arietal regions that aear to share anatomical and functional similarities between macaques and humans (Culham & Valyear, 2006) and more recent non-invasive functional connectivity studies are beginning to rovide information about human arietal connectivity (Rushworth et al., 2006). Beginning anteriorly, the human arietal lobe is located immediately osterior to the central sulcus, where the somatosensory /$ - see front matter Ó 2008 Elsevier Inc. All rights reserved. doi: /j.nlm

2 156 I.R. Olson, M. Berryhill / Neurobiology of Learning and Memory 91 (2009) cortices (Brodmann areas (BA) 1, 2, and 3) occuy the ostcentral sulcus. More osterior regions, referred to herein as the osterior arietal cortex (PPC) are traditionally divided into the suerior arietal lobe (SPL; BA 5 and 7), the medial arietal lobe (mesial extent of BA 7), and the inferior arietal lobe (IPL; BA 39 and 40). 1 The SPL is osterior to somatosensory cortex and above the intraarietal sulcus (IPS), excluding medial arietal cortex. The medial arietal lobe consists rimarily of the recuneus, which is buried in the interhemisheric fissure. Recently some authors have defined the medial arietal cortex very inclusively, including the limbic osterior cingulate and retroslenial cortices in their definitions of this region (Vincent et al., 2006). Here, we hold to the more traditional definition of medial arietal cortex. The IPL is located below the horizontal ortion of the IPS, anterior to the suerior occiital lobe, and consists of the angular (BA 39) and the suramarginal gyri (BA 40) Inferior arietal lobe and medial temoral lobe connectivity In 1957, Scoville and Milner reorted that bilateral damage to the human medial temoral lobe causes chronic anterograde amnesia (Scoville & Milner, 1957). We now know that within the medial temoral lobe (MTL), the hiocamus lays a central role in satial and eisodic memory formation. Monkey tractograhy studies have identified two large axons tracts connecting the IPL to the medial temoral lobe. First, ortions of the inferior longitudinal fasciculus connect the angular gyrus with the arahiocamal gyrus (Seltzer & Pandya, 1984). Second, the cingulum bundle, which lies within the cingulate cortex, connects lateral and medial regions of the osterior IPL (PG and Ot 2 to the arahiocamal gyrus (Seltzer & Pandya, 1984). Connections also exist between entorhinal cortex and IPL area 7 in the monkey (Insausti & Amaral, 2008; Wellman & Rockland, 1997). Most interestingly, there are connections between area CA1 in the anterior ortion of the hiocamus and area 7a, in the osterior IPL of the monkey (also known as PG or Ot) (Clower, West, Lynch, & Strick, 2001; Rockland & Van Hoesen, 1999) and 7b, found in the anterior IPL (also known as area PF) of the monkey (Rockland & Van Hoesen, 1999). Information flow is redominantly directly from CA1 to 7a, suggesting that memory functions of the hiocamus modulate rocessing in area 7a (Clower et al., 2001) (see Fig. 1A). Connections have also been identified between the resubiculum and area 7a (Cavada & Goldman-Rakic, 1989; Ding, Van Hoesen, & Rockland, 2000.) Although these findings are redominantly based on investigations of monkey anatomy, there is some evidence that the human inferior arietal lobe has similar atterns of MTL connectivity. Rushworth and colleagues, using a diffusion weighted tractograhy method, reorted a attern of connectivity between a region of the arahiocamal gyrus just lateral to the hiocamus and the angular gyrus that resembled the inferior longitudinal fasciculus (see Fig. 1C). The angular gyrus in the IPL was the only lateral arietal region with a high robability of connection to the arahiocamus (Rushworth et al., 2006). In addition, resting state fluctuations in the BOLD signal show correlations between the hiocamus and medial lateral PPC (Vincent et al., 2006; see also Greicius & Menon, 2004; Takahashi, Ohki, & Kim, 2008). 1 An alternative anatomical nomenclature divides the osterior arietal lobe into dorsal and ventral regions. The dorsal arietal lobe corresonds to the lateral and medial arts of BA 7, the ventral arietal lobe corresonds to the inferior arietal lobe. 2 The anatomical terms PG, PF, Ot, 7a, and 7b are used rimarily by monkey researchers following von Economo s terminology (von Economo & Koskinas, 1925) Suerior and inferior arietal frontal connectivity Portions of the frontal lobe are known to lay a critical suorting role in mnemonic functions. In the monkey, several large fiber tracts connect both inferior and suerior arietal regions to the refrontal cortex. The dominant white matter tract connecting these regions is the suerior longitudinal fasciculus (SLF). The SLF can be divided into three subcomonents from the most suerior to the most inferior: SLF I, SLF II, SLF III (Makris et al., 2005; Schmahmann et al., 2007) (see Fig. 1B). The SLF I connects medial and dorsal ortions of the SPL (art of areas PE, PG, 31) to dorsal remotor and refrontal regions (BA 6 and 9, sulementary motor area) (Schmahmann & Pandya, 2006; Schmahmann et al., 2007) and is most likely imortant for higher order motor behavior (Petrides & Pandya, 2006). The SLF