Differential inhibition onto developing and mature granule cells generates high-frequency filters with variable gain

  1. María Belén Pardi
  2. Mora Belén Ogando
  3. Alejandro F Schinder
  4. Antonia Marin-Burgin  Is a corresponding author
  1. Instituto de Investigación en Biomedicina de Buenos Aires - CONICET - Partner Institute of the Max Planck Society, Argentina
  2. Leloir Institute -CONICET, Argentina

Abstract

Adult hippocampal neurogenesis provides the dentate gyrus with heterogeneous populations of granule cells (GC) originated at different times. The contribution of these cells to information encoding is under current investigation. Here we show that incoming spike trains activate different populations of GC determined by the stimulation frequency and GC age. Immature GC respond to a wider range of stimulus frequencies, whereas mature GC are less responsive at high frequencies. This difference is dictated by feed forward inhibition, which restricts mature GC activation. Yet, the stronger inhibition of mature GC results in a higher temporal fidelity compared to that of immature GC. Thus, hippocampal inputs activate two populations of neurons with variable frequency filters: immature cells, with wide‐range responses, that are reliable transmitters of the incoming frequency, and mature neurons, with narrow frequency response, that are precise at informing the beginning of the stimulus, but with a sparse activity.

Article and author information

Author details

  1. María Belén Pardi

    Instituto de Investigación en Biomedicina de Buenos Aires - CONICET - Partner Institute of the Max Planck Society, Buenos Aires, Argentina
    Competing interests
    The authors declare that no competing interests exist.
  2. Mora Belén Ogando

    Instituto de Investigación en Biomedicina de Buenos Aires - CONICET - Partner Institute of the Max Planck Society, Buenos Aires, Argentina
    Competing interests
    The authors declare that no competing interests exist.
  3. Alejandro F Schinder

    Laboratory of Neuronal Plasticity, Leloir Institute -CONICET, Buenos Aires, Argentina
    Competing interests
    The authors declare that no competing interests exist.
  4. Antonia Marin-Burgin

    Instituto de Investigación en Biomedicina de Buenos Aires - CONICET - Partner Institute of the Max Planck Society, Buenos Aires, Argentina
    For correspondence
    aburgin@ibioba-mpsp-conicet.gov.ar
    Competing interests
    The authors declare that no competing interests exist.

Ethics

Animal experimentation: Experimental protocols were approved by the Institutional Animal Care and Use Committee of the Fundación Instituto Leloir (Protocols Number 2009 08 37 and 64/2015, IACUC, Leloir Institute Foundation) according to the Principles for Biomedical Research involving animals of the Council for International Organizations for Medical Sciences and provisions stated in the Guide for the Care and Use of Laboratory Animals.

Reviewing Editor

  1. Marlene Bartos, Albert-Ludwigs-Universität Freiburg, Germany

Version history

  1. Received: May 16, 2015
  2. Accepted: July 10, 2015
  3. Accepted Manuscript published: July 11, 2015 (version 1)
  4. Version of Record published: July 31, 2015 (version 2)

Copyright

© 2015, Pardi 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

  • 1,497
    Page views
  • 379
    Downloads
  • 20
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.

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. María Belén Pardi
  2. Mora Belén Ogando
  3. Alejandro F Schinder
  4. Antonia Marin-Burgin
(2015)
Differential inhibition onto developing and mature granule cells generates high-frequency filters with variable gain
eLife 4:e08764.
https://doi.org/10.7554/eLife.08764

Further reading

    1. Neuroscience
    Stijn A Nuiten, Jan Willem de Gee ... Simon van Gaal
    Research Article

    Perceptual decisions about sensory input are influenced by fluctuations in ongoing neural activity, most prominently driven by attention and neuromodulator systems. It is currently unknown if neuromodulator activity and attention differentially modulate perceptual decision-making and/or whether neuromodulatory systems in fact control attentional processes. To investigate the effects of two distinct neuromodulatory systems and spatial attention on perceptual decisions, we pharmacologically elevated cholinergic (through donepezil) and catecholaminergic (through atomoxetine) levels in humans performing a visuo-spatial attention task, while we measured electroencephalography (EEG). Both attention and catecholaminergic enhancement improved decision-making at the behavioral and algorithmic level, as reflected in increased perceptual sensitivity and the modulation of the drift rate parameter derived from drift diffusion modeling. Univariate analyses of EEG data time-locked to the attentional cue, the target stimulus, and the motor response further revealed that attention and catecholaminergic enhancement both modulated pre-stimulus cortical excitability, cue- and stimulus-evoked sensory activity, as well as parietal evidence accumulation signals. Interestingly, we observed both similar, unique, and interactive effects of attention and catecholaminergic neuromodulation on these behavioral, algorithmic, and neural markers of the decision-making process. Thereby, this study reveals an intricate relationship between attentional and catecholaminergic systems and advances our understanding about how these systems jointly shape various stages of perceptual decision-making.

    1. Neuroscience
    Manfred G Kitzbichler, Daniel Martins ... Neil A Harrison
    Research Article Updated

    The relationship between obesity and human brain structure is incompletely understood. Using diffusion-weighted MRI from ∼30,000 UK Biobank participants, we test the hypothesis that obesity (waist-to-hip ratio, WHR) is associated with regional differences in two micro-structural MRI metrics: isotropic volume fraction (ISOVF), an index of free water, and intra-cellular volume fraction (ICVF), an index of neurite density. We observed significant associations with obesity in two coupled but distinct brain systems: a prefrontal/temporal/striatal system associated with ISOVF and a medial temporal/occipital/striatal system associated with ICVF. The ISOVF~WHR system colocated with expression of genes enriched for innate immune functions, decreased glial density, and high mu opioid (MOR) and other neurotransmitter receptor density. Conversely, the ICVF~WHR system co-located with expression of genes enriched for G-protein coupled receptors and decreased density of MOR and other receptors. To test whether these distinct brain phenotypes might differ in terms of their underlying shared genetics or relationship to maps of the inflammatory marker C-reactive Protein (CRP), we estimated the genetic correlations between WHR and ISOVF (rg = 0.026, P = 0.36) and ICVF (rg = 0.112, P < 9×10−4) as well as comparing correlations between WHR maps and equivalent CRP maps for ISOVF and ICVF (P<0.05). These correlational results are consistent with a two-way mechanistic model whereby genetically determined differences in neurite density in the medial temporal system may contribute to obesity, whereas water content in the prefrontal system could reflect a consequence of obesity mediated by innate immune system activation.