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  • Review Article
  • Published:

Two cortical systems for memory-guided behaviour

Nature Reviews Neuroscience volume 13, pages 713–726 (2012)Cite this article

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Key Points

  • The perirhinal cortex (PRC), parahippocampal cortex (PHC) and retrosplenial cortex (RSC) are crucial for memory in humans, so it is essential to understand the functions of these areas.

  • The PHC and RSC exhibit patterns of anatomical and functional connectivity that are highly similar to one another and strikingly different from the PRC.

  • The PRC is important for familiarity-based item recognition, associating features of objects and fine-grained perceptual or semantic discriminations.

  • The PHC and RSC are important for recollection-based memories, memory for spatial and episodic context, scene perception, simulation of hypothetical events and certain aspects of spatial navigation and social cognition.

  • Integrating this evidence, we propose a new framework in which the PRC, PHC and RSC are embedded in two extended networks that support different forms of memory-guided behaviour.

  • The PRC is situated in an anterior temporal (AT) system that also includes the amygdala, ventral temporopolar cortex and lateral orbitofrontal cortex. This system may collectively support the assessment of the significance of specific entities.

  • The PHC and RSC are situated in a posterior medial (PM) system that also includes the mammillary bodies, anterior thalamic nuclei, pre- and parasubiculum, posterior cingulate, precuneus and angular gyrus. This system may support the construction of situation models in support of memory, spatial navigation and social cognition.

  • The AT and PM systems are differentially targeted by neurological disorders. For instance, semantic dementia is associated with disproportionate atrophy and dysfunction within the AT system relative to Alzheimer's disease, which disproportionately affects the PM system.

Abstract

Although the perirhinal cortex (PRC), parahippocampal cortex (PHC) and retrosplenial cortex (RSC) have an essential role in memory, the precise functions of these areas are poorly understood. Here, we review the anatomical and functional characteristics of these areas based on studies in humans, monkeys and rats. Our Review suggests that the PRC and PHC–RSC are core components of two separate large-scale cortical networks that are dissociable by neuroanatomy, susceptibility to disease and function. These networks not only support different types of memory but also appear to support different aspects of cognition.

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Figure 1: Anatomy of the perirhinal, parahippocampal and retrosplenial cortices.
Figure 2: Two neocortical systems for memory-guided behaviour.
Figure 3: Schematic depiction of the functions of the anterior temporal and posterior medial systems.

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Acknowledgements

We thank the many colleagues (including three anonymous reviewers) who gave helpful suggestions and comments on previous drafts and apologize to those whose work could not be cited owing to citation limits. This paper was supported by US National Institute of Mental Health grant 1R01MH083734.

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  1. Department of Psychology, University of California at Davis, 1544 Newton Ct., Davis, 95618, California, USA

    Charan Ranganath

  2. Center for Neuroscience, University of California at Davis, 1544 Newton Ct., Davis, 95618, California, USA

    Charan Ranganath & Maureen Ritchey

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NeuroSynth

Glossary

Hippocampal formation

A term used to collectively describe the entorhinal cortex, dentate gyrus, subfields CA1, CA2 and CA3, and the subiculum.

Immediate early gene

A gene that encodes a transcription factor that is induced within minutes of raised neuronal activity without requiring a protein signal. Immediate early gene activation is therefore used as an indirect marker of neuronal activation.

Semantic priming

A quickening in reaction time for responding to words that are preceded by a semantically related “priming stimulus”.

Autobiographical memories

Memories of personal events from an individual's life.

Retrograde amnesia

Memory loss of events that occurred before the onset of a memory disorder. Typically, following the onset of medial temporal lobe damage, patients show a reduced ability to recollect episodes from the time period before the brain damage occurred.

Delayed non-matching to place task

A spatial recognition memory task in which animals have to distinguish a non-visited arm of a maze from a previously visited arm and enter the non-visited arm in order to receive a reward.

Theta oscillations

Large, rhythmic changes in the amplitude of local field potentials that are seen in the 5–12 Hz frequency in rodents and in the 4–8 Hz range in humans. Theta oscillations are evident during active exploration of novel environments and have been functionally associated with spatial navigation and memory for temporal sequences.

Theory of mind

The ability to understand the mental states — such as beliefs, desires and intentions — of others.

Connectional fingerprints

The patterns of cortico–cortical connections exhibited by cytoarchitectonic areas.

Systems consolidation

A hypothesized process by which the brain regions that support memory of a particular experience are thought to change over time. Systems consolidation theories are typically invoked to explain differential effects of brain lesions on memories of recent and remote events.

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Ranganath, C., Ritchey, M. Two cortical systems for memory-guided behaviour. Nat Rev Neurosci 13, 713–726 (2012). https://doi.org/10.1038/nrn3338

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