II unites the osterior IPL (area PO in the IPS, PG, Ot) with the mid- and dorsolateral refrontal cortices (BA 6, 8, 9, 46) (Schmahmann & Pandya, 2006; Schmahmann et al., 2007). The fronto-occiital fasciculus links a broad swath of medial (areas PO, PG medial) and osterior IPL regions (areas PG lateral, Ot, DP) with a band of regions in dorsolateral refrontal cortex (areas 6D, 8Ad, 8B, 9, 46d) (Schmahmann & Pandya, 2006). SLF III connects the anterior inferior arietal lobe (region PF/PO of the IPS) and the anterior intraarietal area within the IPS, with ventral remotor, ventral refrontal, and dorsolateral refrontal cortex (areas 6,44, 9/46) (Schmahmann & Pandya, 2006; Schmahmann et al., 2007). The function of these tracts is unknown, although it has been suggested that they are imortant for visual attention and working memory (Cavada & Goldman-Rakic, 1989; Schmahmann et al., 2007). Last, a searate axon tract, the cingulum bundle (temoral asects only) links osterior IPL (area PG, Ot) to the sulementary motor area and the dorsolateral refrontal cortex (Mori, 2005). The cingulum bundle is considered the dorsal limbic athway as it has branches that extend not only throughout the length of the cingulate, but also to the hiocamus and arahiocamus (Seltzer & Pandya, 1984). Thus, via the cingulum bundle, the osterior IPL is connected both to the dorsolateral refrontal cortex and to the hiocamus. 3. Working memory for satial attributes Over 50 years ago MacDonald Critchley remarked Bilateral disease of the brain, and esecially of the arieto-occiital regions, may be followed by the most consicuous satial disorders, esecially entailing visual disorientation. (Critchley, 1953,. 354). Of the many satial rocesses linked to arietal lobe function, satial WM is a more recent addition. This tye of memory allows one to remember satial information over short delay eriods where one looked a few moments ago, for instance. There are several sources of evidence linking the arietal lobe to satial working memory: neurohysiological, neurosychological, brain imaging, and transcranial magnetic stimulation (TMS). Memory cells are cells that dislay ersistent activity during the delay eriod of a WM task. The discharge of memory cells is higher during the delay eriod than during baseline eriods between trials. Such cells were first found in the dorsolateral refrontal cortex (PFC) of monkeys erforming satial WM tasks (Fuster & Alexander, 1970; Niki & Watanabe, 1976). Since their discovery, memory cells have also been found in other brain regions including the lateral intraarietal cortex in the PPC (Gnadt & Andersen, 1988; Mazzoni, Bracewell, Barash, & Andersen, 1996). PPC memory cells also exhibit delay activity during satial WM tasks (Constantinidis & Steinmetz, 1996; Fuster, 1990; Gnadt & Andersen, 1988, reviewed inconstantinidis, 2006; Constantinidis & Procyk, 2004; Constantinidis & Wang, 2004) that is comarable

3 I.R. Olson, M. Berryhill / Neurobiology of Learning and Memory 91 (2009) Fig. 1. Parietal medial temoral lobe connections. (A) Hiocamal area CA1 (black dots in left-most anel) rojects to area 7a (demarked with an oval in the right-most anel) in the lateral intraarietal area (LIP), as shown by retrograde viral tracing in the cebus monkey (Clower et al., 2001). The middle figures rovide anatomical orientation for monkey area 7a. (B) Parietal frontal lobe connections. The three branches of the macaque suerior longitudinal fasciculus (SLF I III) are shown from two ersectives: on the left, the lateral view and on the right the coronal view demonstrating the medial connections and the lateral connections (Schmahmann et al., 2007). (C) Human tractograhy. The left anel shows the results of a human diffusion weighted tractograhy study in which broad connections between inferior arietal regions and the whole of the arahiocamal gyrus (left anel), and connections between suerior arietal and frontal areas (right anel) were found (Rushworth et al., 2006). Figures taken with kind ermission from the ublishers. to delay activity observed in PFC neurons (Fuster, 1984). Selective cooling of areas 5 and 7 disruts satial memory (Quintana & Fuster, 1993). In accord with these findings, it has been known for several decades that damage to the right PPC in humans leads to imaired satial WM. Satial WM deficits subsequent to PPC damage are observed across a range of tasks and stimuli (see Table 1) such as old/new recognition of simultaneously or sequentially resented locations (Berryhill & Olson, 2008b; Husain et al., 2001; Malhotra et al., 2005; Pisella, Berberovic, & Mattingley, 2004), or recall, by ointing, to a series of locations (Baldo & Dronkers, 2006; De Renzi, Faglioni, & Previdi, 1977; De Renzi & Nichelli, 1975; Hanley, Young, & Pearson, 1991; Malhotra et al., 2005). It is imortant to bear in mind that IPL lesions, near the temoroarietal junction frequently result in hemisatial neglect (Vallar & Perani, 1986). Hemisatial neglect is a heterogeneous disorder (Shimozaki, Kingstone, Olk, Stowe, & Eckstein, 2006, reviewed in Buxbaum, 2006; Driver & Vuilleumier, 2001; Ellis, Della Sala, & Logie, 1996; Halligan, Fink, Marshall, & Vallar, 