Trends in Cognitive Sciences
Volume 9, Issue 9, September 2005, Pages 445-453
Journal home page for Trends in Cognitive Sciences

Parietal lobe contributions to episodic memory retrieval

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Although the parietal lobe is not traditionally thought to support declarative memory, recent event-related fMRI studies of episodic retrieval have consistently revealed a range of memory-related influences on activation in lateral posterior parietal cortex (PPC) and precuneus extending into posterior cingulate and retrosplenial cortex. This article surveys the fMRI literature on PPC activation during remembering, a literature that complements earlier electroencephalography data. We consider these recent memory-related fMRI responses within the context of classical ideas about parietal function that emphasize space-based attention and motor intention. We conclude by proposing three hypotheses concerning how parietal cortex might contribute to memory.

Introduction

Episodic memory – conscious memory for everyday events [1] – has long been known to depend on the medial temporal lobe (MTL) memory system 2, 3 and on prefrontal contributions to encoding and retrieval 4, 5. Although theoretical and experimental emphasis remains on specifying how MTL and prefrontal structures mediate the acquisition, consolidation and retrieval of episodic memories, an emerging body of functional imaging evidence suggests that a full understanding of episodic memory might also require specification of parietal contributions to retrieval 6, 7. Here we review this surprising new literature and develop hypotheses regarding how parietal cortex might support remembering.

The basic phenomenon that has sparked interest in parietal contributions to episodic retrieval is that differential parietal responses are observed when individuals correctly recognize previously encountered old items (hits) as compared with correctly identifying new unstudied items (correct rejections; CRs). The earliest observations of such ‘old/new’ effects (alternatively labeled ‘retrieval success’ effects; [8]) were obtained with electroencephalography, wherein the magnitude of event-related potentials (ERP) differed at left and medial parietal scalp electrode sites during hits and CRs (for review, see [9]). More recently, event-related functional MRI (fMRI) studies have documented greater activation during hits than during CRs in posterior parietal cortex (PPC), including inferior and superior parietal lobules, as well as medial structures that extend from precuneus into posterior cingulate and retrosplenial cortices.

Beyond simply identifying neural regions that demonstrate old/new effects (Box 1), fMRI studies have suggested a range of distinct memory-related influences on parietal activation. For example, activation in PPC modulates based on the perception that information is old (or familiar) even when that perception is in error 10, 11. PPC activation also increases when recognition is accompanied by the recollection of event details 12, 13, 14, 15, and, in forced-choice recognition designs, regions in PPC are engaged when retrieval is oriented towards recollecting episodic details as compared with detecting item familiarity 13, 16, 17. This article surveys these recent fMRI findings of PPC activation during episodic retrieval. In the course of doing so, we consider how these findings from the memory literature relate to classical attention and intention accounts of parietal function. We conclude by proposing a set of hypotheses about how parietal cortices might contribute to remembering.

Section snippets

The old/new effect – a multi-study analysis

Event-related fMRI studies of retrieval have revealed greater PPC activation during hits as compared with CRs. Across experiments, such old/new effects generalize across verbal and visual-object targets (e.g. words and faces, 8, 18, 19, 20) and across yes/no recognition, remember/know, recognition confidence, and source recollection paradigms 11, 12, 14, 15, 21, 22, demonstrating that certain PPC regions are sensitive to, or signal some aspect of, successful retrieval 8, 10, 12, 23. Although

Factors that modulate parietal responses at retrieval

PPC regions show old/new effects that generalize across different item modalities, variable response conditions, and multiple data samples across laboratories (Figure 1), suggesting that these regions consistently track processes correlated with the successful retrieval of episodic information. However, comparisons between hits and CRs do not specify the particular mnemonic attributes that give rise to the observed activation differences, because the processing of hits and CRs can differ along

Relation to classical accounts of parietal function

Lesions to parietal cortex can result in neglect, an attentional deficit, or apraxia, a deficit in planning motor movements 42, 43. Such observations, together with data from single-unit recording studies in monkeys, have motivated the space-based attention and motor intention theories of parietal function 44, 45. An important question is whether memory-related parietal responses can be explained in terms of these classical ideas. For example, given that eye movements [46] and response times

Understanding parietal contributions to retrieval

Clues about parietal contributions to memory come from anatomy. Lateral parietal, retrosplenial, and posterior cingulate cortices are connected directly or indirectly to the MTL 47, 48, 49. Monkey IPL has direct reciprocal projections to parahippocampal cortex 48, 50 and direct projections to hippocampus [51]. Along the midline, afferent connections to retrosplenial cortex are dominated by MTL projections. Kobayashi and Amaral [49] speculate, based on this anatomy, that retrosplenial cortex

Conclusions

As surveyed here, fMRI studies have revealed the surprising (but remarkably consistent) finding that specific parietal regions are active during episodic retrieval tasks. The basic observations can be summarized as follows:

(1) Multiple parietal regions are active during episodic retrieval, including regions within the intraparietal sulcus extending laterally to the inferior parietal lobule, as well as midline structures that extend from the retrosplenial cortex and posterior cingulate to the

Acknowledgements

We thank Ian Dobbins for provision of data and for insightful discussions, and David Van Essen for use of Caret software and the PALS approach. Supported by the National Science Foundation, National Institutes of Health, McKnight Endowment Fund for Neuroscience, Ellison Medical Foundation, Alfred P. Sloan Foundation, McDonnell Foundation, and the Howard Hughes Medical Institute.

