Overlapping Parietal Activity in Memory and Perception: Evidence for the Attention to Memory Model

“The MTL ROI was derived using the left hippocampus label of the AAL atlas (Tzourio-Mazoyer et al., 2002) in the WFU Pickatlas tool, whereas the visual cortex ROI was created by selecting left BA 17 from Pickatlasʼs Brodmannʼs area labels and dilating the volume by four voxels in three dimensions.”

“Although DPC and VPC have been associated, respectively, with top–down and bottom–up attention in both perception (Corbetta & Shulman, 2002) and memory tasks (Cabeza et al., 2008; Ciaramelli et al., 2008), a recent fMRI meta-analysis suggested that the exact locations of top–down and bottom–up…”

“The pairs were selected from free association norms (Nelson, McEvoy, & Schreiber, 2004 ) so that groups of three pairs formed four-word “chains” (eg, dog–cat–tiger–stripe; penguin–tuxedo–prom–date; malt–shake–rattle–snake).”

“Although the current study was not designed to compare different hypotheses regarding parietal contributions to episodic retrieval (for a review, see Wagner et al., 2005), the results are more consistent with the AtoM model than with alternative accounts.”

“In the memory domain, conditions involving demanding memory search or monitoring processes tend to show greater DPC activity, whereas conditions involving rich, attentiongrabbing memories tend to show greater VPC activity (Cabeza et al., 2008).”

“Several hypotheses have been advanced to account for the contributions of posterior parietal regions to episodic retrieval (for reviews, see Cabeza, Ciaramelli, Olson, &Moscovitch, 2008; Ciaramelli, Grady, & Moscovitch, 2008; Vilberg & Rugg, 2008; Wagner, Shannon, Kahn, & Buckner, 2005).”

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“One hypothesis is that memory retrieval involves attentional reorienting to spontaneously evoked memories, in a manner analogous to visuospatial reorienting (Cabeza et al., 2012a, 2008, 2011; Ciaramelli et al., 2008).”

“In doing so, this multi-domain meta-analysis was able to preserve the selection criteria and other parameters that are considered highly relevant to researchers working in each subject area (a full description of the method used to define each domain is provided in Supplementary Material) (Cabeza et al. 2008; Ciaramel…”

“…resources to memory retrieval based on current goals), whereas the VPC activity reveals the capture of bottom-up attention by the target (attention captured by the bottom-up information that enters a working memory either from the senses or from long-term memory) [Cabeza et al., 2008, 2011].”

“Alternatively, pMTG and/or AG might contribute to specific conceptual retrieval processes as opposed to aspects of representation (Cabeza et al., 2011; Humphreys and Lambon Ralph, 2014).”

“This pattern of responding in the angular gyrus is consistent with the purported role of inferior parietal cortex in focusing attention on memory (Cabeza et al., 2011).”

“Neuroimaging studies have also shown that these tasks activate similar brain regions (Cabeza et al., 2011; Hutchinson et al., 2009).”

“Cabeza et al. (2011) suggested that the overlapping activation in perception and memory for this network suggests an attention-to-memory account, as in the present account.”

“…regions, performs top-down attentional control of episodic retrieval, biasing medial temporal lobe activity, in a manner similar to the attentional control of sensory perceptual regions (Cabeza, 2008). fMRI studies support this idea of parietal involvement in memory retrieval (Cabeza et al., 2011).”

“The bottom-up attention account, which is a component of the Attention-to-Memory model (AtoM) (Cabeza, 2008; Cabeza, Ciaramelli, Olson, & Moscovitch, 2008; Ciaramelli, Grady, Levine, Ween, & Moscovitch, 2010; Ciaramelli, Grady, & Moscovitch, 2008) has previously been used to explain the E/R-flip in ventral parietal co…”

“Subsequent analyses have shown greater connectivity between the supramarginal gyrus and occipital areas when a salient perceptual stimulus is detected, but greater connectivity with the MTL when a salient memory is detected (Cabeza et al., 2011).”

“Connectivity analyses have demonstrated that IPs and TPJ show increased connectivity with the medial temporal lobe (MTL) during episodic retrieval as opposed to visuospatial attentional orienting (Burianová et al., 2012; Cabeza et al., 2011).”

“According to the attention to memory model (Cabeza et al., 2011; Cabeza, Ciaramelli, Olson, & Moscovitch, 2008; Ciaramelli et al., 2008), when a memory is recovered, attention is redirected toward the newly retrieved memory by the ventral parietal cortex, which acts as an attentional circuit breaker.”

“parietal cortex mediates automatic bottom-up attention processes captured by retrieved memory output (detection) (Ciaramelli et al., 2008; Cabeza et al., 2011).”

“One of these is the intraparietal sulcus, an area that is thought to play a role in top-down attention to episodic memory targets (Simons, Peers, Mazuz, Berryhill, & Olson, 2010) or confidence in episodic memory retrieval (Cabeza et al., 2011).”

