NMDA spikes mediate amplification of inputs in the rat piriform cortex

  1. Amit Kumar
  2. Oded Schiff
  3. Edi Barkai
  4. Bartlett W Mel  Is a corresponding author
  5. Alon Poleg-Polsky  Is a corresponding author
  6. Jackie Schiller  Is a corresponding author
  1. Technion-Israel Institute of Technology, Israel
  2. University of Haifa, Israel
  3. University of Southern California, United States
  4. University of Colorado School of Medicine, United States

Abstract

The piriform cortex (PCx) receives direct input from the olfactory bulb (OB) and is the brain's main station for odor recognition and memory. The transformation of the odor code from OB to PCx is profound: mitral and tufted cells in olfactory glomeruli respond to individual odorant molecules, whereas pyramidal neurons (PNs) in the PCx responds to multiple, apparently random combinations of activated glomeruli. How these 'discontinuous' receptive fields are formed from OB inputs remains unknown. Counter to the prevailing view that olfactory PNs sum their inputs passively, we show for the first time that NMDA spikes within individual dendrites can both amplify OB inputs and impose combination selectivity upon them, while their ability to compartmentalize voltage signals allows different dendrites to represent different odorant combinations. Thus, the 2-layer integrative behavior of olfactory PN dendrites provides a parsimonious account for the nonlinear remapping of the odor code from bulb to cortex.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Amit Kumar

    Department of Physiology, Technion-Israel Institute of Technology, Haifa, Israel
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0674-3641
  2. Oded Schiff

    Department of Physiology, Technion-Israel Institute of Technology, Haifa, Israel
    Competing interests
    The authors declare that no competing interests exist.
  3. Edi Barkai

    Department of Neurobiology, University of Haifa, Haifa, Israel
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7325-4269
  4. Bartlett W Mel

    Biomedical Engineering Department, University of Southern California, Los Angeles, United States
    For correspondence
    mel@usc.edu
    Competing interests
    The authors declare that no competing interests exist.
  5. Alon Poleg-Polsky

    Department of Physiology and Biophysics, University of Colorado School of Medicine, Aurora, United States
    For correspondence
    ALON.POLEG-POLSKY@UCDENVER.EDU
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1327-5129
  6. Jackie Schiller

    Department of Physiology, Technion-Israel Institute of Technology, Haifa, Israel
    For correspondence
    jackie@technion.ac.il
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9182-7166

Funding

Israeli Science Foundation

  • Jackie Schiller

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

Reviewing Editor

  1. Naoshige Uchida, Harvard University, United States

Ethics

Animal experimentation: All animal procedures were in accordance with guidelines established by the NIH on the care and use of animals in research and were confirmed by the Technion Institutional Animal Care and Use Committee (IL-012-01-18, valid until 10/4/2022).

Version history

  1. Received: May 18, 2018
  2. Accepted: December 20, 2018
  3. Accepted Manuscript published: December 21, 2018 (version 1)
  4. Version of Record published: January 15, 2019 (version 2)

Copyright

© 2018, Kumar 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

  • 2,278
    Page views
  • 439
    Downloads
  • 23
    Citations

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

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. Amit Kumar
  2. Oded Schiff
  3. Edi Barkai
  4. Bartlett W Mel
  5. Alon Poleg-Polsky
  6. Jackie Schiller
(2018)
NMDA spikes mediate amplification of inputs in the rat piriform cortex
eLife 7:e38446.
https://doi.org/10.7554/eLife.38446

Share this article

https://doi.org/10.7554/eLife.38446

Further reading

    1. Neuroscience
    Kiwamu Kudo, Kamalini G Ranasinghe ... Srikantan S Nagarajan
    Research Article

    Alzheimer’s disease (AD) is characterized by the accumulation of amyloid-β and misfolded tau proteins causing synaptic dysfunction, and progressive neurodegeneration and cognitive decline. Altered neural oscillations have been consistently demonstrated in AD. However, the trajectories of abnormal neural oscillations in AD progression and their relationship to neurodegeneration and cognitive decline are unknown. Here, we deployed robust event-based sequencing models (EBMs) to investigate the trajectories of long-range and local neural synchrony across AD stages, estimated from resting-state magnetoencephalography. The increases in neural synchrony in the delta-theta band and the decreases in the alpha and beta bands showed progressive changes throughout the stages of the EBM. Decreases in alpha and beta band synchrony preceded both neurodegeneration and cognitive decline, indicating that frequency-specific neuronal synchrony abnormalities are early manifestations of AD pathophysiology. The long-range synchrony effects were greater than the local synchrony, indicating a greater sensitivity of connectivity metrics involving multiple regions of the brain. These results demonstrate the evolution of functional neuronal deficits along the sequence of AD progression.

    1. Medicine
    2. Neuroscience
    Luisa Fassi, Shachar Hochman ... Roi Cohen Kadosh
    Research Article

    In recent years, there has been debate about the effectiveness of treatments from different fields, such as neurostimulation, neurofeedback, brain training, and pharmacotherapy. This debate has been fuelled by contradictory and nuanced experimental findings. Notably, the effectiveness of a given treatment is commonly evaluated by comparing the effect of the active treatment versus the placebo on human health and/or behaviour. However, this approach neglects the individual’s subjective experience of the type of treatment she or he received in establishing treatment efficacy. Here, we show that individual differences in subjective treatment - the thought of receiving the active or placebo condition during an experiment - can explain variability in outcomes better than the actual treatment. We analysed four independent datasets (N = 387 participants), including clinical patients and healthy adults from different age groups who were exposed to different neurostimulation treatments (transcranial magnetic stimulation: Studies 1 and 2; transcranial direct current stimulation: Studies 3 and 4). Our findings show that the inclusion of subjective treatment can provide a better model fit either alone or in interaction with objective treatment (defined as the condition to which participants are assigned in the experiment). These results demonstrate the significant contribution of subjective experience in explaining the variability of clinical, cognitive, and behavioural outcomes. We advocate for existing and future studies in clinical and non-clinical research to start accounting for participants’ subjective beliefs and their interplay with objective treatment when assessing the efficacy of treatments. This approach will be crucial in providing a more accurate estimation of the treatment effect and its source, allowing the development of effective and reproducible interventions.