Imaging a memory trace over half a life-time in the medial temporal lobe reveals a time-limited role of CA3 neurons in retrieval

  1. Vanessa Lux
  2. Erika Atucha
  3. Takashi Kitsukawa
  4. Magdalena M Sauvage  Is a corresponding author
  1. Ruhr University Bochum, Germany
  2. Osaka University, Japan

Abstract

Whether retrieval still depends on the hippocampus as memories age or relies then on cortical areas remains a major controversy. Despite evidence for a functional segregation between CA1, CA3 and parahippocampal areas, their specific role within this frame is unclear. Especially, the contribution of CA3 is questionable as very remote memories might be too degraded to be used for pattern completion. To identify the specific role of these areas, we imaged brain activity in mice during retrieval of recent, early remote and very remote fear memories by detecting the immediate-early gene Arc. Investigating correlates of the memory trace over an extended period allowed us to report that, in contrast to CA1, CA3 is no longer recruited in very remote retrieval. Conversely, we showed that parahippocampal areas are then maximally engaged. These results suggest a shift from a greater contribution of the trisynaptic loop to the temporoammonic pathway for retrieval.

Article and author information

Author details

  1. Vanessa Lux

    Functional Architecture of Memory unit, Mercator Research Group, Medical Faculty, Ruhr University Bochum, Bochum, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Erika Atucha

    Functional Architecture of Memory unit, Mercator Research Group, Medical Faculty, Ruhr University Bochum, Bochum, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Takashi Kitsukawa

    Graduate School of Frontier Biosciences, Osaka University, Osaka, Japan
    Competing interests
    The authors declare that no competing interests exist.
  4. Magdalena M Sauvage

    Functional Architecture of Memory unit, Mercator Research Group, Medical Faculty, Ruhr University Bochum, Bochum, Germany
    For correspondence
    magdalena.sauvage@gmail.com
    Competing interests
    The authors declare that no competing interests exist.

Ethics

Animal experimentation: All procedures were approved by the Ruhr-Universität Bochum Institutional Animal Use Committee and the LANUV (8.87-51.04.20.09.323)

Copyright

© 2016, Lux et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 2,765
    views
  • 729
    downloads
  • 26
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Vanessa Lux
  2. Erika Atucha
  3. Takashi Kitsukawa
  4. Magdalena M Sauvage
(2016)
Imaging a memory trace over half a life-time in the medial temporal lobe reveals a time-limited role of CA3 neurons in retrieval
eLife 5:e11862.
https://doi.org/10.7554/eLife.11862

Share this article

https://doi.org/10.7554/eLife.11862

Further reading

    1. Computational and Systems Biology
    2. Neuroscience
    Anna Cattani, Don B Arnold ... Nancy Kopell
    Research Article

    The basolateral amygdala (BLA) is a key site where fear learning takes place through synaptic plasticity. Rodent research shows prominent low theta (~3–6 Hz), high theta (~6–12 Hz), and gamma (>30 Hz) rhythms in the BLA local field potential recordings. However, it is not understood what role these rhythms play in supporting the plasticity. Here, we create a biophysically detailed model of the BLA circuit to show that several classes of interneurons (PV, SOM, and VIP) in the BLA can be critically involved in producing the rhythms; these rhythms promote the formation of a dedicated fear circuit shaped through spike-timing-dependent plasticity. Each class of interneurons is necessary for the plasticity. We find that the low theta rhythm is a biomarker of successful fear conditioning. The model makes use of interneurons commonly found in the cortex and, hence, may apply to a wide variety of associative learning situations.

    1. Neuroscience
    Bharath Krishnan, Noah Cowan
    Insight

    Mice can generate a cognitive map of an environment based on self-motion signals when there is a fixed association between their starting point and the location of their goal.