References (80)

  • A.M. Morcom et al.

    Effects of age on retrieval cue processing as revealed by ERPs

    Neuropsychologia

    (2004)
  • R.L. Buckner

    Memory and executive function in aging and AD: Multiple factors that cause decline and reserve factors that compensate

    Neuron

    (2004)
  • A. Baddeley

    Recent developments in working memory

    Curr. Opin. Neurobiol.

    (1998)
  • A.P. Yonelinas

    The nature of recollection and familiarity: A review of 30 years of research

    J. Mem. Lang.

    (2002)
  • D.L. Schacter

    Late onset of anterior prefrontal activity during true and false recognition: An event-related fMRI study

    Neuroimage

    (1997)
  • P.C. Fletcher

    The mind's eye–precuneus activation in memory-related imagery

    Neuroimage

    (1995)
  • R.L. Buckner

    Functional-anatomic study of episodic retrieval using fMRI. I. Retrieval effort versus retrieval success

    Neuroimage

    (1998)
  • L.L. Jacoby

    A process dissociation framework: Separating automatic from intentional uses of memory

    J. Mem. Lang.

    (1991)
  • K. Allan

    Electrophysiological evidence for dissociable processes contributing to recollection

    Acta Psychol. (Amst.)

    (1998)
  • E. Tulving

    Elements of Episodic Memory

    (1983)
  • L.R. Squire

    Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans

    Psychol. Rev.

    (1992)
  • N.J. Cohen et al.

    Memory, Amnesia, and the Hippocampal System

    (1993)
  • D.T. Stuss et al.

    Neuropsychological studies of the frontal lobes

    Psychol. Bull.

    (1984)
  • A.P. Shimamura

    Memory and frontal lobe function

  • R.L. Buckner et al.

    The cognitive neuroscience of remembering

    Nat. Rev. Neurosci.

    (2001)
  • M.D. Rugg

    The neural basis of episodic memory: Evidence from functional neuroimaging

    Philos. Trans. R. Soc. Lond. B Biol. Sci.

    (2002)
  • M.D. Rugg

    Event-related potential studies of human memory

  • M.E. Wheeler et al.

    Functional dissociation among components of remembering: Control, perceived oldness, and content

    J. Neurosci.

    (2003)
  • I. Kahn

    Functional-neuroanatomic correlates of recollection: Implications for models of recognition memory

    J. Neurosci.

    (2004)
  • R.N.A. Henson

    Recollection and familiarity in recognition memory: An event-related functional magnetic resonance imaging study

    J. Neurosci.

    (1999)
  • L.L. Eldridge

    Remembering episodes: A selective role for the hippocampus during retrieval

    Nat. Neurosci.

    (2000)
  • I.G. Dobbins et al.

    Domain-general and domain-sensitive prefrontal mechanisms for recollecting events and detecting novelty

    Cereb. Cortex

    (2005)
  • K.B. McDermott

    Retrieval success is accompanied by enhanced activation in anterior prefrontal cortex during recognition memory: An event-related fMRI study

    J. Cogn. Neurosci.

    (2000)
  • R.N. Henson

    Face repetition effects in implicit and explicit memory tests as measured by fMRI

    Cereb. Cortex

    (2002)
  • R.N.A. Henson

    Confidence in recognition memory for words: Dissociating right prefrontal roles in episodic retrieval

    J. Cogn. Neurosci.

    (2000)
  • S. Cansino

    Brain activity underlying encoding and retrieval of source memory

    Cereb. Cortex

    (2002)
  • B.J. Shannon et al.

    Functional-anatomic correlates of memory retrieval that suggest nontraditional processing roles for multiple distinct regions within posterior parietal cortex

    J. Neurosci.

    (2004)
  • Van Essen, D.C. A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex. NeuroImage (in...
  • D.C. Van Essen

    An integrated software suite for surface-based analyses of cerebral cortex

    J. Am. Med. Inform. Assoc.

    (2001)
  • M.D. Rugg

    Brain regions supporting intentional and incidental memory: A PET study

    Neuroreport

    (1997)
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