Phasic and tonic neuron ensemble codes for stimulus-environment conjunctions in the lateral entorhinal cortex

  1. Maryna Pilkiw
  2. Nathan Insel
  3. Younghua Cui
  4. Caitlin Finney
  5. Mark D Morrissey
  6. Kaori Takehara-Nishiuchi  Is a corresponding author
  1. University of Toronto, Canada
  2. University of Montana, United States
  3. University or Toronto, Canada

Abstract

The lateral entorhinal cortex (LEC) is thought to bind sensory events with the environment where they took place. To compare the relative influence of transient events and temporally stable environmental stimuli on the firing of LEC cells, we recorded neuron spiking patterns in the region during blocks of a trace eyeblink conditioning paradigm performed in two environments and with different conditioning stimuli. Firing rates of some neurons were phasically selective for conditioned stimuli in a way that depended on which room the rat was in; nearly all neurons were tonically selective for environments in a way that depended on which stimuli had been presented in those environments. As rats moved from one environment to another, tonic neuron ensemble activity exhibited prospective information about the conditioned stimulus associated with the environment. Thus, the LEC formed phasic and tonic codes for event-environment associations, thereby accurately differentiating multiple experiences with overlapping features.

Article and author information

Author details

  1. Maryna Pilkiw

    Department of Cell and Systems Biology, University of Toronto, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1200-1708
  2. Nathan Insel

    Department of Psychology, University of Montana, Missoula, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Younghua Cui

    Department of Psychology, University of Toronto, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. Caitlin Finney

    Department of Psychology, University of Toronto, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Mark D Morrissey

    Department of Psychology, University or Toronto, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  6. Kaori Takehara-Nishiuchi

    Department of Cell and Systems Biology, University of Toronto, Toronto, Canada
    For correspondence
    takehara@psych.utoronto.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7282-7838

Funding

Natural Sciences and Engineering Research Council of Canada (RGPIN-2015-05458)

  • Kaori Takehara-Nishiuchi

Canadian Institutes of Health Research (MOP-133693)

  • Kaori Takehara-Nishiuchi

Canada Foundation for Innovation (25026)

  • Kaori Takehara-Nishiuchi

Natural Sciences and Engineering Research Council of Canada (396157093)

  • Maryna Pilkiw

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

Ethics

Animal experimentation: All surgical and experimental procedures were approved by the Animal Care and Use Committee at the University of Toronto (protocol number: 20011400).

Reviewing Editor

  1. Geoffrey Schoenbaum, National Institutes of Health, United States

Publication history

  1. Received: May 13, 2017
  2. Accepted: July 5, 2017
  3. Accepted Manuscript published: July 6, 2017 (version 1)
  4. Version of Record published: July 31, 2017 (version 2)

Copyright

© 2017, Pilkiw 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

  • 2,451
    Page views
  • 338
    Downloads
  • 15
    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. Maryna Pilkiw
  2. Nathan Insel
  3. Younghua Cui
  4. Caitlin Finney
  5. Mark D Morrissey
  6. Kaori Takehara-Nishiuchi
(2017)
Phasic and tonic neuron ensemble codes for stimulus-environment conjunctions in the lateral entorhinal cortex
eLife 6:e28611.
https://doi.org/10.7554/eLife.28611

Further reading

    1. Developmental Biology
    2. Neuroscience
    Ashtyn T Wiltbank et al.
    Research Article

    Efficient neurotransmission is essential for organism survival and is enhanced by myelination. However, the genes that regulate myelin and myelinating glial cell development have not been fully characterized. Data from our lab and others demonstrates that cd59, which encodes for a small GPI-anchored glycoprotein, is highly expressed in developing zebrafish, rodent, and human oligodendrocytes (OLs) and Schwann cells (SCs), and that patients with CD59 dysfunction develop neurological dysfunction during early childhood. Yet, the function of Cd59 in the developing nervous system is currently undefined. In this study, we demonstrate that cd59 is expressed in a subset of developing SCs. Using cd59 mutant zebrafish, we show that developing SCs proliferate excessively and nerves may have reduced myelin volume, altered myelin ultrastructure, and perturbed node of Ranvier assembly. Finally, we demonstrate that complement activity is elevated in cd59 mutants and that inhibiting inflammation restores SC proliferation, myelin volume, and nodes of Ranvier to wildtype levels. Together, this work identifies Cd59 and developmental inflammation as key players in myelinating glial cell development, highlighting the collaboration between glia and the innate immune system to ensure normal neural development.

    1. Neuroscience
    Arefeh Sherafati et al.
    Research Article Updated

    Cochlear implants are neuroprosthetic devices that can restore hearing in people with severe to profound hearing loss by electrically stimulating the auditory nerve. Because of physical limitations on the precision of this stimulation, the acoustic information delivered by a cochlear implant does not convey the same level of acoustic detail as that conveyed by normal hearing. As a result, speech understanding in listeners with cochlear implants is typically poorer and more effortful than in listeners with normal hearing. The brain networks supporting speech understanding in listeners with cochlear implants are not well understood, partly due to difficulties obtaining functional neuroimaging data in this population. In the current study, we assessed the brain regions supporting spoken word understanding in adult listeners with right unilateral cochlear implants (n=20) and matched controls (n=18) using high-density diffuse optical tomography (HD-DOT), a quiet and non-invasive imaging modality with spatial resolution comparable to that of functional MRI. We found that while listening to spoken words in quiet, listeners with cochlear implants showed greater activity in the left prefrontal cortex than listeners with normal hearing, specifically in a region engaged in a separate spatial working memory task. These results suggest that listeners with cochlear implants require greater cognitive processing during speech understanding than listeners with normal hearing, supported by compensatory recruitment of the left prefrontal cortex.