Elsevier

Neuropsychologia

Volume 50, Issue 14, December 2012, Pages 3764-3774
Neuropsychologia

Reviews and perspectives
Explaining the encoding/retrieval flip: Memory-related deactivations and activations in the posteromedial cortex

https://doi.org/10.1016/j.neuropsychologia.2012.08.021Get rights and content

Abstract

The posteromedial cortex (PMC) is strongly linked to episodic memory and age-related memory deficits. The PMC shows deactivations during a variety of demanding cognitive tasks as compared to passive baseline conditions and has been associated with the default-mode of the brain. Interestingly, the PMC exhibits opposite levels of functional MRI activity during encoding (learning) and retrieval (remembering), a pattern dubbed the encoding/retrieval flip (E/R-flip). Yet, the exact role of the PMC in memory function has remained unclear. This review discusses the possible neurofunctional and clinical significance of the E/R-flip pattern. Regarding neurofunctional relevance, we will review four hypotheses on PMC function: (1) the internal orienting account, (2) the self-referential processing account, (3) the reallocation account, and (4) the bottom-up attention account. None of these accounts seem to provide a complete explanation for the E/R-flip pattern in PMC. Regarding clinical relevance, we review work on aging and Alzheimer's disease, indicating that amyloid deposits within PMC, years before clinical memory deficits become apparent. High amyloid burden within PMC is associated with detrimental influences on memory encoding, in particular, the attenuation of beneficial PMC deactivations. Finally, we discuss functional subdivisions within PMC that help to provide a more precise picture of the variety of signals observed within PMC. Collective data from anatomical, task-related fMRI and resting-state studies all indicate that the PMC is composed of three main regions, the precuneus, retrosplenial, and posterior cingulate cortex, each with a distinct function. We will conclude with a summary of the findings and provide directions for future research.

Highlights

► Posteromedial cortex (PMC) deactivates when Encoding and activates when Retrieving. ► Pre-clinical markers of Alzheimer's are linked to PMC changes and the E/R-flip. ► Four neurocognitive accounts are discussed that can possibly explain the E/R-flip. ► Future research on PMC function requires consideration of its functional subregions.

Introduction

The posteromedial cortex (PMC) is strongly associated with episodic memory and considered a central node of the default-mode (Buckner et al., 2008, Raichle et al., 2001). The default-mode network (DMN) involves a set of strongly connected regions that in functional neuroimaging studies tends to be activated during rest but deactivated during demanding cognitive tasks (Mazoyer et al., 2001, McKiernan et al., 2003, Shulman et al., 1997). According to the default-mode hypothesis, these deactivations arise, because PMC and other DMN regions support cognitive processes that normally occur during rest, but must be temporarily shut down when available resources are needed for active task performance (Raichle et al., 2001). Interestingly, successful learning of events (episodic encoding) has been associated with reduced activity in the PMC, whereas successful retrieval of events (episodic retrieval) has been associated with increased activity in the same region (e.g. Buckner et al., 1996, Daselaar et al., 2004, Hayama et al., 2012, Kim, 2011, Otten and Rugg, 2001, Shrager et al., 2008, Wagner et al., 1998, Wagner et al., 2005). These opposing effects, which have been dubbed the encoding/retrieval flip (E/R-flip), were originally reported by Daselaar et al. (2009) who observed this pattern not across participants in separate encoding and retrieval studies, but within the same study and within the same participants for a variety of stimuli and memory paradigms. Since then, the E/R-flip pattern has been replicated in several other studies (Gilbert, Armbruster, & Panagiotidi, 2011; Huijbers et al., 2009, Huijbers et al., 2011; Kim, Daselaar, & Cabeza, 2010; Vannini, O'Brien, O'Keefe, Pihlajamaki, Laviolette, & Sperling, 2011). Yet, despite the robustness of the E/R-flip, the functional significance of this pattern and the role of the PMC in memory still remain unclear.

This review aims to clarify the relation between the function of the PMC and the E/R-flip pattern, and includes three sections. Section 2 reviews studies that found the E/R-flip pattern and discusses how the E/R-flip may lead to competition between encoding and retrieval processes. Section 2.3 discusses the relevance of the E/R-flip for clinical studies of aging and Alzheimer's disease and provides a direct link between PMC deactivations during encoding and memory-decline. Section 3 focuses on four different hypotheses that could potentially explain the E/R-flip pattern in the PMC. Section 4 of our review discusses anatomical, functional, and connectivity findings indicating three functionally distinct subregions within PMC; the precuneus (Pcun), posterior cingulate cortex (PCC), and retrosplenial cortex (RsC). Distinguishing between these subregions should help to further clarify the role of PMC in memory function. The review ends with a concluding section and directions for future research.