2003; Heilman, Jeong, & Finney, 2004; Heilman, Valenstein, & Watson, 2000; Hillis, 2006, Pisella & Mattingley, 2004) characterized by a failure to attend, react to, or to erceive stimuli resented in the contralesional visual field. Satial WM deficits are known to occur in atients with hemisatial neglect. For instance, several recent studies of neglect atients required subjects to remember sequentially resented locations arrayed in a vertical line. The results showed that neglect atients had imaired satial WM erformance (Malhotra, Mannan, Driver, & Husain, 2004; Malhotra et al., 2005; Parton et al., 2006). When the eye movements of neglect atients were assessed in visual search tasks, it was shown that they tend to revisit reviously foveated items as if they were new items, indicative of a satial WM imairment (Husain et al., 2001; Wojciulik, Husain, Clarke, & Driver, 2001). After neglect resolves (or even if it never existed), satial WM deficits remain resent (see Table 1), indicating that the satial WM deficits are not attributable to inattentiveness to ortions of sace. Converging evidence for the imortance of the right PPC in satial WM is offered by several TMS studies showing that transient inactivation of these regions imairs satial WM (Kessels, van Zandvoort, Postma, Kaelle, & de Haan, 2000; Koch et al., 2005; Oliveri et al., 2001). Neuroimaging studies have overwhelmingly corroborated these findings (D Esosito et al., 1998; Hartley & Seer, 2000; Smith &

4 158 I.R. Olson, M. Berryhill / Neurobiology of Learning and Memory 91 (2009) Table 1 Neurosychological studies of satial working memory as assessed by recall or recognition in atients with utative arietal lobe damage Authors Task Lesion sites Sared Imaired De Renzi and Nichelli (1975) Recall: Corsi L hemi, R hemi De Renzi et al. (1977) Recall: Corsi R hemi, R hemi with visual field defect Hanley et al. (1991) Recall: Corsi R hemi, (case study) Markowitsch et al. (1999) Recall: Corsi L angular gyrus, Case Della Sala, Gray, Baddeley, Allamano, and Recall: Pattern San, Corsi R hemi, L hemi, Bi hemi Wilson (1999) Kessels et al. (2000) Recall: Corsi R hemi, L hemi, Bi hemi, subcortical Postma, Sterken, de Vries, and de Haan Recall: Percetual Localization (2AFC) R hemi, L hemi (2000) Kessels, Jaa Kaelle, de Haan, and Recall: Object-Location Conjunction, L hemi, R hemi, Bi hemi, Anterior (frontal, *Corsi Postma (2002) Locations, Corsi, Maze learning temoral), Posterior (occiital, arietal) block *conjunction task Pisella et al. (2004) Old/new recognition R PPC + neglect, non-ppc + neglect Malhotra et al. (2005) Recall Old/new Recognition: Vertical Corsi R PPC + neglect; R PPC non-neglect van Asselen et al. (2006) Recall: Corsi R PFC, L PFC, R PPC, L PPC Nys, van Zandvoort, van der Wor, Recall: Corsi R hemi + neglect, L hemi + neglect, Bi Kaelle, and de Haan (2006) hemi + neglect, Baldo and Dronkers (2006) Recall: Corsi L inf PPC, L inf frontal Berryhill and Olson (2008b) Old/new recognition: locations R PPC Ferber and Danckert (2006) Old/new recognition: Vertical locations R PPC + neglect, R PPC Vuilleumier et al. (2007) Old/new recognition R PPC + neglect Husain et al. (2001) Visual search revisiting R PPC + neglect, R PPC Parton et al. (2006) Visual search revisiting R PPC + neglect, R PPC Mannan et al. (2005) Visual search revisiting R PPC (by lesion location) + neglect Note that in many studies recise cerebral localization was not rovided. Highlighted text in the lesion site column indicates which atient oulation, if any, was imaired. Abbreviations: Bi, bilateral; Corsi, Corsi block-taing task; hemi, hemishere; inf, inferior; L, left; R, right; PPC, osterior arietal cortex; PFC, refrontal cortex; 2AFC, twoalternative forced-choice. Jonides, 1997; Smith & Jonides, 1998; Ungerleider, Courtney, & Haxby, 1998). More recent event-related fmri findings suggest that the PPC is involved secifically in maintaining satial information, as shown by sustained delay-eriod activity (reviewed in Curtis, 2006; Linden, 2007) and ossibly in WM maniulation (Postle et al., 2006). The PPC aears to work in concert with the PFC to solve the comutations necessary for accurate satial WM. The firing atterns of these regions is intrinsically linked: when cell oulations in the dorsolateral PFC and lateral PPC cells were simultaneously recorded during a delayed saccade task, the neural activity atterns were shown to match (Chafee & Goldman-Rakic, 1998; Quintana & Fuster, 1999). Selective lesions to these regions in the macaque leads to a similar disrution in saccadic memory saccades become less accurate as the delay eriod lengthens (reviewed in Curtis, 2006). Similarly, cortical cooling of either region while recording single-units in the other region showed that these regions have a strong interdeendency during satial WM tasks (Chafee & Goldman-Rakic, 2000). Similarly, TMS to either the PPC or dorsolateral PFC during satial WM maintenance slows reaction times (Koch et al., 2005; Oliveri et al., 2001). Both regions are robustly activated during satial WM tasks (Jonides et al., 1993; Smith & Jonides, 1998; reviewed in D Esosito, 2007; Naghavi & Nyberg, 