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Overlapping Parietal Activity in Memory and Perception: Evidence for the Attention to Memory Model
Open accessAbstract
The specific role of different parietal regions to episodic retrieval is a topic of intense debate. According to the Attention to Memory (AtoM) model, dorsal parietal cortex (DPC) mediates top–down attention processes guided by retrieval goals, whereas ventral parietal cortex (VPC) mediates bottom–up attention processes captured by the retrieval output or the retrieval cue. This model also hypothesizes that the attentional functions of DPC and VPC are similar for memory and perception. To investigate this last hypothesis, we scanned participants with event-related fMRI whereas they performed memory and perception tasks, each comprising an orienting phase (top–down attention) and a detection phase (bottom–up attention). The study yielded two main findings. First, consistent with the AtoM model, orienting-related activity for memory and perception overlapped in DPC, whereas detection-related activity for memory and perception overlapped in VPC. The DPC overlap was greater in the left intraparietal sulcus, and the VPC overlap in the left TPJ. Around overlapping areas, there were differences in the spatial distribution of memory and perception activations, which were consistent with trends reported in the literature. Second, both DPC and VPC showed stronger connectivity with medial-temporal lobe during the memory task and with visual cortex during the perception task. These findings suggest that, during memory tasks, some parietal regions mediate similar attentional control processes to those involved in perception tasks (orienting in DPC vs. detection in VPC), although on different types of information (mnemonic vs. sensory).
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“Indeed, Cabeza et al. (2011;2012) have also proposed that the ventral parietal cortex could have an overarching function, but it has subregions that, through different functional connectivity, apply the function to different types of information according to different goals.”
From Functional Heterogeneity and Convergence in the Right Temporoparietal Junction (2016) · cites this paper as Cabeza et al. 2011
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“Even if the region of overlap performs a common function such as contextual updating, the pattern of the input to or output from this region could be different depending on the task being performed (Cabeza et al. 2011;Cabeza et al. 2012;Geng and Vossel 2013).”
From Functional Heterogeneity and Convergence in the Right Temporoparietal Junction (2016) · cites this paper as Cabeza et al. 2011
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Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., Mazoyer, B., & Joliot, M. (2002) · NeuroImage · doi:10.1006/nimg.2001.0978 · Cited by 16,319 · cited 1×
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“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…”
InfluentialMaldjian, J. A., Laurienti, P. J., Kraft, R., & Burdette, J. H. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00169-1 · Cited by 5,066
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“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).”
Parietal lobe contributions to episodic memory retrieval
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“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.”
The parietal cortex and episodic memory: an attentional account
Cabeza, R. E. L., Ciaramelli, E., Olson, I. R., & Moscovitch, M. (2008) · Nature reviews. Neuroscience · doi:10.1038/nrn2459 · Cited by 1,256 · cited 9×
“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).”
InfluentialSelf-citationMeasures of Association for Cross Classifications*
Goodman, L. A., & Kruskal, W. (1954) · Journal of the American Statistical Association · doi:10.1080/01621459.1954.10501231 · Cited by 684
Memory retrieval and the parietal cortex: A review of evidence from a dual-process perspective
Vilberg, K. L., & Rugg, M. D. (2008) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2008.01.004 · Cited by 644 · cited 3×
“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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InfluentialSelf-citationIntegrating Memories in the Human Brain: Hippocampal-Midbrain Encoding of Overlapping Events
Daphna Shohamy, A., & Wagner, A. D. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.023 · Cited by 525 · cited 1×
“It is worth noting that the overlapping word pair learning task is different than typical transitive inference tasks (e.g., Shohamy & Wagner, 2008), because it does not fulfill the transitive property (e.g., dog is associated with cat and cat is associated with tiger, but dog is not associated with…”
Cognitive contributions of the ventral parietal cortex: an integrative theoretical account
Cabeza, R., Ciaramelli, E., & Moscovitch, M. (2012) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2012.04.008 · Cited by 373
Self-citationBerryhill, M. E., Phuong, L., Picasso, L., Cabeza, R. E. L., & Olson, I. R. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4163-07.2007 · Cited by 339 · cited 1×
“For example, patients with VPC lesions have difficulty spontaneously reporting retrieved memories about themselves, but these memories are available and can be accessed by specific questions that guide top–down attention toward these memories (Berryhill, Phuong, Picasso, Cabeza, & Olson, 2007 ).”
Self-citationRole of parietal regions in episodic memory retrieval: The dual attentional processes hypothesis
Cabeza, R. E. L. (2008) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2008.03.019 · Cited by 319 · cited 1×
“Other important factors include the spatial versus nonspatial nature of the task and the verbal versus nonverbal nature of the stimuli (Cabeza, 2008).”
Self-citationHutchinson, J. B., Uncapher, M. R., & Wagner, A. D. (2009) · Learning & Memory · doi:10.1101/lm.919109 · Cited by 277 · cited 9×
“…perception and memory overlapped in DPC (mainly in IPS) and that detection-related activity for perception and memory overlapped in VPC (mainly in TPJ) is not inconsistent with differences in localization between perception and memory found by Sestieri et al. (2010) and Hutchinson et al. (2009).”
InfluentialDissociation Between Memory Accuracy and Memory Confidence Following Bilateral Parietal Lesions
Simons, J. S., Peers, P. V., Mazuz, Y. S., Berryhill, M. E., & Olson, I. R. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp116 · Cited by 232 · cited 1×
“Such patients also have problems subjectively evaluating their retrieved memories (Drowos, Berryhill, Andre, & Olson, 2010 ; Simons, Peers, Mazuz, Berryhill, & Olson, 2010 ; Davidson et al, 2008 ), possibly because their memory retrieval is less spontaneous, so the patients' sense of re-experience is diminished.”
