Brain networks underlying episodic memory retrieval

https://doi.org/10.1016/j.conb.2012.11.005Get rights and content

The importance of the medial temporal lobe to episodic memory has been recognized for decades. Recent human fMRI findings have begun to delineate the functional roles of different MTL regions, most notably the hippocampus, for the retrieval of episodic memories. Importantly, these studies have also identified a network of cortical regions  each interconnected with the MTL  that are also consistently engaged during successful episodic retrieval. Along with the MTL these regions appear to constitute a content-independent network that acts in concert with cortical regions representing the contents of retrieval to support consciously accessible representations of prior experiences.

Highlights

► Recollection depends on a content-insensitive network centered on the hippocampus. ► The recollection network comprises both medial temporal and neocortical regions. ► The network interacts with cortical regions that represent retrieved content.

Introduction

Episodic memory  consciously accessible memory for unique events  allows us to represent past experiences and to flexibly employ these representations in service of current and future goals [1]. The present review focuses on recent human fMRI findings relevant to the functional neuroanatomy of successful episodic memory retrieval. The majority of the reviewed studies took as their starting point a ‘dual-process’ model of memory [2, 3]. These models posit that a retrieval cue (such as a recognition memory test item) can elicit two qualitatively distinct kinds of mnemonic information: a multi-dimensional recollection signal that provides information about qualitative aspects of a prior event, including its context, and a scalar familiarity signal that can support simple judgments of prior occurrence. From this perspective, identifying the neural bases of episodic retrieval requires experimental designs that permit recollection-driven and familiarity-driven memory to be dissociated (Box 1). Current evidence suggests that the distinction between recollection and familiarity holds both within the MTL and at the level of the cerebral cortex, where a network of regions that appears to be preferentially engaged during successful recollection can be identified.

Section snippets

Memory signals within the MTL

The MTL  the hippocampus and surrounding perirhinal, entorhinal and parahippocampal cortices  has long been recognized as a key brain area supporting episodic memory. Reminiscent of electrophysiological findings in primates [4], fMRI studies have reported that perirhinal activity covaries inversely with the familiarity of recognition memory test items (e.g., [5]). These fMRI results are consistent with evidence from animal lesion studies [6] and a human single-case study [7] that suggest a

Cortical recollection effects

In addition to enhancement of hippocampal and parahippocampal activity, successful recollection is characteristically associated with engagement of several cortical regions, including retrosplenial/posterior cingulate cortex (BA 23/29/30/31), ventral posterior parietal cortex centered on the angular gyrus (BA 39) and mPFC (BA 10/32) [11]. Because of the density of its connections with the hippocampus and the memory impairments that accompany lesions to the region, retrosplenial cortex has been

A general recollection network?

As it was just reviewed, recollection-sensitive fMRI effects have consistently been identified in the hippocampus, parahippocampal, retrosplenial/posterior cingulate and lateral parietal cortices, and mPFC (Figure 2). The robustness of these effects in the face of wide variation in test materials and procedures for operationalizing recollection have led to the proposal that the regions constitute a content-independent network engaged whenever a retrieval cue elicits recollection [43, 44]. In

Content-selective recollection effects

According to an influential class of models (e.g., [49, 50]), a key role of the hippocampus is to store non-overlapping representations of the distributed patterns of cortical activity elicited when different events are encoded. When an effective retrieval cue is present, the appropriate hippocampal representation is reactivated, causing the reinstatement of the original pattern of activity in the cortex and the event to be ‘re-experienced’. Thus, successful recollection should be associated

Summary and open questions

Recollection of a prior experience is associated with engagement of a general network, centered on the hippocampus, in concert with cortical regions that, collectively, represent the contents of recollection. Among the many questions raised by this framework, three questions stand out. First, what are the specific functional roles of the different regions comprising this network? Second, how does the network interact with content-sensitive regions thought to represent the contents of

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgment

Preparation of this article and some of the research described in it was supported by NIMH grant 5R01MH072966.

References (57)

  • A. Baddeley

    The episodic buffer: a new component of working memory?

    Trends Cogn Sci

    (2000)
  • A.P. Shimamura

    Episodic retrieval and the cortical binding of relational activity

    Cogn Affect Behav Neurosci

    (2011)
  • K.L. Vilberg et al.

    The neural correlates of recollection: transient versus sustained fMRI effects

    J Neurosci

    (2012)
  • S. Haramati et al.

    The posterior parietal cortex in recognition memory: a neuropsychological study

    Neuropsychologia

    (2008)
  • M.E. Berryhill et al.

    Parietal lobe and episodic memory: bilateral damage causes impaired free recall of autobiographical memory

    J Neurosci

    (2007)
  • J.S. Simons et al.

    Dissociation between memory accuracy and memory confidence following bilateral parietal lesions

    Cereb Cortex

    (2010)
  • H.R. Hayama et al.

    Overlap between the neural correlates of cued recall and source memory: evidence for a generic recollection network?

    J Cogn Neurosci

    (2012)
  • D.L. Schacter et al.

    Episodic simulation of future events: concepts, data, and applications

    Ann N Y Acad Sci

    (2008)
  • K.A. Norman et al.

    Modeling hippocampal and neocortical contributions to recognition memory: a complementary-learning-systems approach

    Psychol Rev

    (2003)
  • J.D. Johnson et al.

    Recollection, familiarity, and cortical reinstatement: a multivoxel pattern analysis

    Neuron

    (2009)
  • B.A. Kuhl et al.

    Neural reactivation reveals mechanisms for updating memory

    J Neurosci

    (2012)
  • E. Tulving

    Elements of episodic memory

    (1983)
  • J.T. Wixted et al.

    A continuous dual-process model of remember/know judgments

    Psychol Rev

    (2010)
  • D. Montaldi et al.

    The neural system that mediates familiarity memory

    Hippocampus

    (2006)
  • M.W. Brown et al.

    Recognition memory: what are the roles of the perirhinal cortex and hippocampus?

    Nat Rev Neurosci

    (2001)
  • B. Bowles et al.

    Impaired familiarity with preserved recollection after anterior temporal-lobe resection that spares the hippocampus

    Proc Natl Acad Sci U S A

    (2007)
  • M. Suzuki et al.

    Recollection-related hippocampal activity during continuous recognition: a high-resolution fMRI study

    Hippocampus

    (2011)
  • C.E. Stark et al.

    Making memories without trying: medial temporal lobe activity associated with incidental memory formation during recognition

    J Neurosci

    (2003)
  • Cited by (505)

    View all citing articles on Scopus
    View full text