Plasticity of olfactory bulb inputs mediated by dendritic NMDA-spikes in rodent piriform cortex

  1. Amit Kumar
  2. Edi Barkai
  3. Jackie Schiller  Is a corresponding author
  1. Technion-Israel Institute of Technology, Israel
  2. University of Haifa, Israel

Abstract

The piriform cortex (PCx) is essential for learning of odor information. The current view postulates odor learning in the PCx is mainly due to plasticity in intracortical (IC) synapses, while odor information from the olfactory bulb carried via the lateral olfactory tract (LOT) is 'hardwired'. Here we revisit this notion by studying location and pathway dependent plasticity rules. We find that in contrast to the prevailing view, synaptic and optogenetically activated LOT synapses undergo strong and robust long-term potentiation (LTP) mediated by only few local NMDA-spikes delivered at theta frequency, while global spike timing dependent plasticity protocols (STDP) failed to induce LTP in these distal synapses. In contrast, IC synapses in apical and basal dendrites undergo plasticity with both NMDA-spikes and STDP protocols but to a smaller extent compared with LOT synapses. These results are consistent with a self-potentiating mechanism of odor information via NMDA-spikes which can form branch-specific memory traces of odors that can further associate with contextual IC information via STDP mechanisms to provide cognitive and emotional value to odors.

Data availability

The data generated or analysed during this study are included in the manuscript and Supporting files for Figure 1C-G, Figure 2B,D, Figure 3B,D, F-H, Figure 4 B,D, Figure 5B-D, Figure 6 C-D and Figure 7 B-F, are loaded.

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. 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
  3. 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

Israel Science Foundation

  • Jackie Schiller

Prince Center for Neurodegenerative Diseases

  • 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. Katalin Toth, University of Ottawa, Canada

Ethics

Animal experimentation: All animal procedures were done in accordance with guidelines established by NIH on the care and use of animals in research and were confirmed by the Technion Institutional Animal Care and Use Committee (Permit number IL-012-01-18).

Version history

  1. Received: May 14, 2021
  2. Preprint posted: May 25, 2021 (view preprint)
  3. Accepted: October 25, 2021
  4. Accepted Manuscript published: October 26, 2021 (version 1)
  5. Version of Record published: November 8, 2021 (version 2)

Copyright

© 2021, 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

  • 1,197
    Page views
  • 250
    Downloads
  • 7
    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. Edi Barkai
  3. Jackie Schiller
(2021)
Plasticity of olfactory bulb inputs mediated by dendritic NMDA-spikes in rodent piriform cortex
eLife 10:e70383.
https://doi.org/10.7554/eLife.70383

Share this article

https://doi.org/10.7554/eLife.70383

Further reading

    1. Neuroscience
    Songyao Zhang, Tuo Zhang ... Tianming Liu
    Research Article

    Cortical folding is an important feature of primate brains that plays a crucial role in various cognitive and behavioral processes. Extensive research has revealed both similarities and differences in folding morphology and brain function among primates including macaque and human. The folding morphology is the basis of brain function, making cross-species studies on folding morphology important for understanding brain function and species evolution. However, prior studies on cross-species folding morphology mainly focused on partial regions of the cortex instead of the entire brain. Previously, our research defined a whole-brain landmark based on folding morphology: the gyral peak. It was found to exist stably across individuals and ages in both human and macaque brains. Shared and unique gyral peaks in human and macaque are identified in this study, and their similarities and differences in spatial distribution, anatomical morphology, and functional connectivity were also dicussed.

    1. Neuroscience
    Avani Koparkar, Timothy L Warren ... Lena Veit
    Research Article

    Complex skills like speech and dance are composed of ordered sequences of simpler elements, but the neuronal basis for the syntactic ordering of actions is poorly understood. Birdsong is a learned vocal behavior composed of syntactically ordered syllables, controlled in part by the songbird premotor nucleus HVC (proper name). Here, we test whether one of HVC’s recurrent inputs, mMAN (medial magnocellular nucleus of the anterior nidopallium), contributes to sequencing in adult male Bengalese finches (Lonchura striata domestica). Bengalese finch song includes several patterns: (1) chunks, comprising stereotyped syllable sequences; (2) branch points, where a given syllable can be followed probabilistically by multiple syllables; and (3) repeat phrases, where individual syllables are repeated variable numbers of times. We found that following bilateral lesions of mMAN, acoustic structure of syllables remained largely intact, but sequencing became more variable, as evidenced by ‘breaks’ in previously stereotyped chunks, increased uncertainty at branch points, and increased variability in repeat numbers. Our results show that mMAN contributes to the variable sequencing of vocal elements in Bengalese finch song and demonstrate the influence of recurrent projections to HVC. Furthermore, they highlight the utility of species with complex syntax in investigating neuronal control of ordered sequences.