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Title: Low excitatory innervation balances high intrinsic excitability of immature dentate neurons

Abstract

Persistent neurogenesis in the dentate gyrus produces immature neurons with high intrinsic excitability and low levels of inhibition that are predicted to be more broadly responsive to afferent activity than mature neurons. Mounting evidence suggests that these immature neurons are necessary for generating distinct neural representations of similar contexts, but it is unclear how broadly responsive neurons help distinguish between similar patterns of afferent activity. Here we show that stimulation of the entorhinal cortex in mouse brain slices paradoxically generates spiking of mature neurons in the absence of immature neuron spiking. Immature neurons with high intrinsic excitability fail to spike due to insufficient excitatory drive that results from low innervation rather than silent synapses or low release probability. Here, our results suggest that low synaptic connectivity prevents immature neurons from responding broadly to cortical activity, potentially enabling excitable immature neurons to contribute to sparse and orthogonal dentate representations.

Authors:
 [1];  [2];  [3];  [4];  [5];  [5]
  1. Univ. of Alabama, Birmingham, AL (United States); Univ. of Perugia, Perugia (Italy)
  2. Univ. of Perugia, Perugia (Italy)
  3. Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)
  4. Duke Univ. School of Medicine, Durham, NC (United States)
  5. Univ. of Alabama, Birmingham, AL (United States)
Publication Date:
Research Org.:
Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)
Sponsoring Org.:
USDOE National Nuclear Security Administration (NNSA)
OSTI Identifier:
1249080
Report Number(s):
SAND-2016-2583J
Journal ID: ISSN 2041-1723; ncomms11313
Grant/Contract Number:  
AC04-94AL85000
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; biological sciences; neuroscience

Citation Formats

Dieni, Cristina V., Panichi, Roberto, Aimone, James B., Kuo, Chay T., Wadiche, Jacques I., and Overstreet-Wadiche, Linda. Low excitatory innervation balances high intrinsic excitability of immature dentate neurons. United States: N. p., 2016. Web. doi:10.1038/ncomms11313.
Dieni, Cristina V., Panichi, Roberto, Aimone, James B., Kuo, Chay T., Wadiche, Jacques I., & Overstreet-Wadiche, Linda. Low excitatory innervation balances high intrinsic excitability of immature dentate neurons. United States. https://doi.org/10.1038/ncomms11313
Dieni, Cristina V., Panichi, Roberto, Aimone, James B., Kuo, Chay T., Wadiche, Jacques I., and Overstreet-Wadiche, Linda. Wed . "Low excitatory innervation balances high intrinsic excitability of immature dentate neurons". United States. https://doi.org/10.1038/ncomms11313. https://www.osti.gov/servlets/purl/1249080.
@article{osti_1249080,
title = {Low excitatory innervation balances high intrinsic excitability of immature dentate neurons},
author = {Dieni, Cristina V. and Panichi, Roberto and Aimone, James B. and Kuo, Chay T. and Wadiche, Jacques I. and Overstreet-Wadiche, Linda},
abstractNote = {Persistent neurogenesis in the dentate gyrus produces immature neurons with high intrinsic excitability and low levels of inhibition that are predicted to be more broadly responsive to afferent activity than mature neurons. Mounting evidence suggests that these immature neurons are necessary for generating distinct neural representations of similar contexts, but it is unclear how broadly responsive neurons help distinguish between similar patterns of afferent activity. Here we show that stimulation of the entorhinal cortex in mouse brain slices paradoxically generates spiking of mature neurons in the absence of immature neuron spiking. Immature neurons with high intrinsic excitability fail to spike due to insufficient excitatory drive that results from low innervation rather than silent synapses or low release probability. Here, our results suggest that low synaptic connectivity prevents immature neurons from responding broadly to cortical activity, potentially enabling excitable immature neurons to contribute to sparse and orthogonal dentate representations.},
doi = {10.1038/ncomms11313},
url = {https://www.osti.gov/biblio/1249080}, journal = {Nature Communications},
issn = {2041-1723},
number = ,
volume = 7,
place = {United States},
year = {2016},
month = {4}
}

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Free Publicly Available Full Text
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Cited by: 8 works
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    Works referencing / citing this record:

    Restorative effects of human neural stem cell grafts on the primate spinal cord
    journal, February 2018


    Development of Depotentiation in Adult-Born Dentate Granule Cells
    journal, October 2019


    Modeling Contextual Modulation of Memory Associations in the Hippocampus
    journal, November 2018


    Modulation of Aversive Memory by Adult Hippocampal Neurogenesis
    journal, May 2017


    Restorative effects of human neural stem cell grafts on the primate spinal cord
    journal, February 2018


    Development of Depotentiation in Adult-Born Dentate Granule Cells
    journal, October 2019


    Modeling Contextual Modulation of Memory Associations in the Hippocampus
    journal, November 2018


    Pten loss results in inappropriate excitatory connectivity
    journal, April 2019