“…that aligns attention externally to relevant sensory stimulation (Connor, Egeth, & Yantis, 2004; Corbetta & Shulman, 2002; Posner & Rothbart, 2007) or internally to explicit memory (Binder & Desai, 2011; Buckner et al., 2008), as described in the attention to memory model (Cabeza et al., 2011).”

“Suggestions regarding the contribution of parietal areas to memory include attentional functions (e.g. Cabeza, 2008; Cabeza et al., 2011; Ciaramelli et al., 2010,, 2008), expectation and salience (Buchsbaum et al., 2011; Jaeger et al., 2013; O'Connor et al., 2010), retrieval buffering (e.g.,…”

“Several researchers (e.g., Cabeza et al., 2011; Ciaramelli, Grady, & Moscovitch, 2008; Ciaramelli, et al., 2010; Hutchinson, Uncapher, & Wagner, 2009; Jaeger, Konkel, & Dobbins, 2013; Vilberg & Rugg, 2008) have demonstrated that the dorsal and ventral regions of the PPC exhibit differential…”

“…of processes, an ability of multivoxel pattern analysis to discriminate different tasks within regions of overlap, and distinct connectivity patterns of activation foci (Hutchinson et al., 2009; Scholz et al., 2009; Cabeza et al., 2011, 2012; Daselaar et al., 2013; Lee and McCarthy, 2016).”

“performed (Cabeza et al. 2011; Cabeza et al. 2012; Geng andVossel 2013).”

“…connection that we found between the DPC and left hippocampus during cued recognition memory supports the hypothesis that the left DPC initiates a search for the original associate of cuewords, biasing activity in the hippocampus in accordance with retrieval goals (see also Cabeza et al., 2011).”

“The identification of distinct pathways in the parietal cortex for top–down attentional processes (e.g., goal-directed attention) and lower-level sensory input was initially founded in the visual modality (Cabeza et al., 2011; Ciaramelli et al., 2010).”

“In the context of our discussion, this emphasizes the importance of understanding not only the role of each brain region in retrieval, but also how different regions interact to support distinct mnemonic functions, including retrieval (Simons and Spiers 2003; Mendelsohn et al. 2010; Cabeza et al. 2011; Huijbers et al.…”

“On the other hand, some overlap between visual attention and episodic memory can be observed within the parietal cortex (Cabeza et al., 2011).”

“Among theories of PPC function, the " attention to memory " (AtoM) account (Cabeza et al. 2008, 2011; Ciaramelli et al. 2008) explains retrieval-related activation within parietal cortex as a result of dissociable attention-based functions within dorsal and ventral parietal cortex.”

“…in parietal mnemonic activations, which Kim (2012) labels the cognitive Frontiers in Integrative Neuroscience www.frontiersin.org July 2012 | Volume 6 | Article 41 | 7 control network, intuitively brings to mind the AtoM hypothesis (Cabeza et al., 2008, 2011; Ciaramelli et al., 2008, 2010).”

“of violated expectations by retrieving episodic memory details from expected perceptual schemas [11; 12; 25; 41; 53].”

“According to the attention to memory model hypothesis, very similar attention mechanisms are involved in memory tasks, on the one hand, and sensory processing tasks, on the other (Cabeza et al., 2011).”

“This differential pattern between a search-efficiency-related working memory demand along the IPS and a retrieval-related activation in the TPJ region fits well with a distinction that has been proposed by Cabeza et al. (2011) for the parietal involvement in explicit memory.”

“However, in a study that attempted to directly assess the amount of overlap between attentional re-orienting and successful retrieval (Cabeza et al., 2011), the two classes of effect were found to partially overlap.”

“…is involved in voluntary, goal-directed attention, whereas the ventral parietal cortex, which is usually involved in bottom-up attention, appears to be associated with involuntary recollection (see Hutchinson et al., 2009, for some counter-evidence, but also Cabeza et al., 2011, for a response).”

“The dorsal PPC regions shows activation in association with verbal episodic memory tasks requiring participants to orient to internally retrieved memories (Cabeza et al., 2011).”

“The location of this peak of activation is congruent with previous fMRI findings, showing that dorsal parietal activations during memory tasks tend to be in the lower part of this region, that is, the lateral bank of the IPS (Cabeza et al., 2011; Hutchinson et al., 2009).”

“However, a study that compared attention-reorienting and recollection directly within-participants found overlapping activations with some differences in distribution (Cabeza et al., 2011).”

“These findings are in line with the attention-to-memory model, which proposes that the dorsal/ventral system distinction present in external attention also applies for attending to internal (mnemonic) representations (Cabeza et al., 2011; Ciaramelli et al., 2008; see also Asplund et al., 2010).”

“A similar approach has been taken in recent work, demonstrating shared engagement of neural circuits across both visual search and memory search tasks (Cabeza et al., 2011) as well as recognition and cued recall tasks (Hayama et al.”

“Activation studies have shown that the parietal lobe is one of the most frequently activated areas also during episodic memory retrieval [42], and that dorsal and ventral parietal cortex have distinct functions within episodic memory, as well as overlapping activity for memory and perception [43, 44].”