2005; Passingham & Sakai, 2004; Ungerleider et al., 1998; Wager & Smith, 2003). In site of these similarities, there are differences between the neural rofiles associated with the PPC and the PFC. The mnemonic activity of PPC neurons, secifically neurons in area 7a, aears to be closely aligned with bottom-u attentional activity as PPC neurons fire to any salient stimuli, even when the it is behaviorally irrelevant and PPC neurons begin firing before PFC neurons under bottom-u attentional conditions, suggesting that this region detects and registers the satial location of visually resented stimuli (Constantinidis & Steinmetz, 2005; reviewed in Constantinidis, 2006). In contrast, the mnemonic activity of lateral PFC and frontal eye field neurons may be more closely aligned with to-down attention as frontal neurons begin to fire before lateral intraarietal neurons under to-down attentional conditions (Buschman & Miller, 2007). 4. Working memory for objects or object features In contrast to the strong converging evidence linking the PPC to satial WM functions, the evidence for functional links between the PPC and object WM is weaker. Neurons in macaque lateral intraarietal sulcus are resonsive to object shae during the remember eriods of delayed-match-to-samle tasks. Neuronal selectivity can be indeendent of eye movements, reaching, or object maniulation or in other words, indeendent from satial rocessing (Sereno & Amador, 2006; Sereno & Maunsell, 1998). Also, lateral intraarietal neurons exhibit delay activity to target color when it is behaviorally relevant (Toth and Assad, 2002). In humans, BOLD activity in the IPS has been shown to titrate with the number of shaes and colors that can be held in memory over brief amount of time, suggesting that this region has some role in governing WM caacity (Macoveanu, Klingberg, & Tegner, 2006; Todd & Marois, 2004; Todd & Marois, 2005; Xu & Chun, 2006). This activity is not due to the number of items viewed at encoding, but rather to the number of items accurately maintained in WM, lending suort to the idea that the function of the IPS is mnemonic, not ercetual (Todd & Marois, 2004). Converging evidence for these findings can be found in a small number of neurosychological studies. We required subjects with or without right PPC damage to remember four sequentially resented colors, abstract shaes, or common objects over a short delay eriod and then make an old/new recognition decision. A sequential task in which all information was resented at central fixation was used to minimize satial demands. The results showed that right PPC damage was associated with diminished WM erformance across stimulus categories (Berryhill & Olson, 2008b); for face WM imairments see (Warrington & James, 1967). A subsequent study tested atients with bilateral arietal lobe damage on exactly the same

5 I.R. Olson, M. Berryhill / Neurobiology of Learning and Memory 91 (2009) task. A similar attern of deficits was observed (Berryhill & Olson, 2008a). Unfortunately, the results of other studies cast some doubt on the robustness of these findings. Several atients with right PPC damage and neglect were tested on an object WM task and no deficits were observed (Pisella et al., 2004). Another study found that right PPC atients were imaired on object delay-match-to-samle tasks only when the robed dimension (object or satial) was unredictable (Finke, Bublak, & Zihl, 2006), hinting that the right PPC s role in WM may be attentional rather than mnemonic. One of the only TMS studies relevant to this question administered single TMS ulses during the maintenance eriod of an object WM task, but found no effect of unilateral or bilateral PPC stimulation on erformance (Oliveri et al., 2001). As a whole, the evidence suggests that object WM relies to some degree on an intact arietal lobe although several unanswered questions remain (see Box 1, question 1). The fact that there are discreant findings is troubling, and the reason for this remains elusive, although we have observed that the manner in which memory is robed leads to different atterns of erformance after arietal lobe damage. This finding hints that retrieval rocesses may be key to understanding the functionality of the PPC (Berryhill & Olson, 2008a; Berryhill, Phuong, Picasso, Cabeza, & Olson, 2007; Drowos, Berryhill, & Olson, acceted for ublication). We exand on this toic in the next section. 