Low excitatory innervation balances high intrinsic excitability of immature dentate neurons

Dieni, Cristina V.; Panichi, Roberto; Aimone, James B.; Kuo, Chay T.; Wadiche, Jacques I.; Overstreet-Wadiche, Linda

doi:10.1038/ncomms11313

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

Journal Article · Wed Apr 20 00:00:00 EDT 2016 · Nature Communications

DOI: https://doi.org/10.1038/ncomms11313 · OSTI ID:1249080

Dieni, Cristina V. ^[1]; Panichi, Roberto ^[2]; Aimone, James B. ^[3]; Kuo, Chay T. ^[4]; Wadiche, Jacques I. ^[5]; Overstreet-Wadiche, Linda ^[5]

Univ. of Alabama, Birmingham, AL (United States); Univ. of Perugia, Perugia (Italy)
Univ. of Perugia, Perugia (Italy)
Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)
Duke Univ. School of Medicine, Durham, NC (United States)
Univ. of Alabama, Birmingham, AL (United States)

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.

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Research Organization:: Sandia National Laboratories (SNL-NM), Albuquerque, NM (United States)

Sponsoring Organization:: USDOE National Nuclear Security Administration (NNSA)

Grant/Contract Number:: AC04-94AL85000

OSTI ID:: 1249080

Report Number(s):: SAND--2016-2583J; ncomms11313

Journal Information:: Nature Communications, Journal Name: Nature Communications Vol. 7; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Pattern separation of spiketrains in hippocampal neurons Madar, Antoine D.; Ewell, Laura A.; Jones, Mathew V. https://doi.org/10.1101/107706	posted_content	January 2019
A pool of postnatally-generated interneurons persists in an immature stage in the olfactory bulb Benito, Nuria; Gaborieau, Elodie; Sanz Diez, Alvaro The Journal of Neuroscience https://doi.org/10.1101/299511	journal	April 2018
Mature dentate granule cells show different intrinsic properties depending on the behavioral context of their activation Peret, Angélique; Pléau, Claire; Pearlstein, Edouard BioRxiv https://doi.org/10.1101/309906	posted_content	September 2019
Temporal pattern separation in hippocampal neurons through multiplexed neural codes Madar, Antoine D.; Ewell, Laura A.; Jones, Mathew V. PLOS Computational Biology https://doi.org/10.1101/421479	journal	January 2019
Ion-channel regulation of response decorrelation in a multi-scale model of the dentate gyrus Mishra, Poonam; Narayanan, Rishikesh Current Research in Neurobiology https://doi.org/10.1101/720078	journal	July 2019
Multifaceted circuit functions of adult-born neurons Dieni, Cristina V.; Gonzalez, Jose Carlos; Overstreet-Wadiche, Linda F1000Research, Vol. 8 https://doi.org/10.12688/f1000research.20642.1	journal	January 2019
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Development of Depotentiation in Adult-Born Dentate Granule Cells Tao, Xiaoqing; Sun, Ning; Mu, Yangling Frontiers in Cell and Developmental Biology, Vol. 7 https://doi.org/10.3389/fcell.2019.00236	journal	October 2019
Adult Hippocampal Neurogenesis: Regulation and Possible Functional and Clinical Correlates Baptista, Pedro; Andrade, José P. Frontiers in Neuroanatomy, Vol. 12 https://doi.org/10.3389/fnana.2018.00044	journal	June 2018
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Silent synapses generate sparse and orthogonal action potential firing in adult-born hippocampal granule cells Li, Liyi; Sultan, Sébastien; Heigele, Stefanie eLife, Vol. 6 https://doi.org/10.7554/elife.23612	journal	August 2017
Dendritic spikes in hippocampal granule cells are necessary for long-term potentiation at the perforant path synapse Kim, Sooyun; Kim, Yoonsub; Lee, Suk-Ho eLife, Vol. 7 https://doi.org/10.7554/elife.35269	journal	March 2018

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