Cortico-hippocampal network connections support the multidimensional quality of episodic memory

  1. Rose A Cooper  Is a corresponding author
  2. Maureen Ritchey
  1. Boston College, United States

Abstract

Episodic memories reflect a bound representation of multimodal features that can be reinstated with varying precision. Yet little is known about how brain networks involved in memory, including the hippocampus and posterior-medial (PM) and anterior-temporal (AT) systems, interact to support the quality and content of recollection. Participants learned color, spatial, and emotion associations of objects, later reconstructing the visual features using a continuous color spectrum and 360-degree panorama scenes. Behaviorally, dependencies in memory were observed for the gist but not precision of event associations. Supporting this integration, hippocampus, AT, and PM regions showed increased connectivity and reduced modularity during retrieval compared to encoding. These inter-network connections tracked a multidimensional, objective measure of memory quality. Moreover, distinct patterns of connectivity tracked item color and spatial memory precision. These findings demonstrate how hippocampal-cortical connections reconfigure during episodic retrieval, and how such dynamic interactions might flexibly support the multidimensional quality of remembered events.

Data availability

Data and code have been made available via GitHub: https://github.com/memobc/paper-orbitfmri

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Rose A Cooper

    Department of Psychology, Boston College, Chestnut Hill, United States
    For correspondence
    rose.cooper@bc.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1521-8371
  2. Maureen Ritchey

    Department of Psychology, Boston College, Chestnut Hill, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5957-3642

Funding

National Institutes of Health (R00MH103401)

  • Maureen Ritchey

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Human subjects: Informed consent was obtained from all participants prior to the experiment. Procedures were approved by the Boston College Institutional Review Board (17.026).

Reviewing Editor

  1. Muireann Irish, University of Sydney, Australia

Publication history

  1. Received: January 28, 2019
  2. Accepted: March 22, 2019
  3. Accepted Manuscript published: March 22, 2019 (version 1)
  4. Version of Record published: April 5, 2019 (version 2)

Copyright

© 2019, Cooper & Ritchey

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.

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  1. Rose A Cooper
  2. Maureen Ritchey
(2019)
Cortico-hippocampal network connections support the multidimensional quality of episodic memory
eLife 8:e45591.
https://doi.org/10.7554/eLife.45591
  1. Further reading

Further reading

    1. Developmental Biology
    2. Neuroscience
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    Research Article Updated

    Defining the origin of neuronal diversity is a major challenge in developmental neurobiology. The Drosophila visual system is an excellent paradigm to study how cellular diversity is generated. Photoreceptors from the eye disc grow their axons into the optic lobe and secrete Hedgehog (Hh) to induce the lamina, such that for every unit eye there is a corresponding lamina unit made up of post-mitotic precursors stacked into columns. Each differentiated column contains five lamina neuron types (L1-L5), making it the simplest neuropil in the optic lobe, yet how this diversity is generated was unknown. Here, we found that Hh pathway activity is graded along the distal-proximal axis of lamina columns, and further determined that this gradient in pathway activity arises from a gradient of Hh ligand. We manipulated Hh pathway activity cell autonomously in lamina precursors and non-cell autonomously by inactivating the Hh ligand and by knocking it down in photoreceptors. These manipulations showed that different thresholds of activity specify unique cell identities, with more proximal cell types specified in response to progressively lower Hh levels. Thus, our data establish that Hh acts as a morphogen to pattern the lamina. Although this is the first such report during Drosophila nervous system development, our work uncovers a remarkable similarity with the vertebrate neural tube, which is patterned by Sonic Hh. Altogether, we show that differentiating neurons can regulate the neuronal diversity of their distant target fields through morphogen gradients.

    1. Developmental Biology
    2. Neuroscience
    Anadika R Prasad, Inês Lago-Baldaia ... Vilaiwan M Fernandes
    Research Article Updated

    Neural circuit formation and function require that diverse neurons are specified in appropriate numbers. Known strategies for controlling neuronal numbers involve regulating either cell proliferation or survival. We used the Drosophila visual system to probe how neuronal numbers are set. Photoreceptors from the eye-disc induce their target field, the lamina, such that for every unit eye there is a corresponding lamina unit (column). Although each column initially contains ~6 post-mitotic lamina precursors, only 5 differentiate into neurons, called L1-L5; the ‘extra’ precursor, which is invariantly positioned above the L5 neuron in each column, undergoes apoptosis. Here, we showed that a glial population called the outer chiasm giant glia (xgO), which resides below the lamina, secretes multiple ligands to induce L5 differentiation in response to epidermal growth factor (EGF) from photoreceptors. By forcing neuronal differentiation in the lamina, we uncovered that though fated to die, the ‘extra’ precursor is specified as an L5. Therefore, two precursors are specified as L5s but only one differentiates during normal development. We found that the row of precursors nearest to xgO differentiate into L5s and, in turn, antagonise differentiation signalling to prevent the ‘extra’ precursors from differentiating, resulting in their death. Thus, an intricate interplay of glial signals and feedback from differentiating neurons defines an invariant and stereotyped pattern of neuronal differentiation and programmed cell death to ensure that lamina columns each contain exactly one L5 neuron.