5. Mechanistic role of the arietal lobe in working memory The mechanistic role of the arietal lobe in WM is currently unknown. The neuroimaging literature has focused on WM maintenance and two hyothetical roles of the PPC in WM that have emerged are in the maniulation of information during WM maintenance (Chamod & Petrides, 2007; Wendelken, Bunge, & Carter, 2008), and in total information accumulation during WM maintenance (Xu, 2007). In contrast, the neurosychological literature has offered the hyothesis that the PPC s role in WM is in instantiating articular retrieval rocesses (Berryhill & Olson, 2008a) Information maniulation hyothesis Several investigators have roosed that the mnemonic function of the PPC is secifically associated with the maniulation of information held in WM (Chamod & Petrides, 2007; Wendelken et al., 2008). For instance, in one recent study subjects were required to remember letters and colors under several different conditions. In the low and high memory load conditions, the task was to remember the alhanumeric items in the memory set and resond whether two robe items had been resent in the receding memory set. In the organization condition, the task was to remember whether the robe items had been reviously shown in the same color. In their second exeriment, the organization task was to satially reorganize the items according to arrows. In both studies, the authors observed frontal activity (DLPFC, VLPFC) during the delay eriod associated with WM load. However, suerior arietal activity (BA 7) was only observed when WM maintenance required maniulation (Wendelken et al., 2008). Similar SPL regions are activated during other tasks demanding item reorganization in WM such as order sequencing tasks (Marshuetz & Smith, 2006; Marshuetz, Smith, Jonides, DeGutis, & Chenevert, 2000; Wager & Smith, 2003), and mathematical calculation tasks (Dehaene, Molko, Cohen, & Wilson, 2004; Dehaene, Selke, Pinel, Stanescu, & Tsivkin, 1999). One roblem with this interretation is it does not account for the large number of WM studies in which the task does not include a maniulation requirement, yet SPL activations are observed. Also, the maniulation hyothesis falls rey to the difficulty exlanation, that greater PPC activations in the maniulation condition are simly due to the greater difficulty of that task comared to the baseline condition Information load hyothesis Behavioral studies have shown that on average, most eole can maintain aroximately four objects in visual WM (Luck & Vogel, 1997) and that memory caacity varies with the comlexity (Alvarez & Cavanagh, 2004), or with the similarity of these items (Awh, Barton, & Vogel, 2007; Olson & Jiang, 2002). Interestingly, ortions of the arietal lobe aear to be sensitive to memory caacity limitations. In one study, subjects observed an array of colored squares and after a brief delay, were shown a robe image and made a same/different judgment. In a whole brain analysis, only one region titrated with memory caacity: the suerior IPS. Note that suerior IPS activity was not modulated by set size but rather, the number of objects that subjects could accurately maintain in memory such that neural activity leveled off as memory caacity reached asymtote. Additional analyses revealed that activity correlated with individual erformance on the object WM task (Todd & Marois,2004, 2005). This finding and those of others (Xu & Chun, 2006) suggest that one role of the suerior IPS in WM is to maintain a finite number of objects over short delay eriods. An alternative exlanation is that the suerior IPS maintains visual features, rather than discrete objects, over a short eriod of time. Note that the number of objects and visual features are highly correlated in most studies using visual stimuli. To understand their individual contributions, Xu (2007) dissociated feature and object information. In her study, subjects were required to remember stimulus arrays with the same number of objects (all black shaes) but different numbers of features (variably colored shaes). In a searate task, the number of objects was varied, but the number of features remained constant. The results showed that the suerior IPS exhibited greater changes in signal strength when there were more visual features resent. However, there was no difference in the suerior IPS when the number of objects was varied, holding the number of features constant (Xu & Chun, 2006; see also Xu, 2007). This finding rovides evidence for the view that the suerior IPS reresents the sum total of ercetual information stored in WM. These findings redict that suerior IPS damage will diminish visual WM caacity, as a function of the number of visual features of the items. We tested this rediction in two studies by requiring atients with unilateral or bilateral arietal lobe damage to remember visual stimuli that varied in the number of features: color atches, novel shaes, and common objects. The first art of the rediction was suorted: visual WM caacity was diminished after PPC damage. However, the second art of the rediction was not borne out in these data: there was no effect of stimulus comlexity or number of features on atient erformance (Berryhill & Olson, 2008a, 2008b), suggesting that visual feature load does not fully exlain the mechanistic function of the PPC in WM Retrieval rocess hyothesis In a series of WM studies, we examined the role of the PPC in WM while maniulating the retrieval rocess. The erformance of two atients with bilateral arietal damage was comared to that of matched controls (Berryhill & Olson, 2008a). In the first air of exeriments, order WM was tested with either recall or recognition retrieval robes. Subjects observed four