Section snippets

Converging evidence for the encoding/retrieval flip

The most powerful method for identifying brain regions associated with successful memory encoding processes using fMRI is known as the subsequent memory paradigm. In this paradigm, encoding trials are back-sorted based on whether they are subsequently remembered (hit) or forgotten (miss). There have been numerous fMRI studies using this paradigm, which have generally found greater activity for encoding hits than misses, or a positive encoding success effect, in the medial temporal lobe (MTL), a

Theoretical accounts

The clinical research reviewed in the previous section suggests a link between PMC integrity, the E/R-flip pattern, and episodic memory. However, these findings do not explain the E/R-flip in terms of underlying cognitive processes. Four prevailing theories could potentially explain the E/R-flip: (1) the internal orienting account, (2) the self-referential processing account, (3) the reallocation account and, (4) the bottom-up attention account. Below, we discuss evidence in favor of, and

Functional subdivisions of PMC

One critical issue when interpreting fMRI results regarding PMC is that there is considerable evidence indicating functional subdivisions within PMC. Thus, simply considering these different areas as a single PMC region with one unitary function can hinder our understanding of the PMC. As noted at the beginning of this review, three major regions can be roughly discriminated within PMC: RsC, Pcun, and PCC.

The E/R-flip has been reported most consistently within PCC and Pcun (e.g. Daselaar et

Conclusions

The PMC reliably shows opposing levels of activation during encoding and retrieval, the E/R-flip pattern, and this can lead to a competition between encoding and retrieval states. In terms of clinical relevance, age-related pathology, specifically amyloid deposition within the PMC, has detrimental effects on the E/R-flip. Thus, the E/R-flip is an interesting candidate for tracking longitudinal changes in episodic memory during pre-clinical stages of Alzheimer's disease (Sperling et al., 2011).

Acknowledgments

This work was supported by the European Molecular Biology Organization: ALTF 318-2011 [W.H.], the Amsterdam Brain Imaging Platform [W.H, S.D.], the Marie Curie Fellowship: FP7-PEOPLE-2007-4-1-IOF from the European Union [P.V.], the Swedish Brain Foundation and Swedish Society for Medicine [P.V.], the Institutes of Health: K24 AG035007 [R.S.], R01 AG027435-S1 [R.S.], P01AG036694 [R.S.], P50AG00513421 [R.S.], and the Alzheimer's Association: IIRG-06-27374 [R.S] and the Netherlands Organization

References (112)

  • N. Jaiswal et al.

    Encoding of visual–spatial information in working memory requires more cerebral efforts than retrieval: Evidence from an EEG and virtual reality study

    Brain Research

    (2010)
  • K.M. Kennedy et al.

    Effects of beta-amyloid accumulation on neural function during encoding across the adult lifespan

    Neuroimage

    (2012)
  • H. Kim

    Neural activity that predicts subsequent memory and forgetting: A meta-analysis of 74 fMRI studies

    Neuroimage

    (2011)
  • H. Kim et al.

    Overlapping brain activity between episodic memory encoding and retrieval: roles of the task-positive and task-negative networks

    Neuroimage

    (2010)
  • J. Kong et al.

    Exploring the brain in pain: Activations, deactivations and their relation

    Pain

    (2010)
  • B. Mazoyer et al.

    Cortical networks for working memory and executive functions sustain the conscious resting state in man

    Brain Research Bulletin

    (2001)
  • G. Northoff et al.

    Self-referential processing in our brain—A meta-analysis of imaging studies on the self

    Neuroimage

    (2006)
  • L.J. Otten et al.

    When more means less: Neural activity related to unsuccessful memory encoding

    Current Biology

    (2001)
  • K.A. Paller et al.

    Observing the transformation of experience into memory

    Trends in Cognitive Sciences

    (2002)
  • C.C. Rowe et al.

    Amyloid imaging results from the Australian Imaging, Biomarkers and Lifestyle (AIBL) study of aging

    Neurobiology of Aging

    (2010)
  • M.D. Rugg et al.

    Retrieval processing and episodic memory

    Trends in Cognitive Sciences

    (2000)
  • R. Scheeringa et al.

    Neuronal dynamics underlying high- and low-frequency EEG oscillations contribute independently to the human BOLD signal

    Neuron

    (2011)
  • R. Scheeringa et al.