Self-citationDoes lateral parietal cortex support episodic memory?
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Self-citationFunctional Parcellation of Attentional Control Regions of the Brain
Woldorff, M. G., Hazlett, C. J., Fichtenholtz, H. M., Weissman, D. H., Dale, A. M., & Song, A. W. (2004) · Journal of Cognitive Neuroscience · doi:10.1162/089892904322755638 · Cited by 212 · cited 1×
“As an example of this last factor, for example, there is evidence that regions mediating similar attentional processes for audition versus vision are close to each other but not overlapping (Wu, Weissman, Roberts, & Woldorff, 2007; Woldorff et al., 2004).”
Self-citationFunctional Heterogeneity in Posterior Parietal Cortex Across Attention and Episodic Memory Retrieval
Hutchinson, J. B., Uncapher, M. R., Weiner, K. S., Bressler, D. W., Silver, M. A., Preston, A. R., & Wagner, A. D. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs278 · Cited by 178
The Inferior Parietal Lobule and Recognition Memory: Expectancy Violation or Successful Retrieval?
O’Connor, A. R., Han, S., & Dobbins, I. G. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.4225-09.2010 · Cited by 161
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“…perception and memory overlapped in DPC (mainly in IPS) and that detection-related activity for perception and memory overlapped in VPC (mainly in TPJ) is not inconsistent with differences in localization between perception and memory found by Sestieri et al. (2010) and Hutchinson et al. (2009).”
InfluentialThe neural circuitry underlying the executive control of auditory spatial attention
Wu, C., Weissman, D. H., Roberts, K., & Woldorff, M. G. (2007) · Brain Research · doi:10.1016/j.brainres.2006.11.088 · Cited by 153 · cited 1×
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Self-citationCiaramelli, E., Grady, C. L., Levine, B., Ween, J. E., & Moscovitch, M. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1209-09.2010 · Cited by 138
Self-citationHuijbers, W., Vannini, P., Sperling, R. A., Pennartz, C. M. A., Cabeza, R. E. L., & Daselaar, S. M. (2012) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2012.08.021 · Cited by 118
Self-citationAn fMRI investigation of posttraumatic flashbacks
Whalley, M. G., Kroes, M. C. W., Huntley, Z., Rugg, M. D., Davis, S. W., & Brewin, C. R. (2013) · Brain and Cognition · doi:10.1016/j.bandc.2012.10.002 · Cited by 115
Remember the Source: Dissociating Frontal and Parietal Contributions to Episodic Memory
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“However, if the accumulator reaches threshold just before the response, the current study would link this mechanism to VPC, whereas accumulator theorists have linked it to IPS in DPC (eg, Donaldson, Wheeler, & Petersen, 2010 ).”
Nieuwenhuis, S., Elzinga, B. M., Ras, P. H., Berends, F., Duijs, P., Samara, Z., & Slagter, H. A. (2012) · Brain and Cognition · doi:10.1016/j.bandc.2012.10.003 · Cited by 74
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Drowos, D. B., Berryhill, M. E., André, J. M., & Olson, I. R. (2010) · Neuropsychology · doi:10.1037/a0018902 · Cited by 61 · cited 1×
“Such patients also have problems subjectively evaluating their retrieved memories (Drowos, Berryhill, Andre, & Olson, 2010 ; Simons, Peers, Mazuz, Berryhill, & Olson, 2010 ; Davidson et al, 2008 ), possibly because their memory retrieval is less spontaneous, so the patients' sense of re-experience is diminished.”
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Self-citationActivation of right parietal cortex during memory retrieval of nonlinguistic auditory stimuli
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Self-citationThe inferior parietal lobule and temporoparietal junction: A network perspective
Igelström, K. M., & Graziano, M. S. A. (2017) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2017.01.001 · Cited by 367
“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).”
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“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…”
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Metadata
- Authors
- Cabeza, R., Mazuz, Y. S., Stokes, J., Kragel, J. E., Woldorff, M. G., Ciaramelli, E., Olson, I. R., & Moscovitch, M.
- Affiliations
- Duke University (US)
- University of Bologna (IT)
- Temple University (US)
- University of Toronto (CA)
- ORCID
- Venue
- Journal of Cognitive Neuroscience
- Publisher
- MIT Press - Journals
- Published
- 2011-11-01
- Volume
- 23
- Issue
- 11
- Pages
- 3209-3217
- ISSN
- 0898-929X (ISSN-L)
- 1530-8898
- PMC
- PMC3518433
- OpenAlex
- W2101277424
- Cited by
- 148
- References
- 35
- Citations by year
- 2026: 3 · 2025: 9 · 2024: 9 · 2023: 9 · 2022: 11 · 2021: 6 · 2020: 6 · 2019: 4 · 2018: 9 · 2017: 10 · 2016: 4 · 2015: 21 · 2014: 14 · 2013: 15 · 2012: 16
- FWCI
- 7.31
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Cognitive Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Archivio istituzionale della ricerca (Alma Mater Studiorum Università di Bologna) (submittedVersion)
- Funders
- National Institute on Aging (R01AG019731, AG 19731, AG23770, R01AG023770, R56AG023770)
- National Institute of Mental Health (R01MH091113)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Cognitive Functions and Memory
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- dorsal parietal cortex, episodic memory retrieval, top-down attention, bottom-up attention, orienting, detection, intraparietal sulcus, temporoparietal junction, visual cortex connectivity
- MeSH terms
- Adult, Attention, Brain Mapping, Female, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Neural Pathways, Orientation, Oxygen, Paired-Associate Learning, Parietal Lobe, Photic Stimulation, Reaction Time, Mental Recall, Visual Perception, Vocabulary, Linear Models, Young Adult
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