6 160 I.R. Olson, M. Berryhill / Neurobiology of Learning and Memory 91 (2009) sequentially resented items (colors, shaes, or objects) and after a brief delay, the same items were reeated. The recognition task was to make a same/different judgment regarding the order of the four items. In the recall version, a single robe item aeared after the delay and the task was to rovide the ordinal osition (1 4) of that image. The atients exhibited imaired WM erformance when robed by old/new recognition, but intact WM erformance when robed by recall. In a second air of studies, the task was to remember the identity of four common objects over a brief delay, and then to make either an old/new judgment or to verbally name the objects that had been shown. The same attern of reserved recall accomanied by imaired recognition was observed (see Fig. 2). These findings cannot be attributed to deficient encoding or maintenance rocesses because these demands were held constant; only the retrieval rocess varied. This finding leads us to suggest that the PPC s role in WM is secifically linked to retrieval rocesses. If true, this function coincides with a wealth of findings on retrieval in the eisodic memory literature, discussed next. 6. Eisodic memory Findings linking eisodic memory to the arietal lobe have recently aroused considerable attention from the cognitive neuroscience community. Several excellent reviews of this toic are available and we direct interested readers to these sources (Cabeza, 2008; Cabeza, Ciaramelli, Olson, & Moscovitch, 2008; Simons & Mayes, 2008), see also Uncaher & Wagner, this volume; Vilberg & Rugg, 2008; Wagner, Shannon, Kahn, & Buckner, 2005). To summarize: arietal activity is greater when an old stimulus is correctly identified as old, comared to when a new item is correctly identified as new. The benefit afforded stimuli retrieved as old is extended to items that were incorrectly erceived as old (Kahn, Davachi, & Wagner, 2004; Wheeler & Buckner, 2003). Searable regions in the lateral arietal lobe, a suerior and an inferior region, show comlementary atterns of activity; the suerior area aears to reflect to-down influence in mediating low-confidence resonses and the inferior region reflects bottom-u influence mediating high-confidence resonses (Kim & Cabeza, 2007). Until recently, these findings were viewed with sketicism because they suffered from an absence of converging evidence from other techniques. A key iece of converging evidence was recently rovided by a study of atients with bilateral arietal lobe lesions (lesions are shown in Fig. 2A). In this study, atients and matched controls were asked to recollect various autobiograhical memories. In condition 1, they freely recalled events from their lifetime in as much detail as ossible. In condition 2, they answered secific questions about these memories. The results showed that arietal lobe damage decreased the vividness and amount of detail freely recalled. However, when atients were robed for secific details ertaining to their memories, they erformed normally (Berryhill et al., 2007; see also Hunkin et al., 1995). We recently tested the same atients on the Deese McDermott Roediger (DRM) false memory aradigm and found that they exhibited normal false memory when tested by recall and imaired levels when tested by old/new recognition (see Fig. 2). Interestingly, they also exhibited an abnormally low level of remember resonses comared to know resonse (Drowos et al., acceted for ublication) (see Fig. 2). 7. Mechanistic role of the arietal lobe in eisodic memory A large number of fmri studies have reorted that ortions of the PPC are modulated as a function of eisodic memory retrieval demands. We do not discuss these findings in detail as they have been thoroughly reviewed elsewhere (Cabeza, 2008; Naghavi & Nyberg, 2005; Wagner et al., 2005). Suffice it to say that these findings come from a number of different laboratories using different tasks and stimuli, making a comelling case for PPC involvement in eisodic memory retrieval. Discerning what exactly that role might be is the subject of much current investigation. Suggested roles include serving as an eisodic buffer, a tye of WM (Baddeley, 2000; Vilberg, Moosavi, & Rugg, 2006; Vilberg & Rugg, 2008), roviding an assessment of memory signal strength, as a mnemonic accumulator (Wagner et al., 2005), in directing internal attention (Cabeza, 2008; Cabeza et al., 2008; Ciaramelli, Grady, & Moscovitch, 2008), or as a gauge of memory subjectivity or confidence (Ally, Simons, Fig. 2. Parietal lesions and working memory, eisodic memory erformance. (A) Working memory and eisodic memory was investigated in two atients with bilateral arietal lobe lesions. MRI images show the lesions outlined in red. (B) Three exeriments sanning short and long-term forms of memory robed memory with two different resonse tasks. In order and object WM (left), recall (Rec) erformance was reserved whereas recognition (Recog) erformance was imaired (Berryhill & Olson, 2008a). In a long-term memory (LTM) task, erformance was assessed with the DRM aradigm, and the same attern of reserved recall and imaired recognition erformance was observed (Drowos et al., 2008, acceted ending revisions). Data are shown as standardized scores in which erformance greater than 1.96 standard deviations is considered imaired.