“For example, in a cued recognition experiment, DPC was active when participants anticipated a target based on a memory cue, whereas VPC mediated fast detection of memory targets in the absence of cues (Ciaramelli et al., 2010a; see also Cabeza et al., 2011).”

“It is therefore assumed that perception and memory require similar attentional control processes (Cabeza et al., 2011).”

“, 2012) and LM (Cabeza et al., 2011; Ciaramelli et al., 2010; Polyn et al., 2005), different regions are activated at different retrieval stages.”

“To investigate this assumption, Cabeza et al. (2011) had participants search for and detect a memory target (i.e., the last word of a previously encoded word quartet: e.g., dog – cat – tiger – stripe) or a visual target (i.e., a vowel in a stream of consonants).”

“However, evidence for such MTL-parietal functional coupling during memory decision-making is scarce (Cabeza et al., 2011; Geib et al., 2017; Kuhl et al., 2013).”

“Glucose metabolism between seizures was measured, with reductions relative to non-déjà vu-experiencing patients observed in the MTL, but also in the parietal cortex, a region implicated in attention to memory (Cabeza et al., 2011; O'Connor, Han, & Dobbins, 2010).”

“Cabeza et al. (2011) show that the superior parietal lobule performs strategic memory retrieval, a combination of memory and top–down attention from the dorsal streams.”

“We suggest that this functional difference can be attributed to two different processing modes related to the developed memory as outlined in previous theories (Cabeza et al., 2008, 2011).”

“The dPPC is involved in top-down attention processing during memory encoding (Cabeza, 2008; Ciaramelli et al., 2008; Daselaar et al., 2009; Hutchinson et al., 2009; Uncapher and Wagner, 2009; Cabeza et al., 2011, 2012).”

“operating on perceptual information coming from sensory regions (Cabeza et al., 2011).”

“…intraparietal sulcus, subserve top-down and bottom-up attention processes respectively (Burianová, Ciaramelli, Grady, & Moscovitch, 2012; Cabeza, 2008; Cabeza et al., 2011; Cabeza, Ciaramelli, & Moscovitch, 2012; Cabeza, Ciaramelli, Olson, & Moscovitch, 2008; Ciaramelli, Grady, & Moscovitch, 2008).”

“…that the ventral parietal cortex, which showed the most age differences during neutral reversal, reflects bottom-up attention processes elicited by the retrieval cues or by behaviorally relevant stimuli, especially when they are unexpected (Corbetta and Shulman, 2002; Cabeza et al., 2008, 2011).”

“Previous studies utilizing functional MRI have identified increased activity in the parietal cortex during episodic memory retrieval (for reviews, see: Cabeza, Ciaramelli, Olson, & Moscovitch, 2008; Cabeza et al., 2011; Ciaramelli, Grady, & Moscovitch, 2008; Donaldson, Wheeler, & Peterson, 2009; Hutchinson, Uncapher,…”

“DPC activity has been linked to familiarity before (Cabeza et al., 2011; Ciaramelli et al., 2008), but these findings suggest that a more accurate interpretation of the activity patterns might be memory uncertainty.”

“According to the attention to memory model hypothesis that very similar attention mechanism are involved in memory tasks at the one hand and sensory processing tasks at the other [Cabeza et al., 2011].”

“The ventral parietal cortex, a region strongly associated with bottom-up attentional capture,(24,25) is also engaged during remembering.(26) Although the local processing of perceptual and memory content is segregated in this region,(27,28) pattern-information analysis has been used to track memory reactivation in the…”

“This is especially important when additional postretrieval processes are necessary to discriminate between what is true memorized content and what is not (Cabeza et al., 2011; Ciaramelli, Grady, & 2008).”

“, 2006) and have been related to a dorsal attention network involved in preparing and applying goal-directed selection for stimuli and responses (Cabeza et al., 2011; Corbetta and Shulman, 2002).”

“Specifically, superior parietal lobule shows increased activation in response to perceptual search (Sestieri et al., 2010), and retrieval goals can guide this top-down attentional process (Cabeza et al., 2008; Cabeza et al., 2011).”

“…word can act as a cue to refresh a representation of a word-in-noise, and aid in its identification, was founded upon a model of auditory attention to memory (Zimmermann, Moscovitch, & Alain, 2016), based upon the initial model in vision (Cabeza et al., 2011; Ciaramelli, Grady, & Moscovitch, 2008).”

“More recently, the bilateral AG has been shown to be involved in focusing attention on memory when information in memory has to be evaluated internally and has associated this region with the default mode network (Cabeza et al., 2011; Sormaz et al., 2018a, 2018b).”

“Second, in order to assess the pattern of activation in a-priori regions and to complement the whole-brain analysis, we adopted anatomical regions of interest (ROI) approach [55].”

“During memory tasks, the functional coupling between HPC and VAN is enhanced 114,115 , which in turn relates to mnemonic quality 116 .”