Demixed principal component analysis of neural population data

  1. Dmitry Kobak  Is a corresponding author
  2. Wieland Brendel
  3. Christos Constantinidis
  4. Claudia E Feierstein
  5. Adam Kepecs
  6. Zachary F Mainen
  7. Ranulfo Romo
  8. Xue-Lian Qi
  9. Naoshige Uchida
  10. Christian K Machens
  1. Champalimaud Centre for the Unknown, Portugal
  2. Wake Forest University School of Medicine, United States
  3. Cold Spring Harbor Laboratory, United States
  4. Universidad Nacional Autónoma de México, Mexico
  5. Harvard University, United States

Abstract

Neurons in higher cortical areas, such as the prefrontal cortex, are often tuned to a variety of sensory and motor variables, and are therefore said to display mixed selectivity. This complexity of single neuron responses can obscure what information these areas represent and how it is represented. Here we demonstrate the advantages of a new dimensionality reduction technique, demixed principal component analysis (dPCA), that decomposes population activity into a few components. In addition to systematically capturing the majority of the variance of the data, dPCA also exposes the dependence of the neural representation on task parameters such as stimuli, decisions, or rewards. To illustrate our method we reanalyze population data from four datasets comprising different species, different cortical areas and different experimental tasks. In each case, dPCA provides a concise way of visualizing the data that summarizes the task-dependent features of the population response in a single figure.

Article and author information

Author details

  1. Dmitry Kobak

    Champalimaud Neuroscience Program, Champalimaud Centre for the Unknown, Lisbon, Portugal
    For correspondence
    dmitry.kobak@neuro.fchampalimaud.org
    Competing interests
    No competing interests declared.
  2. Wieland Brendel

    Champalimaud Neuroscience Program, Champalimaud Centre for the Unknown, Lisbon, Portugal
    Competing interests
    No competing interests declared.
  3. Christos Constantinidis

    Wake Forest University School of Medicine, Winston-Salem, United States
    Competing interests
    No competing interests declared.
  4. Claudia E Feierstein

    Champalimaud Neuroscience Program, Champalimaud Centre for the Unknown, Lisbon, Portugal
    Competing interests
    No competing interests declared.
  5. Adam Kepecs

    Cold Spring Harbor Laboratory, Cold Spring Harbor, United States
    Competing interests
    No competing interests declared.
  6. Zachary F Mainen

    Champalimaud Neuroscience Program, Champalimaud Centre for the Unknown, Lisbon, Portugal
    Competing interests
    No competing interests declared.
  7. Ranulfo Romo

    Instituto de Fisiología Celular-Neurociencias, Universidad Nacional Autónoma de México, Ciudad de México, Mexico
    Competing interests
    No competing interests declared.
  8. Xue-Lian Qi

    Wake Forest University School of Medicine, Winston-Salem, United States
    Competing interests
    No competing interests declared.
  9. Naoshige Uchida

    Harvard University, Cambridge, United States
    Competing interests
    Naoshige Uchida, Reviewing editor, eLife.
  10. Christian K Machens

    Champalimaud Neuroscience Program, Champalimaud Centre for the Unknown, Lisbon, Portugal
    Competing interests
    No competing interests declared.

Reviewing Editor

  1. Mark CW van Rossum, University of Edinburgh, United Kingdom

Version history

  1. Received: August 19, 2015
  2. Accepted: April 7, 2016
  3. Accepted Manuscript published: April 12, 2016 (version 1)
  4. Version of Record published: May 31, 2016 (version 2)

Copyright

© 2016, Kobak 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

  • 35,264
    Page views
  • 6,292
    Downloads
  • 263
    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)

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. Dmitry Kobak
  2. Wieland Brendel
  3. Christos Constantinidis
  4. Claudia E Feierstein
  5. Adam Kepecs
  6. Zachary F Mainen
  7. Ranulfo Romo
  8. Xue-Lian Qi
  9. Naoshige Uchida
  10. Christian K Machens
(2016)
Demixed principal component analysis of neural population data
eLife 5:e10989.
https://doi.org/10.7554/eLife.10989

Share this article

https://doi.org/10.7554/eLife.10989

Further reading

    1. Cell Biology
    2. Neuroscience
    Haibin Yu, Dandan Liu ... Kai Yuan
    Research Article

    O-GlcNAcylation is a dynamic post-translational modification that diversifies the proteome. Its dysregulation is associated with neurological disorders that impair cognitive function, and yet identification of phenotype-relevant candidate substrates in a brain-region specific manner remains unfeasible. By combining an O-GlcNAc binding activity derived from Clostridium perfringens OGA (CpOGA) with TurboID proximity labeling in Drosophila, we developed an O-GlcNAcylation profiling tool that translates O-GlcNAc modification into biotin conjugation for tissue-specific candidate substrates enrichment. We mapped the O-GlcNAc interactome in major brain regions of Drosophila and found that components of the translational machinery, particularly ribosomal subunits, were abundantly O-GlcNAcylated in the mushroom body of Drosophila brain. Hypo-O-GlcNAcylation induced by ectopic expression of active CpOGA in the mushroom body decreased local translational activity, leading to olfactory learning deficits that could be rescued by dMyc overexpression-induced increase of protein synthesis. Our study provides a useful tool for future dissection of tissue-specific functions of O-GlcNAcylation in Drosophila, and suggests a possibility that O-GlcNAcylation impacts cognitive function via regulating regional translational activity in the brain.

    1. Neuroscience
    Sydney Trask, Nicole C Ferrara
    Insight

    Gradually reducing a source of fear during extinction treatments may weaken negative memories in the long term.