7 I.R. Olson, M. Berryhill / Neurobiology of Learning and Memory 91 (2009) Fig. 3. The attention to memory (A to M) model rooses two loci of arietal involvement in memory retrieval that ma onto two forms of attentional demands (Cabeza et al., 2008). To-down attention is controlled and sustained by neurons in the suerior or dorsal arietal cortex (DPC). The DPC directs attention towards a retrieval goal, in this case, the memory of a 1st birthday arty. In contrast, bottom-u attention can be catured by environmental stimuli or by sensory cues, such as the image of the birthday cake. In this case, the medial temoral lobes (MTL) cause the inferior or ventral arietal cortex (VPC) to signal the DPC to attend to the sontaneously retrieved memory. The waveforms reflect the variability in retrieval demands. McKeever, Peers, & Budson, 2008; Simons, Peers, Mazuz, Berryhill, & Olson, submitted for ublication). Our eisodic memory findings, reviewed earlier, also oint towards memory retrieval rocesses being disruted after PPC damage in that eisodic memory is imaired under some, but not other, retrieval conditions (Berryhill et al., 2007; Drowos et al., acceted for ublication). Preserved memory on several eisodic memory tasks, in studies conducted by ourselves and others (Davidson et al., 2008; Simons et al., 2008a; Simons et al., submitted for ublication) indicate that memory retrieval er se is not diminished by arietal lobe damage, but rather a articular subrocess that is taed in some tasks but not others. One roosed hyothesis that aears to offer a hay marriage between the WM findings reviewed earlier, and eisodic memory findings is that ortions of the PPC serve as the interface between WM and eisodic memory retrieval as the eisodic buffer (Baddeley, 2000). According to this hyothesis, the retrieval of greater amounts of integrated multi-modal information causes subjects to have confidence in their retrieval judgments and increases the maintenance demands on the eisodic buffer. This hyothesis can exlain many of the findings in the visual WM literature, such as increased BOLD activations with recollected rather than familiar memories (Daselaar, Fleck, & Cabeza, 2006; Wheeler & Buckner, 2004; Yonelinas, Otten, Shaw, & Rugg, 2005; reviewed in Skinner & Fernandes, 2007), and decreased WM caacity after PPC damage (Berryhill & Olson, 2008a, 2008b). However, it fails to exlain why PPC damage leads to different levels of memory erformance deending on the robe task (Cabeza et al., 2008). A second roosal suggests that ortions of the PPC assess the strength of a memory signal in order to determine whether a stimulus was reviously viewed. This mnemonic accumulator hyothesis (Wagner et al., 2005) can be easily understood as an analogy to signal detection theory in which evidence is accrued and some criterion level is set. This view is unable to exlain why different memory tasks roduce different resonse atterns in the arietal cortex, as some sort of signal estimate should be resistant to the tye of information retrieved (reviewed in Cabeza, 2008). A third ossibility is that the PPC s role in memory retrieval arallels its role in attention (Cabeza, 2008; Cabeza et al., 2008; Wagner et al., 2005). To understand how this may work it is imortant to understand that attention and memory are tightly intertwined at nearly every stage of mnemonic rocessing (reviewed in Awh, Vogel, & Oh, 2006; Chun & Turk-Browne, 2007; Naghavi & Nyberg, 2005). They are linked at encoding because to-down attention to any given item imroves the ercetion of features, such as contrast (Carrasco, Ling, & Read, 2004). Selective attention acts as a gatekeeer, filtering which asects of the environment are encoded into memory, and which items are not. Attention and memory are also intertwined during memory maintenance as demonstrated by the fact that distraction during delay eriods disruts memory erformance. Last, attention may be needed for accurate retrieval because divided attention tasks can cause interference and failures of retrieval even for items that were encoded with full attention (Fernandes & Moscovitch, 2000). As originally conceived, the attention to internal reresentation hyothesis suggested that the arietal lobe focused attention on items held in memory (Wagner et al., 2005). This hyothesis has been exanded from a urely goal driven, or to-down, attentional modulation to include sontaneous, or bottom-u, attentional modulation, which mas onto dorsal and ventral arietal regions (Cabeza, 2008). The most recent version of this exanded view, the attention to memory model (AtoM) suggests that memory goals can be allocated deliberately (to-down) or can be catured by a memory cue (bottom-u) (see Fig. 3). Exlicit directions rovide a goal to guide internal memory retrieval towards a articular memory. This rocess is sustained by a region in the BA 7 of the suerior arietal lobe. In contrast, a memory may be sontaneously evoked by an environmental stimulus in a bottom-u fashion. When this haens, the MTL connections with inferior arietal lobe regions cause the suerior arietal region to redirect attention to the bottom-u driven recollection. This hyothesis can exlain much of the eisodic memory literature, including our findings in which bottom-u, sontaneous retrieval of autobiograhical memories was imaired in atients with bilateral ventral arietal damage, but to-down, cued retrieval was normal (Berryhill et al., 2007). One neurosychological finding fails to suort this model; however, we found that diminishing to-down attention cues to the critical feature that was later tested in an auditory source memory task had little effect on the source memory erformance of atients