    Trial-by-trial coupling between EEG and BOLD identifies networks related to alpha and theta EEG power increases during working memory maintenance

    Neuroimage

    (2009)
  • Y. Shrager et al.

    Activity in both hippocampus and perirhinal cortex predicts the memory strength of subsequently remembered information

    Neuron

    (2008)
  • J. Spaniol et al.

    Event-related fMRI studies of episodic encoding and retrieval: Meta-analyses using activation likelihood estimation

    Neuropsychologia

    (2009)
  • R.A. Sperling et al.

    Toward defining the preclinical stages of Alzheimer's disease: Recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease

    Alzheimers Dement

    (2011)
  • R.A. Sperling et al.

    Amyloid deposition is associated with impaired default network function in older persons without dementia

    Neuron

    (2009)
  • J.J. Summerfield et al.

    Cortical midline involvement in autobiographical memory

    Neuroimage

    (2009)
  • M.R. Uncapher et al.

    Episodic encoding is more than the sum of its parts: An fMRI investigation of multifeatural contextual encoding

    Neuron

    (2006)
  • M.R. Uncapher et al.

    Posterior parietal cortex and episodic encoding: insights from fMRI subsequent memory effects and dual-attention theory

    Neurobiology of Learning and Memory

    (2009)
  • G. Vingerhoets et al.

    Motor imagery in mental rotation: An fMRI study

    Neuroimage

    (2002)
  • A.W. Bero et al.

    Neuronal activity regulates the regional vulnerability to amyloid-[beta] deposition

    Nature Neuroscience

    (2011)
  • R.L. Buckner et al.

    The brain's default network: Anatomy, function, and relevance to disease

    Annals of New York Academy of Sciences

    (2008)
  • R.L. Buckner et al.

    Functional anatomic studies of memory retrieval for auditory words and visual pictures

    Journal of Neuroscience

    (1996)
  • R. Cabeza et al.

    The parietal cortex and episodic memory: An attentional account

    Nature Reviews Neuroscience

    (2008)
  • R. Cabeza et al.

    Overlapping parietal activity in memory and perception: Evidence for the attention to memory model

    Journal of Cognitive Neuroscience

    (2011)
  • R. Cabeza et al.

    Cognitive contributions of the ventral parietal cortex: An integrative theoretical account

    Trends in Cognitive Sciences.

    (2012)
  • A.E. Cavanna et al.

    The precuneus: A review of its functional anatomy and behavioural correlates

    Brain

    (2006)
  • Y. Chao-Gan et al.

    DPARSF: A MATLAB toolbox for "Pipeline" data analysis of resting-state fMRI

    Frontiers in Systems Neuroscience

    (2010)
  • E. Ciaramelli et al.

    Top-down and bottom-up attention to memory are dissociated in posterior parietal cortex: Neuroimagingand and neuropsychological evidence

    Journal of Neuroscience

    (2010)
  • Ciaramelli, E., Grady, C. L., & Moscovitch, M. (2008). Top-down and bottom-up attention to memory: A hypothesis (AtoM)...
  • Cirrito, J. R., Yamada, K. A., Finn, M. B., Sloviter, R. S., Bales, K. R., May, P. C., et al. (2005). Synaptic activity...
  • M. Corbetta et al.

    Control of goal-directed and stimulus-driven attention in the brain

    Nature Reviews Neuroscience

    (2002)
  • J.S. Damoiseaux et al.

    Consistent resting-state networks across healthy subjects

    Proceedings of the National Academy of Science USA

    (2006)
  • S.M. Daselaar et al.

    Triple dissociation in the medial temporal lobes: Recollection, familiarity, and novelty

    Journal of Neurophysiology

    (2006)
  • Daselaar, S. M., Rice, H. J., Greenberg, D. L., Cabeza, R., Labar, K. S., & Rubin, D. C. (2007). The spatiotemporal...
  • S.M. Daselaar et al.

    Posterior midline and ventral parietal activity is associated with retrieval success and encoding failure

    Frontiers in Human Neuroscience

    (2009)
  • L. Davachi et al.

    Multiple routes to memory: Distinct medial temporal lobe processes build item and source memories

    Proceedings of the National Academy of Science USA

    (2003)
  • A. Drzezga et al.

    Neuronal dysfunction and disconnection of cortical hubs in non-demented subjects with elevated amyloid burden

    Brain

    (2011)
  • Dodell-Feder, D., Koster-Hale, J., Bedny, M., & Saxe, R. (2011). fMRI item analysis in a theory of mind task....
  • Cited by (0)

    View full text