1. Neuroscience
Download icon

State-dependent geometry of population activity in rat auditory cortex

  1. Dmitry Kobak
  2. Jose L Pardo-Vazquez  Is a corresponding author
  3. Mafalda Valente
  4. Christian K Machens
  5. Alfonso Renart  Is a corresponding author
  1. Champalimaud Centre for the Unknown, Portugal
Research Article
  • Cited 0
  • Views 2,081
  • Annotations
Cite this article as: eLife 2019;8:e44526 doi: 10.7554/eLife.44526

Abstract

The accuracy of the neural code depends on the relative embedding of signal and noise in the activity of neural populations. Despite a wealth of theoretical work on population codes, there are few empirical characterisations of the high-dimensional signal and noise subspaces. We studied the geometry of population codes in the rat auditory cortex across brain states along the activation-inactivation continuum, using sounds varying in difference and mean level across the ears. As the cortex becomes more activated, single-hemisphere populations go from preferring contralateral loud sounds to a symmetric preference across lateralisations and intensities, gain-modulation effectively disappears, and the signal and noise subspaces become approximately orthogonal to each other and to the direction corresponding to global activity modulations. Level-invariant decoding of sound lateralisation also becomes possible in the active state. Our results provide an empirical foundation for the geometry and state-dependence of cortical population codes.

Data availability

The full Matlab code for the analysis is located at https://github.com/dkobak/a1geometry. We made the spike count data (spike counts for each neuron for each stimulus presentation from −50 ms to 150 ms in 50 ms bins) available in the same repository. This allows most of our figures to be reproduced. The complete dataset that was collected, including spike time data not analysed here, is available upon reasonable request to the corresponding author.

Article and author information

Author details

  1. Dmitry Kobak

    Champalimaud Neuroscience Program, Champalimaud Centre for the Unknown, Lisbon, Portugal
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5639-7209

  2. Jose L Pardo-Vazquez

    Circuit Dynamics and Computation Laboratory, Champalimaud Centre for the Unknown, Lisboa, Portugal
    For correspondence
    jose.pardovazquez@neuro.fchampalimaud.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4623-2440

  3. Mafalda Valente

    Champalimaud Neuroscience Program, Champalimaud Centre for the Unknown, Lisbon, Portugal
    Competing interests
    The authors declare that no competing interests exist.

  4. Christian K Machens

    Champalimaud Neuroscience Program, Champalimaud Centre for the Unknown, Lisbon, Portugal
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1717-1562

  5. Alfonso Renart

    Champalimaud Neuroscience program, Champalimaud Centre for the Unknown, Lisboa, Portugal
    For correspondence
    alfonso.renart@neuro.fchampalimaud.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7916-9930

Funding

Fundacao Bial (389/14)

  • Dmitry Kobak

EU FP7 grant (ICT-2011-9-600925)

  • Alfonso Renart

German Ministry of Education and Research (FKZ 01GQ1601)

  • Dmitry Kobak

HFSP postdoctoral fellowship (LT 000442/2012)

  • Jose L Pardo-Vazquez

Fundacao para a Ciencia e a Tecnologia

  • Mafalda Valente

Champalimaud Foundation

  • Christian K Machens
  • Alfonso Renart

Simons Collaboration on the Global Brain (543009)

  • Christian K Machens

National Institutes of Health (U01 NS094288)

  • Christian K Machens

Marie Curie Career Integration Grant (PCIG11-GA-2012-322339)

  • Alfonso Renart

HFSP Young Investigator Award (RGY0089)

  • Alfonso Renart

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 carried out in accordance with European Union Directive 86/609/EEC and approved by Direçao-Geral de Veterinaria.

Reviewing Editor

  1. Emilio Salinas, Wake Forest School of Medicine, United States

Publication history

  1. Received: December 19, 2018
  2. Accepted: April 7, 2019
  3. Accepted Manuscript published: April 10, 2019 (version 1)
  4. Version of Record published: April 30, 2019 (version 2)

Copyright

© 2019, 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

  • 2,081
    Page views
  • 311
    Downloads
  • 0
    Citations

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

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

    Decoding the brain state-dependent relationship between pupil dynamics and resting state fMRI signal fluctuation

    Filip Sobczak et al.
    Research Article Updated

    Pupil dynamics serve as a physiological indicator of cognitive processes and arousal states of the brain across a diverse range of behavioral experiments. Pupil diameter changes reflect brain state fluctuations driven by neuromodulatory systems. Resting-state fMRI (rs-fMRI) has been used to identify global patterns of neuronal correlation with pupil diameter changes; however, the linkage between distinct brain state-dependent activation patterns of neuromodulatory nuclei with pupil dynamics remains to be explored. Here, we identified four clusters of trials with unique activity patterns related to pupil diameter changes in anesthetized rat brains. Going beyond the typical rs-fMRI correlation analysis with pupil dynamics, we decomposed spatiotemporal patterns of rs-fMRI with principal component analysis (PCA) and characterized the cluster-specific pupil–fMRI relationships by optimizing the PCA component weighting via decoding methods. This work shows that pupil dynamics are tightly coupled with different neuromodulatory centers in different trials, presenting a novel PCA-based decoding method to study the brain state-dependent pupil–fMRI relationship.

    1. Neuroscience

    Task-specific roles of local interneurons for inter- and intraglomerular signaling in the insect antennal lobe

    Debora Fusca, Peter Kloppenburg
    Research Article

    Local interneurons (LNs) mediate complex interactions within the antennal lobe, the primary olfactory system of insects, and the functional analog of the vertebrate olfactory bulb. In the cockroach Periplaneta americana, as in other insects, several types of LNs with distinctive physiological and morphological properties can be defined. Here, we combined whole-cell patch-clamp recordings and Ca2+ imaging of individual LNs to analyze the role of spiking and nonspiking LNs in inter- and intraglomerular signaling during olfactory information processing. Spiking GABAergic LNs reacted to odorant stimulation with a uniform rise in [Ca2+]i in the ramifications of all innervated glomeruli. In contrast, in nonspiking LNs, glomerular Ca2+ signals were odorant specific and varied between glomeruli, resulting in distinct, glomerulus-specific tuning curves. The cell type-specific differences in Ca2+ dynamics support the idea that spiking LNs play a primary role in interglomerular signaling, while they assign nonspiking LNs an essential role in intraglomerular signaling.

    1. Neuroscience

    Dendritic osmosensors modulate activity-induced calcium influx in oxytocinergic magnocellular neurons of the mouse PVN

    Wanhui Sheng et al.
    Research Article Updated

    Hypothalamic oxytocinergic magnocellular neurons have a fascinating ability to release peptide from both their axon terminals and from their dendrites. Existing data indicates that the relationship between somatic activity and dendritic release is not constant, but the mechanisms through which this relationship can be modulated are not completely understood. Here, we use a combination of electrical and optical recording techniques to quantify activity-induced calcium influx in proximal vs. distal dendrites of oxytocinergic magnocellular neurons located in the paraventricular nucleus of the hypothalamus (OT-MCNs). Results reveal that the dendrites of OT-MCNs are weak conductors of somatic voltage changes; however, activity-induced dendritic calcium influx can be robustly regulated by both osmosensitive and non-osmosensitive ion channels located along the dendritic membrane. Overall, this study reveals that dendritic conductivity is a dynamic and endogenously regulated feature of OT-MCNs that is likely to have substantial functional impact on central oxytocin release.