1. Neuroscience
Download icon

Classical conditioning drives learned reward prediction signals in climbing fibers across the lateral cerebellum

  1. William Heffley
  2. Court Hull  Is a corresponding author
  1. Duke University School of Medicine, United States
Research Article
  • Cited 30
  • Views 3,450
  • Annotations
Cite this article as: eLife 2019;8:e46764 doi: 10.7554/eLife.46764

Abstract

Classical models of cerebellar learning posit that climbing fibers operate according to a supervised learning rule to instruct changes in motor output by signaling the occurrence of movement errors. However, cerebellar output is also associated with non-motor behaviors, and recently with modulating reward association pathways in the VTA. To test how the cerebellum processes reward related signals in the same type of classical conditioning behavior typically studied to evaluate reward processing in the VTA and striatum, we have used calcium imaging to visualize instructional signals carried by climbing fibers across the lateral cerebellum in mice before and after learning. We find distinct climbing fiber responses in three lateral cerebellar regions that can each signal reward prediction. These instructional signals are well suited to guide cerebellar learning based on reward expectation and enable a cerebellar contribution to reward driven behaviors, suggesting a broad role for the lateral cerebellum in reward-based learning.

Data availability

Datasets supporting the findings of this study are ~50 GB per experiment, and are therefore available through a request to the corresponding author. Processed data have been provided for each figure, and analysis code has been place in GitHub (https://github.com/Glickfeld-And-Hull-Laboratories/Heffley_Hull_2019_eLife).

Article and author information

Author details

  1. William Heffley

    Department of Neurobiology, Duke University School of Medicine, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7733-7398

  2. Court Hull

    Department of Neurobiology, Duke University School of Medicine, Durham, United States
    For correspondence
    hull@neuro.duke.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0360-8367

Funding

National Institute of Neurological Disorders and Stroke (5R01NS096289)

  • Court Hull

National Institute of Neurological Disorders and Stroke (F31NS103425)

  • William Heffley

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 experimental procedures using animals were carried out with the approval of the Duke University Animal Care and Use Committee (protocol #A010-19-01).

Reviewing Editor

  1. Jennifer L Raymond, Stanford School of Medicine, United States

Publication history

  1. Received: March 12, 2019
  2. Accepted: July 30, 2019
  3. Accepted Manuscript published: September 11, 2019 (version 1)
  4. Version of Record published: November 11, 2019 (version 2)

Copyright

© 2019, Heffley & Hull

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

  • 3,450
    Page views
  • 602
    Downloads
  • 30
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, 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)

Categories and tags

Research organism

Further reading

    1. Neuroscience

    Cerebellar climbing fibers encode expected reward size

    Noga Larry et al.
    Research Article Updated

    Climbing fiber inputs to the cerebellum encode error signals that instruct learning. Recently, evidence has accumulated to suggest that the cerebellum is also involved in the processing of reward. To study how rewarding events are encoded, we recorded the activity of climbing fibers when monkeys were engaged in an eye movement task. At the beginning of each trial, the monkeys were cued to the size of the reward that would be delivered upon successful completion of the trial. Climbing fiber activity increased when the monkeys were presented with a cue indicating a large reward, but not a small reward. Reward size did not modulate activity at reward delivery or during eye movements. Comparison between climbing fiber and simple spike activity indicated different interactions for coding of movement and reward. These results indicate that climbing fibers encode the expected reward size and suggest a general role of the cerebellum in associative learning beyond error correction.

    1. Neuroscience

    Behavior: The cerebellum shows its stripes

    Ashley L Holloway, Talia N Lerner
    Insight

    New studies examine how the different sub-structures in the cerebellum are organized to receive information during complex behavioral tasks

    1. Neuroscience

    Synaptic targets of photoreceptors specialized to detect color and skylight polarization in Drosophila

    Emil Kind et al.
    Research Article Updated

    Color and polarization provide complementary information about the world and are detected by specialized photoreceptors. However, the downstream neural circuits that process these distinct modalities are incompletely understood in any animal. Using electron microscopy, we have systematically reconstructed the synaptic targets of the photoreceptors specialized to detect color and skylight polarization in Drosophila, and we have used light microscopy to confirm many of our findings. We identified known and novel downstream targets that are selective for different wavelengths or polarized light, and followed their projections to other areas in the optic lobes and the central brain. Our results revealed many synapses along the photoreceptor axons between brain regions, new pathways in the optic lobes, and spatially segregated projections to central brain regions. Strikingly, photoreceptors in the polarization-sensitive dorsal rim area target fewer cell types, and lack strong connections to the lobula, a neuropil involved in color processing. Our reconstruction identifies shared wiring and modality-specific specializations for color and polarization vision, and provides a comprehensive view of the first steps of the pathways processing color and polarized light inputs.