Control of adaptive action selection by secondary motor cortex during flexible visual categorization

  1. Tian-Yi Wang
  2. Jing Liu
  3. Haishan Yao  Is a corresponding author
  1. Institute of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, China

Abstract

Adaptive action selection during stimulus categorization is an important feature of flexible behavior. To examine neural mechanism underlying this process, we trained mice to categorize the spatial frequencies of visual stimuli according to a boundary that changed between blocks of trials in a session. Using a model with a dynamic decision criterion, we found that sensory history was important for adaptive action selection after the switch of boundary. Bilateral inactivation of the secondary motor cortex (M2) impaired adaptive action selection by reducing the behavioral influence of sensory history. Electrophysiological recordings showed that M2 neurons carried more information about upcoming choice and previous sensory stimuli when sensorimotor association was being remapped than when it was stable. Thus, M2 causally contributes to flexible action selection during stimulus categorization, with the representations of upcoming choice and sensory history regulated by the demand to remap stimulus-action association.

Data availability

All data generated or analyzed during this study are available on Dryad https://doi.org/10.5061/dryad.1c59zw3rs. Source data files have been provided for Figures 1-6.

The following data sets were generated

Article and author information

Author details

  1. Tian-Yi Wang

    State Key Laboratory of Neuroscience, Institute of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6488-339X
  2. Jing Liu

    State Key Laboratory of Neuroscience, Institute of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Haishan Yao

    State Key Laboratory of Neuroscience, Institute of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai, China
    For correspondence
    haishanyao@ion.ac.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4974-9197

Funding

Strategic Priority Research Program of Chinese Academy of Sciences (XDB32010200)

  • Haishan Yao

Shanghai Municiple Science and Technology Major Project (2018SHZDZX05)

  • Haishan Yao

National Natural Science Foundation of China (31571079,31771151)

  • Haishan Yao

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 use procedures were approved by the Animal Care and Use Committee at the Institute of Neuroscience, Chinese Academy of Sciences (approval number NA-013-2019), and were in accordance with the guidelines of the Animal Advisory Committee at the Shanghai Institutes for Biological Sciences.

Copyright

© 2020, Wang 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

  • 1,827
    views
  • 263
    downloads
  • 21
    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. Tian-Yi Wang
  2. Jing Liu
  3. Haishan Yao
(2020)
Control of adaptive action selection by secondary motor cortex during flexible visual categorization
eLife 9:e54474.
https://doi.org/10.7554/eLife.54474

Share this article

https://doi.org/10.7554/eLife.54474

Further reading

    1. Developmental Biology
    2. Neuroscience
    Agnik Dasgupta, Caleb C Reagor ... AJ Hudspeth
    Research Article

    In a developing nervous system, axonal arbors often undergo complex rearrangements before neural circuits attain their final innervation topology. In the lateral line sensory system of the zebrafish, developing sensory axons reorganize their terminal arborization patterns to establish precise neural microcircuits around the mechanosensory hair cells. However, a quantitative understanding of the changes in the sensory arbor morphology and the regulators behind the microcircuit assembly remain enigmatic. Here, we report that Semaphorin7A (Sema7A) acts as an important mediator of these processes. Utilizing a semi-automated three-dimensional neurite tracing methodology and computational techniques, we have identified and quantitatively analyzed distinct topological features that shape the network in wild-type and Sema7A loss-of-function mutants. In contrast to those of wild-type animals, the sensory axons in Sema7A mutants display aberrant arborizations with disorganized network topology and diminished contacts to hair cells. Moreover, ectopic expression of a secreted form of Sema7A by non-hair cells induces chemotropic guidance of sensory axons. Our findings propose that Sema7A likely functions both as a juxtracrine and as a secreted cue to pattern neural circuitry during sensory organ development.

    1. Neuroscience
    Eun Joo Kim, Mi-Seon Kong ... Jeansok John Kim
    Research Article

    Pavlovian fear conditioning research suggests that the interaction between the dorsal periaqueductal gray (dPAG) and basolateral amygdala (BLA) acts as a prediction error mechanism in the formation of associative fear memories. However, their roles in responding to naturalistic predatory threats, characterized by less explicit cues and the absence of reiterative trial-and-error learning events, remain unexplored. In this study, we conducted single-unit recordings in rats during an ‘approach food-avoid predator’ task, focusing on the responsiveness of dPAG and BLA neurons to a rapidly approaching robot predator. Optogenetic stimulation of the dPAG triggered fleeing behaviors and increased BLA activity in naive rats. Notably, BLA neurons activated by dPAG stimulation displayed immediate responses to the robot, demonstrating heightened synchronous activity compared to BLA neurons that did not respond to dPAG stimulation. Additionally, the use of anterograde and retrograde tracer injections into the dPAG and BLA, respectively, coupled with c-Fos activation in response to predatory threats, indicates that the midline thalamus may play an intermediary role in innate antipredatory-defensive functioning.