Tuning of olfactory cortex ventral tenia tecta neurons to distinct task elements of goal-directed behavior

  1. Kazuki Shiotani
  2. Yuta Tanisumi
  3. Koshi Murata
  4. Junya Hirokawa
  5. Yoshio Sakurai
  6. Hiroyuki Manabe  Is a corresponding author
  1. Graduate School of Brain Science, Doshisha University, Japan
  2. Faculty of Medical Sciences, University of Fukui, Japan
  3. Doshisha University, Japan

Abstract

The ventral tenia tecta (vTT) is a component of the olfactory cortex and receives both bottom-up odor signals and top-down signals. However, the roles of the vTT in odor-coding and integration of inputs are poorly understood. Here, we investigated the involvement of the vTT in these processes by recording the activity from individual vTT neurons during the performance of learned odor-guided reward-directed tasks in mice. We report that individual vTT cells are highly tuned to a specific behavioral epoch of learned tasks, whereby the duration of increased firing correlated with the temporal length of the behavioral epoch. The peak time for increased firing among recorded vTT cells encompassed almost the entire temporal window of the tasks. Collectively, our results indicate that vTT cells are selectively activated during a specific behavioral context and that the function of the vTT changes dynamically in a context-dependent manner during goal-directed behaviors.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.Source data files have been provided for Figure 2, 3, 5 and 6.

Article and author information

Author details

  1. Kazuki Shiotani

    Laboratory of Neural Information, Graduate School of Brain Science, Doshisha University, Kyoto, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5596-5609
  2. Yuta Tanisumi

    Laboratory of Neural Information, Graduate School of Brain Science, Doshisha University, Kyoto, Japan
    Competing interests
    The authors declare that no competing interests exist.
  3. Koshi Murata

    Division of Brain Structure and Function, Faculty of Medical Sciences, University of Fukui, Fukui, Japan
    Competing interests
    The authors declare that no competing interests exist.
  4. Junya Hirokawa

    Graduate School of Brain Science, Graduate School of Brain Science, Doshisha University, Kyotanabe, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1238-5713
  5. Yoshio Sakurai

    Graduate School of Brain Science, Doshisha University, Doshisha University, Kyoto, Japan
    Competing interests
    The authors declare that no competing interests exist.
  6. Hiroyuki Manabe

    Laboratory of Neural Information, Graduate School of Brain Science, Doshisha University, Kyoto, Japan
    For correspondence
    hmanabe@mail.doshisha.ac.jp
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3910-4849

Funding

Japan Society for the Promotion of Science (Grant-in-Aid for JSPS Fellows 18J21358)

  • Kazuki Shiotani

Japan Society for the Promotion of Science (Grant-in-Aid for Challenging Exploratory Research 16K14557)

  • Hiroyuki Manabe

Japan Society for the Promotion of Science (Grant-in-Aid for Scientific Research on Innovative Areas 25135708)

  • Hiroyuki Manabe

Takeda Science Foundation

  • Hiroyuki Manabe

Narishige Neuroscience Research Foundation

  • Hiroyuki Manabe

Japan Society for the Promotion of Science (Grant-in-Aid for Scientific Research(A) 16H02061)

  • Yoshio Sakurai

Japan Society for the Promotion of Science (Grant-in-Aid for Scientific Research on Innovative Areas 18H05088)

  • Yoshio Sakurai

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: Animal experimentation: Animal experiments were approved and performed in accordance with the guidelines for the care and use of laboratory animals established by the Committee for Animal Care (Permit Number: A15089, A16013, A17007, A18011) of Doshisha University. All efforts were made to minimize animal suffering and the number of animals used.

Version history

  1. Received: March 26, 2020
  2. Accepted: August 1, 2020
  3. Accepted Manuscript published: August 4, 2020 (version 1)
  4. Version of Record published: August 12, 2020 (version 2)

Copyright

© 2020, Shiotani 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

  • 2,012
    views
  • 244
    downloads
  • 17
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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. Kazuki Shiotani
  2. Yuta Tanisumi
  3. Koshi Murata
  4. Junya Hirokawa
  5. Yoshio Sakurai
  6. Hiroyuki Manabe
(2020)
Tuning of olfactory cortex ventral tenia tecta neurons to distinct task elements of goal-directed behavior
eLife 9:e57268.
https://doi.org/10.7554/eLife.57268

Share this article

https://doi.org/10.7554/eLife.57268

Further reading

    1. Neuroscience
    Anja T Zai, Anna E Stepien ... Richard HR Hahnloser
    Research Article

    Songbirds’ vocal mastery is impressive, but to what extent is it a result of practice? Can they, based on experienced mismatch with a known target, plan the necessary changes to recover the target in a practice-free manner without intermittently singing? In adult zebra finches, we drive the pitch of a song syllable away from its stable (baseline) variant acquired from a tutor, then we withdraw reinforcement and subsequently deprive them of singing experience by muting or deafening. In this deprived state, birds do not recover their baseline song. However, they revert their songs toward the target by about 1 standard deviation of their recent practice, provided the sensory feedback during the latter signaled a pitch mismatch with the target. Thus, targeted vocal plasticity does not require immediate sensory experience, showing that zebra finches are capable of goal-directed vocal planning.

    1. Neuroscience
    Amanda Chu, Nicholas T Gordon ... Michael A McDannald
    Research Article Updated

    Pavlovian fear conditioning has been extensively used to study the behavioral and neural basis of defensive systems. In a typical procedure, a cue is paired with foot shock, and subsequent cue presentation elicits freezing, a behavior theoretically linked to predator detection. Studies have since shown a fear conditioned cue can elicit locomotion, a behavior that – in addition to jumping, and rearing – is theoretically linked to imminent or occurring predation. A criticism of studies observing fear conditioned cue-elicited locomotion is that responding is non-associative. We gave rats Pavlovian fear discrimination over a baseline of reward seeking. TTL-triggered cameras captured 5 behavior frames/s around cue presentation. Experiment 1 examined the emergence of danger-specific behaviors over fear acquisition. Experiment 2 examined the expression of danger-specific behaviors in fear extinction. In total, we scored 112,000 frames for nine discrete behavior categories. Temporal ethograms show that during acquisition, a fear conditioned cue suppresses reward seeking and elicits freezing, but also elicits locomotion, jumping, and rearing – all of which are maximal when foot shock is imminent. During extinction, a fear conditioned cue most prominently suppresses reward seeking, and elicits locomotion that is timed to shock delivery. The independent expression of these behaviors in both experiments reveals a fear conditioned cue to orchestrate a temporally organized suite of behaviors.