Mice in a labyrinth exhibit rapid learning, sudden insight, and efficient exploration

  1. Matthew Rosenberg
  2. Tony Zhang
  3. Pietro Perona  Is a corresponding author
  4. Markus Meister  Is a corresponding author
  1. California Institute of Technology, United States

Abstract

Animals learn certain complex tasks remarkably fast, sometimes after a single experience. What behavioral algorithms support this efficiency? Many contemporary studies based on two-alternative-forced-choice (2AFC) tasks observe only slow or incomplete learning. As an alternative, we study the unconstrained behavior of mice in a complex labyrinth and measure the dynamics of learning and the behaviors that enable it. A mouse in the labyrinth makes ~2000 navigation decisions per hour. The animal explores the maze, quickly discovers the location of a reward, and executes correct 10-bit choices after only 10 reward experiences - a learning rate 1000-fold higher than in 2AFC experiments. Many mice improve discontinuously from one minute to the next, suggesting moments of sudden insight about the structure of the labyrinth. The underlying search algorithm does not require a global memory of places visited and is largely explained by purely local turning rules.

Data availability

The behavioral data and code that produced the figures are available in a public Github repository cited in the article https://github.com/markusmeister/Rosenberg-2021-Repository. We are also preparing a permanent institutional repository.

The following data sets were generated

Article and author information

Author details

  1. Matthew Rosenberg

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    No competing interests declared.
  2. Tony Zhang

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    No competing interests declared.
  3. Pietro Perona

    Computation and Neural Systems, California Institute of Technology, Pasadena, United States
    For correspondence
    perona@caltech.edu
    Competing interests
    No competing interests declared.
  4. Markus Meister

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    For correspondence
    meister@caltech.edu
    Competing interests
    Markus Meister, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2136-6506

Funding

Simons Foundation (543015)

  • Markus Meister

Simons Foundation (543025)

  • Pietro Perona

National Science Foundation (1564330)

  • Pietro Perona

Google

  • Pietro Perona

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to animal protocol 1656 approved by the institutional animal care and use committee (IACUC) at Caltech.

Copyright

© 2021, Rosenberg 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

  • 22,148
    views
  • 1,692
    downloads
  • 68
    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. Matthew Rosenberg
  2. Tony Zhang
  3. Pietro Perona
  4. Markus Meister
(2021)
Mice in a labyrinth exhibit rapid learning, sudden insight, and efficient exploration
eLife 10:e66175.
https://doi.org/10.7554/eLife.66175

Share this article

https://doi.org/10.7554/eLife.66175

Further reading

    1. Computational and Systems Biology
    2. Neuroscience
    Cesare V Parise, Marc O Ernst
    Research Article

    Audiovisual information reaches the brain via both sustained and transient input channels, representing signals’ intensity over time or changes thereof, respectively. To date, it is unclear to what extent transient and sustained input channels contribute to the combined percept obtained through multisensory integration. Based on the results of two novel psychophysical experiments, here we demonstrate the importance of the transient (instead of the sustained) channel for the integration of audiovisual signals. To account for the present results, we developed a biologically inspired, general-purpose model for multisensory integration, the multisensory correlation detectors, which combines correlated input from unimodal transient channels. Besides accounting for the results of our psychophysical experiments, this model could quantitatively replicate several recent findings in multisensory research, as tested against a large collection of published datasets. In particular, the model could simultaneously account for the perceived timing of audiovisual events, multisensory facilitation in detection tasks, causality judgments, and optimal integration. This study demonstrates that several phenomena in multisensory research that were previously considered unrelated, all stem from the integration of correlated input from unimodal transient channels.

    1. Cell Biology
    2. Computational and Systems Biology
    Sarah De Beuckeleer, Tim Van De Looverbosch ... Winnok H De Vos
    Research Article

    Induced pluripotent stem cell (iPSC) technology is revolutionizing cell biology. However, the variability between individual iPSC lines and the lack of efficient technology to comprehensively characterize iPSC-derived cell types hinder its adoption in routine preclinical screening settings. To facilitate the validation of iPSC-derived cell culture composition, we have implemented an imaging assay based on cell painting and convolutional neural networks to recognize cell types in dense and mixed cultures with high fidelity. We have benchmarked our approach using pure and mixed cultures of neuroblastoma and astrocytoma cell lines and attained a classification accuracy above 96%. Through iterative data erosion, we found that inputs containing the nuclear region of interest and its close environment, allow achieving equally high classification accuracy as inputs containing the whole cell for semi-confluent cultures and preserved prediction accuracy even in very dense cultures. We then applied this regionally restricted cell profiling approach to evaluate the differentiation status of iPSC-derived neural cultures, by determining the ratio of postmitotic neurons and neural progenitors. We found that the cell-based prediction significantly outperformed an approach in which the population-level time in culture was used as a classification criterion (96% vs 86%, respectively). In mixed iPSC-derived neuronal cultures, microglia could be unequivocally discriminated from neurons, regardless of their reactivity state, and a tiered strategy allowed for further distinguishing activated from non-activated cell states, albeit with lower accuracy. Thus, morphological single-cell profiling provides a means to quantify cell composition in complex mixed neural cultures and holds promise for use in the quality control of iPSC-derived cell culture models.