8 162 I.R. Olson, M. Berryhill / Neurobiology of Learning and Memory 91 (2009) with bilateral PPC damage (Simons et al., submitted for ublication). The last hyothesis we discuss, the subjective memory hyothesis rooses that the arietal lobe is resonsible for the subjective exerience of confidence and vividness in one s retrieved memories (Ally et al., 2008). This hyothesis finds suort in a small number of neuroimaging findings (Chua, Schacter, Rand-Giovannetti, & Serling, 2006; Durate, Henson, & Graham, 2008), in statements made by arietal atients that they had diminished vividness and confidence in their memory abilities (Ally et al., 2008; Davidson et al., 2008), and in neurosychological findings showing decreased levels of memory confidence (Davidson et al., 2008; Drowos et al., acceted for ublication; Simons et al., submitted for ublication), and memory vividness (Berryhill et al., 2007). Interesting, several years ago Hunkin and colleagues reorted on a atient, DH, who had arieto-occiital damage due to a closed head injury. This atient had semantic memories for his lifetime but he felt that he lacked genuine memories of this life. He claimed that he did not feel that he had truly exerienced these memories: He said it was as if he had read a book about his life but he did not confuse these facts with real memories any more than one would confuse a story in a book with real life (Hunkin et al., 1995). Again, this finding suorts the contention that the arietal lobe may have a secial role in eliciting or interreting subjective memory states. These reorts are reminiscent of findings in the hemisatial neglect literature indicating that ortions of the arietal lobe (right inferior) lay a role in subjective states of awareness. Perhas it is the case that the inferior arietal lobe lays an analogous role in awareness, and hence confidence, of memories. 8. Conclusions The functionality of the PPC, like that of the frontal lobe, cannot be characterized as simly sensory, motor, or cognitive. Parietal functions that were identified generations ago in lesion studies satial attention, visual guidance of action (eye movements, grasing), calculation, reading do not aear to have an underlying categorical structure that rovides for easy analysis. Comlicating the situation, in this aer we suggest that an additional function should be added to this list: memory retrieval. Our review indicates that (1) the PPC lays a critical role in satial working memory. (2) The PPC may also have a role in object WM, although this role remains less substantiated. (3) The PPC s role in WM may be most strongly linked to memory retrieval (Berryhill & Olson, 2008a). (4) The PPC lays an imortant role in eisodic memory retrieval, although encoding functions may also exist (see Uncaher & Wagner, this volume). Links between the osterior arietal lobe and memory retrieval were first noted in fmri studies of eisodic memory. More recently, lesion studies indicate that PPC damage can cause selective retrieval difficulties in the context of eisodic retrieval tasks. (5) Many mechanistic accounts of the PPC s role in eisodic memory have been roosed. Two accounts that find agreement with much of the existing data are the attention to memory (AtoM) hyothesis (Cabeza et al., 2008) and the subjective memory hyothesis (Ally et al., 2008). The goal of this review is in art to raise interest in these remaining questions and to rovoke researchers to develo clearly testable hyotheses (see Box 1). The rosect of answering these questions is certain to drive the field of memory research in the years to come. Box 1 Question for future research [1] Given that a hallmark of arietal functioning is satial selectivity, is object WM truly indeendent from satial rocessing functions of the PPC? According to one view, whenever we encode objects, we automatically encode and maintain stimulus location, even when location is task irrelevant (Jiang, Olson, & Chun, 2000). In suort of this finding, macaque research indicates that PPC coding is largely retinotoic even in object WM tasks and that IPS neurons are more sensitive to remembered locations than remembered objects (Sabes, Breznen, & Andersen, 2002). The object attributes to which IPS neurons are most sensitive shae and size are inherently satial in nature. However, the inter-secies generalizability of these findings is oorly understood. [2] Are the arietal mechanisms for attention and memory encoding one and the same? According to one view, PPC activations during WM tasks simly reresent attention to objects (Cowan, 2001; Majerus et al., 2007). In suort of this view, a recent fmri study robed set-size effects during an object WM task and two control tasks of ercetual attention, finding similar IPS activity and limitations during all tasks (Mitchell & Cusack, 2008). Because the attention task had no WM requirements, the authors suggest that the activity reflects the rocessing of attended items. [3] Can different mnemonic rocesses be linked to different arietal lobe regions? Eisodic memory retrieval has been associated with IPL activations, while visual working memory maintenance has been associated with IPS activations. Exected laterality differences left PPC for verbal material, right PPC for visual material have seldom been reorted in fmri studies, although they are commonly reorted in neurosychological studies. [4] Our neurosychological findings showed a dissociation between WM recall and recognition such that arietal lobe damage only adversely affected recognition. A similar dissociation has not been reorted in long-term memory tasks and indeed, several studies have reorted normal levels of recognition memory after arietal lobe damage (Davidson et al., 2008; Simons et al., 2008a, submitted for ublication). Are recall and recognition differentially reliant on the arietal lobe at different time scales? Acknowledgments We thank Roberto Cabeza for helful discussions. We also thank Alexandra Giardino. This research was suorted by RO1 MH to I. Olson and Ruth Kirschstein NRSA F32 NS to M. Berryhill. References Ally, B. A., Simons, J. S., McKeever, J. D., Peers, P. V., & Budson, A. E. (2008). Parietal contributions to recollection: Electrohysiological evidence from aging and atients with arietal lesions. Neurosychologia, 46, Alvarez, G. A., & Cavanagh, P. (2004). The caacity of visual short-term memory is set by visual information load and by number of objects. Psychological Science, 15, Awh, E., Barton, B., & Vogel, E. K. (2007). 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