Long-Range population dynamics of anatomically defined neocortical networks

  1. Jerry L Chen
  2. Fabian F Voigt
  3. Mitra Javadzadeh
  4. Roland Krueppel
  5. Fritjof Helmchen  Is a corresponding author
  1. Boston University, United States
  2. University of Zurich, Switzerland
  3. Federal Ministry of Education and Research, Germany

Abstract

The coordination of activity across neocortical areas is essential for mammalian brain function. Understanding this process requires simultaneous functional measurements across the cortex. However, it has not been possible to dissociate direct cortico-cortical interactions from other sources of neuronal correlations by targeting recordings to neuronal subpopulations that anatomically project between areas. Here, we combined anatomical tracers with a novel multi-area two-photon microscope to perform simultaneous calcium imaging across mouse primary (S1) and secondary (S2) somatosensory whisker cortex during texture discrimination behavior, specifically identifying feedforward and feedback neurons. We observed coordinated S1-S2 activity that is related to motor behaviors such as goal-directed whisking and licking but is not specific to identified projection neurons. However, feedforward and feedback neurons especially participated in inter-areal coordination when motor behavior was paired with whisker-texture touches, suggesting that direct S1-S2 interactions are sensory-dependent. Our results demonstrate specific functional coordination of anatomically-identified projection neurons across sensory cortices.

Article and author information

Author details

  1. Jerry L Chen

    Department of Biology, Boston University, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Fabian F Voigt

    Brain Research Institute, University of Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  3. Mitra Javadzadeh

    Brain Research Institute, University of Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  4. Roland Krueppel

    Federal Ministry of Education and Research, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Fritjof Helmchen

    Brain Research Institute, University of Zurich, Zurich, Switzerland
    For correspondence
    helmchen@hifo.uzh.ch
    Competing interests
    The authors declare that no competing interests exist.

Ethics

Animal experimentation: Experimental procedures followed the guidelines of the Veterinary Office of Switzerland and were approved by the Cantonal Veterinary Office in Zurich. Experiments were carried out under the approved licenses 62/2011 and 285/2014.

Copyright

© 2016, Chen 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

  • 5,922
    views
  • 1,443
    downloads
  • 104
    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. Jerry L Chen
  2. Fabian F Voigt
  3. Mitra Javadzadeh
  4. Roland Krueppel
  5. Fritjof Helmchen
(2016)
Long-Range population dynamics of anatomically defined neocortical networks
eLife 5:e14679.
https://doi.org/10.7554/eLife.14679

Share this article

https://doi.org/10.7554/eLife.14679

Further reading

    1. Genetics and Genomics
    2. Neuroscience
    Akanksha Bafna, Gareth Banks ... Patrick M Nolan
    Research Article

    The mammalian suprachiasmatic nucleus (SCN), situated in the ventral hypothalamus, directs daily cellular and physiological rhythms across the body. The SCN clockwork is a self-sustaining transcriptional-translational feedback loop (TTFL) that in turn coordinates the expression of clock-controlled genes (CCGs) directing circadian programmes of SCN cellular activity. In the mouse, the transcription factor, ZFHX3 (zinc finger homeobox-3), is necessary for the development of the SCN and influences circadian behaviour in the adult. The molecular mechanisms by which ZFHX3 affects the SCN at transcriptomic and genomic levels are, however, poorly defined. Here, we used chromatin immunoprecipitation sequencing to map the genomic localization of ZFHX3-binding sites in SCN chromatin. To test for function, we then conducted comprehensive RNA sequencing at six distinct times-of-day to compare the SCN transcriptional profiles of control and ZFHX3-conditional null mutants. We show that the genome-wide occupancy of ZFHX3 occurs predominantly around gene transcription start sites, co-localizing with known histone modifications, and preferentially partnering with clock transcription factors (CLOCK, BMAL1) to regulate clock gene(s) transcription. Correspondingly, we show that the conditional loss of ZFHX3 in the adult has a dramatic effect on the SCN transcriptome, including changes in the levels of transcripts encoding elements of numerous neuropeptide neurotransmitter systems while attenuating the daily oscillation of the clock TF Bmal1. Furthermore, various TTFL genes and CCGs exhibited altered circadian expression profiles, consistent with an advanced in daily behavioural rhythms under 12 h light–12 h dark conditions. Together, these findings reveal the extensive genome-wide regulation mediated by ZFHX3 in the central clock that orchestrates daily timekeeping in mammals.

    1. Neuroscience
    Shuo Zhang, Yan Tian ... Haiyan Wu
    Research Article

    Active inference integrates perception, decision-making, and learning into a united theoretical framework, providing an efficient way to trade off exploration and exploitation by minimizing (expected) free energy. In this study, we asked how the brain represents values and uncertainties (novelty and variability), and resolves these uncertainties under the active inference framework in the exploration-exploitation trade-off. Twenty-five participants performed a contextual two-armed bandit task, with electroencephalogram (EEG) recordings. By comparing the model evidence for active inference and reinforcement learning models of choice behavior, we show that active inference better explains human decision-making under novelty and variability, which entails exploration or information seeking. The EEG sensor-level results show that the activity in the frontal, central, and parietal regions is associated with novelty, while the activity in the frontal and central brain regions is associated with variability. The EEG source-level results indicate that the expected free energy is encoded in the frontal pole and middle frontal gyrus and uncertainties are encoded in different brain regions but with overlap. Our study dissociates the expected free energy and uncertainties in active inference theory and their neural correlates, speaking to the construct validity of active inference in characterizing cognitive processes of human decisions. It provides behavioral and neural evidence of active inference in decision processes and insights into the neural mechanism of human decisions under uncertainties.