1. Neuroscience
Download icon

Rat anterior cingulate cortex recalls features of remote reward locations after disfavoured reinforcements

Research Article
  • Cited 27
  • Views 2,699
  • Annotations
Cite this article as: eLife 2018;7:e29793 doi: 10.7554/eLife.29793

Abstract

The anterior cingulate cortex (ACC) encodes information supporting mnemonic and cognitive processes. We show here that a rat's position can be decoded with high spatiotemporal resolution from ACC activity. ACC neurons encoded the current state of the animal and task, except for brief excursions that sometimes occurred at target feeders. During excursions, the decoded position became more similar to a remote target feeder than the rat's physical position. Excursions recruited activation of neurons encoding choice and reward, and the likelihood of excursions at a feeder was inversely correlated with feeder preference. These data suggest that the excursion phenomenon was related to evaluating real or fictive choice outcomes, particularly after disfavoured reinforcements. We propose that the multiplexing of position with choice-related information forms a mental model isomorphic with the task space, which can be mentally navigated via excursions to recall multimodal information about the utility of remote locations.

Data availability

The pre-processed data used for the paper and the computer codes for the artificial neural network are available for download at a publicly accessible repository (https://github.com/mashhoori/ACC-Recalls-Features-of-Remote-Reward-Locations).

Article and author information

Author details

  1. Ali Mashhoori

    Canadian Centre for Behavioural Neuroscience, University of Lethbridge, Lethbridge, Canada
    Competing interests
    The authors declare that no competing interests exist.
  2. Saeedeh Hashemniayetorshizi

    Canadian Centre for Behavioural Neuroscience, University of Lethbridge, Lethbridge, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Bruce L McNaughton

    Canadian Centre for Behavioural Neuroscience, University of Lethbridge, Lethbridge, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. David Euston

    Canadian Centre for Behavioural Neuroscience, University of Lethbridge, Lethbridge, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Aaron J Gruber

    Canadian Centre for Behavioural Neuroscience, University of Lethbridge, Lethbridge, Canada
    For correspondence
    aaron.gruber@uleth.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2700-5429

Funding

Alberta Innovates - Health Solutions

  • Bruce L McNaughton
  • David Euston
  • Aaron J Gruber

Natural Sciences and Engineering Research Council of Canada

  • Saeedeh Hashemniayetorshizi
  • Bruce L McNaughton
  • David Euston
  • Aaron J Gruber

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 procedures were approved by the university's animal welfare committee (Protocol #1512) in accordance with the Canadian Council on Animal Care.

Reviewing Editor

  1. Timothy E Behrens, University of Oxford, United Kingdom

Publication history

  1. Received: June 21, 2017
  2. Accepted: April 4, 2018
  3. Accepted Manuscript published: April 17, 2018 (version 1)
  4. Version of Record published: May 2, 2018 (version 2)
  5. Version of Record updated: September 9, 2021 (version 3)

Copyright

© 2018, Mashhoori 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

  • 2,699
    Page views
  • 354
    Downloads
  • 27
    Citations

Article citation count generated by polling the highest count across the following sources: Scopus, Crossref, PubMed Central.

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)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Neuroscience
    Gordon H Petty et al.
    Research Article

    Neocortical sensory areas have associated primary and secondary thalamic nuclei. While primary nuclei transmit sensory information to cortex, secondary nuclei remain poorly understood. We recorded juxtasomally from secondary somatosensory (POm) and visual (LP) nuclei of awake mice while tracking whisking and pupil size. POm activity correlated with whisking, but not precise whisker kinematics. This coarse movement modulation persisted after facial paralysis and thus was not due to sensory reafference. This phenomenon also continued during optogenetic silencing of somatosensory and motor cortex and after lesion of superior colliculus, ruling out a motor efference copy mechanism. Whisking and pupil dilation were strongly correlated, possibly reflecting arousal. Indeed LP, which is not part of the whisker system, tracked whisking equally well, further indicating that POm activity does not encode whisker movement per se. The semblance of movement-related activity is likely instead a global effect of arousal on both nuclei. We conclude that secondary thalamus monitors behavioral state, rather than movement, and may exist to alter cortical activity accordingly.

    1. Neuroscience
    Jorrit S Montijn et al.
    Tools and Resources Updated

    Neurophysiological studies depend on a reliable quantification of whether and when a neuron responds to stimulation. Simple methods to determine responsiveness require arbitrary parameter choices, such as binning size, while more advanced model-based methods require fitting and hyperparameter tuning. These parameter choices can change the results, which invites bad statistical practice and reduces the replicability. New recording techniques that yield increasingly large numbers of cells would benefit from a test for cell-inclusion that requires no manual curation. Here, we present the parameter-free ZETA-test, which outperforms t-tests, ANOVAs, and renewal-process-based methods by including more cells at a similar false-positive rate. We show that our procedure works across brain regions and recording techniques, including calcium imaging and Neuropixels data. Furthermore, in illustration of the method, we show in mouse visual cortex that (1) visuomotor-mismatch and spatial location are encoded by different neuronal subpopulations and (2) optogenetic stimulation of VIP cells leads to early inhibition and subsequent disinhibition.