Hippocampus and neocortex: recognition and spatial memory

https://doi.org/10.1016/j.conb.2011.02.002Get rights and content

Recognition and spatial memory are typically associated with the perirhinal cortex and hippocampal formation, respectively. Solely focusing on these structures for these specific mnemonic functions may, however, be limiting progress in the field. The distinction between these subdivisions of memory is becoming less defined as, for example, hippocampal cells traditionally considered to encode locations also encode place–object associations. There is increasing evidence for the involvement of overlapping networks of brain structures for aspects of both spatial and recognition memory. Future models of spatial and recognition memory will have to extend beyond the hippocampus and perirhinal cortex to incorporate a wider network of cortical and subcortical structures.

Research highlights

► Recognition and spatial memory are typically associated with the perirhinal cortex and hippocampal formation, respectively. ► There is increasing evidence for the involvement of overlapping networks of brain structures for components of both spatial and recognition memory. ► Research into object–context associations has shown how hippocampal spatial representations contribute to wider aspects of memory. ► Future models of spatial and recognition memory need to extend beyond the hippocampus and perirhinal cortex.

Introduction

The neural processes that allow us to form episodic memories, that is, remember events we experience throughout our lives, are still far from fully understood. Neuropsychological studies have been pivotal in identifying those brain structures that are necessary for forming new memories but typically studies in animals are required to investigate these mnemonic processes with higher anatomical resolution. There continues to be a debate as to whether the term episodic memory can even be applied to non-humans; this is particularly relevant when considering vivid experiences where remembering can give a sense of ‘re-living’ the event in a way that has been likened to mental-time travel (see [1]). Whether or not episodic memory is directly comparable across species, there are certainly aspects of episodic memory that can be assessed in animals such as memory for objects, spatial routes and locations, and spatiotemporal context. The recent use of convergent approaches to assess the neural substrates of both recognition memory and spatial learning, including electrophysiological recordings, immediate-early gene imaging, and lesion disconnection studies, has identified an interactive network of regions that support these functions. In this review, we will discuss findings from recent studies that have shed light on aspects of object recognition, spatial memory, and how these two forms of memory are brought together. Recent findings will be put into the context of a more unified model of memory that focuses on interactions, rather than dissociations, between brain regions.

Section snippets

Recognition memory

One component of memory is recognising whether you have encountered someone or something before. This ability can be assessed non-verbally by using a preferential viewing paradigm that builds on the innate preference of animals, including humans, to look at, or explore, something novel. In rats, the spontaneous object recognition task has been used to assess the neural substrates of recognition memory [2] (see Figure 1). While there is an ongoing debate about the extent to which the hippocampus

Space, place and navigation

The hippocampus has long been implicated in spatial memory in both humans and animals [16]. Cells within the hippocampal formation contain a number of electrophysiological properties consistent with their role in forming allocentric representations of space, including head-direction, place and grid cells [17, 18]. Two recent studies have shown how these electrophysiological properties develop in very young rats from when they first explore outside of the nest [19, 20]. The authors of both

Putting things in context

While the traditional focus in animal research has been to assess either memory for objects or memory for places, a growing trend is to combine these different aspects of memory within the same task. This is arguably a more realistic approach in terms of what animals instinctively learn and also more comparable to the combined components of human episodic memory [31, 32]. Combining memory for objects and the contexts in which they occur in has also shifted the focus away from the more

Conclusions

Spatial and recognition memory have typically been considered to be distinct types of memory that are supported by separate brain regions: the hippocampal formation and perirhinal cortex, respectively. However, an overemphasis on these specific neural structures and their respective importance for spatial and recognition memory may impede progress in the field. Recent research has brought together divergent models of memory, by using behavioural tests that combine aspects of spatial and object

References and recommended reading

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

  • • of special interest

  • •• of outstanding interest

Acknowledgements

SDV is funded by a Wellcome Trust Senior Research Fellowship in Basic Biomedical Science [WT090954AIA]; MMA is funded by a Wellcome Trust research grant [WT087855]. The authors wish to thank Andrew Nelson and John Aggleton for their extremely helpful comments on the manuscript.

References (58)

  • S.D. Vann et al.

    Hippocampal, retrosplenial, and prefrontal hypoactivity in a model of diencephalic amnesia: evidence towards an interdependent subcortical–cortical memory network

    Hippocampus

    (2009)
  • C.D. Harvey et al.

    Intracellular dynamics of hippocampal place cells during virtual navigation

    Nature

    (2009)
  • E. Tulving

    Episodic memory: from mind to brain

    Annu Rev Psychol

    (2002)
  • M.W. Brown et al.

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

    Nat Rev Neurosci

    (2001)
  • M.W. Brown et al.

    Recognition memory: material, processes, and substrates

    Hippocampus

    (2010)
  • S.M. McTighe et al.

    Paradoxical false memory for objects after brain damage

    Science

    (2010)
  • S.J. Bartko et al.

    Perirhinal cortex resolves feature ambiguity in configural object recognition and perceptual oddity tasks

    Learn Mem

    (2007)
  • M.M. Albasser et al.

    New behavioral protocols to extend our knowledge of rodent object recognition memory

    Learn Mem

    (2010)
  • B.D. Winters et al.

    A distributed cortical representation underlies crossmodal object recognition in rats

    J Neurosci

    (2010)
  • J.S. Holdstock et al.

    Integrating visual and tactile information in the perirhinal cortex

    Cereb Cortex

    (2009)
  • M.M. Albasser et al.

    Qualitatively different modes of perirhinal-hippocampal engagement when rats explore novel vs. familiar objects as revealed by c-Fos imaging

    Eur J Neurosci

    (2010)
  • M.R. Horne et al.

    Lesions of the perirhinal cortex do not impair integration of visual and geometric information in rats

    Behav Neurosci

    (2010)
  • J. O’Keefe et al.

    The Hippocampus as a Cognitive Map

    (1978)
  • E.I. Moser et al.

    Place cells, grid cells, and the brain's spatial representation system

    Annu Rev Neurosci

    (2008)
  • T.J. Wills et al.

    Development of the hippocampal cognitive map in preweanling rats

    Science

    (2010)
  • R.F. Langston et al.

    Development of the spatial representation system in the rat

    Science

    (2010)
  • J.L. Calton et al.

    Hippocampal place cell instability after lesions of the head direction cell network

    J Neurosci

    (2003)
  • P.E. Sharp et al.

    Lesions of the mammillary body region severely disrupt the cortical head direction, but not place cell signal

    Hippocampus

    (2008)
  • S.D. Vann

    Transient spatial deficit associated with bilateral lesions of the lateral mammillary nuclei

    Eur J Neurosci

    (2005)
  • Cited by (72)

    View all citing articles on Scopus
    View full text