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.

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.

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

  • 2,143
    views
  • 261
    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. Evolutionary Biology
    2. Neuroscience
    Gregor Belušič
    Insight

    The first complete 3D reconstruction of the compound eye of a minute wasp species sheds light on the nuts and bolts of size reduction.

    1. Neuroscience
    Li Shen, Shuo Li ... Yi Jiang
    Research Article

    When observing others’ behaviors, we continuously integrate their movements with the corresponding sounds to enhance perception and develop adaptive responses. However, how the human brain integrates these complex audiovisual cues based on their natural temporal correspondence remains unclear. Using electroencephalogram (EEG), we demonstrated that rhythmic cortical activity tracked the hierarchical rhythmic structures in audiovisually congruent human walking movements and footstep sounds. Remarkably, the cortical tracking effects exhibit distinct multisensory integration modes at two temporal scales: an additive mode in a lower-order, narrower temporal integration window (step cycle) and a super-additive enhancement in a higher-order, broader temporal window (gait cycle). Furthermore, while neural responses at the lower-order timescale reflect a domain-general audiovisual integration process, cortical tracking at the higher-order timescale is exclusively engaged in the integration of biological motion cues. In addition, only this higher-order, domain-specific cortical tracking effect correlates with individuals’ autistic traits, highlighting its potential as a neural marker for autism spectrum disorder. These findings unveil the multifaceted mechanism whereby rhythmic cortical activity supports the multisensory integration of human motion, shedding light on how neural coding of hierarchical temporal structures orchestrates the processing of complex, natural stimuli across multiple timescales.