High and asymmetric somato-dendritic coupling of V1 layer 5 neurons independent of visual stimulation and locomotion

  1. Valerio Francioni
  2. Zahid Padamsey
  3. Nathalie L Rochefort  Is a corresponding author
  1. University of Edinburgh, United Kingdom

Abstract

Active dendrites impact sensory processing and behaviour. However, it remains unclear how active dendritic integration relates to somatic output in vivo. We imaged semi-simultaneously GCaMP6s signals in the soma, trunk and distal tuft dendrites of layer 5 pyramidal neurons in the awake mouse primary visual cortex. We found that apical tuft signals were dominated by widespread, highly correlated calcium transients throughout the tuft. While these signals were highly coupled to trunk and somatic transients, the frequency of calcium transients was found to decrease in a distance-dependent manner from soma to tuft. Ex vivo recordings suggest that low-frequency back-propagating action potentials underlie the distance-dependent loss of signals, while coupled somato-dendritic signals can be triggered by high-frequency somatic bursts or strong apical tuft depolarization. Visual stimulation and locomotion increased neuronal activity without affecting somato-dendritic coupling. High, asymmetric somato-dendritic coupling is therefore a widespread feature of layer 5 neurons activity in vivo.

Data availability

Raw data (changes of fluorescence over time) are provided in all the main figures (figure 1-4) and in two supplementary figures.Additionally, we provide two data source videos (supplementary video 1 and supplementary video 2).We are willing to share all raw data (videos) upon acceptance of the manuscript. Due to the large volume of imaging data sets, we will give access to a local dedicated server from Rochefort lab.All analyses were performed using custom-written scripts in MATLAB, which will be freely available via GitHub repository (https://github.com/rochefort-lab), upon acceptance of the manuscript.

Article and author information

Author details

  1. Valerio Francioni

    Centre for Discovery Brain Sciences, University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Zahid Padamsey

    Centre for Discovery Brain Sciences, University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Nathalie L Rochefort

    Centre for Discovery Brain Sciences, University of Edinburgh, Edinburgh, United Kingdom
    For correspondence
    n.rochefort@ed.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3498-6221

Funding

Wellcome (102857/Z/13/Z)

  • Nathalie L Rochefort

Royal Society (102857/Z/13/Z)

  • Nathalie L Rochefort

University Of Edinburgh (PhD fellowship)

  • Valerio Francioni

Simons Initiative for the Developing Brain (Project grant)

  • Nathalie L Rochefort

European Union's FP7 program (CIG 631770)

  • Nathalie L Rochefort

RS MacDonald Charitable Trust (Seedcorn Grant)

  • Nathalie L Rochefort

Royal Society (Royal Commission for the Exhibition 1851)

  • Zahid Padamsey

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 experiments and procedures involving animals were approved by the University of Edinburgh Animal Welfare and the ethical review board (AWERB) and performed under the appropriate PIL and PPL license from the UK Home Office in accordance with the Animal (Scientific Procedures) act 1986 and the European Directive 86/609/EEC on the protection of animals used for experimental purposes.

Copyright

© 2019, Francioni 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

  • 3,220
    views
  • 410
    downloads
  • 42
    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. Valerio Francioni
  2. Zahid Padamsey
  3. Nathalie L Rochefort
(2019)
High and asymmetric somato-dendritic coupling of V1 layer 5 neurons independent of visual stimulation and locomotion
eLife 8:e49145.
https://doi.org/10.7554/eLife.49145

Share this article

https://doi.org/10.7554/eLife.49145

Further reading

    1. Neuroscience
    Cuong Pham, Yuji Komaki ... Dongdong Li
    Research Article

    Brain water homeostasis not only provides a physical protection, but also determines the diffusion of chemical molecules key for information processing and metabolic stability. As a major type of glia in brain parenchyma, astrocytes are the dominant cell type expressing aquaporin water channel. How astrocyte aquaporin contributes to brain water homeostasis in basal physiology remains to be understood. We report that astrocyte aquaporin 4 (AQP4) mediates a tonic water efflux in basal conditions. Acute inhibition of astrocyte AQP4 leads to intracellular water accumulation as optically resolved by fluorescence-translated imaging in acute brain slices, and in vivo by fiber photometry in mobile mice. We then show that aquaporin-mediated constant water efflux maintains astrocyte volume and osmotic equilibrium, astrocyte and neuron Ca2+ signaling, and extracellular space remodeling during optogenetically induced cortical spreading depression. Using diffusion-weighted magnetic resonance imaging (DW-MRI), we observed that in vivo inhibition of AQP4 water efflux heterogeneously disturbs brain water homeostasis in a region-dependent manner. Our data suggest that astrocyte aquaporin, though bidirectional in nature, mediates a tonic water outflow to sustain cellular and environmental equilibrium in brain parenchyma.

    1. Neuroscience
    Chad Heer, Mark Sheffield
    Research Article

    Neuromodulatory inputs to the hippocampus play pivotal roles in modulating synaptic plasticity, shaping neuronal activity, and influencing learning and memory. Recently, it has been shown that the main sources of catecholamines to the hippocampus, ventral tegmental area (VTA) and locus coeruleus (LC), may have overlapping release of neurotransmitters and effects on the hippocampus. Therefore, to dissect the impacts of both VTA and LC circuits on hippocampal function, a thorough examination of how these pathways might differentially operate during behavior and learning is necessary. We therefore utilized two-photon microscopy to functionally image the activity of VTA and LC axons within the CA1 region of the dorsal hippocampus in head-fixed male mice navigating linear paths within virtual reality (VR) environments. We found that within familiar environments some VTA axons and the vast majority of LC axons showed a correlation with the animals’ running speed. However, as mice approached previously learned rewarded locations, a large majority of VTA axons exhibited a gradual ramping-up of activity, peaking at the reward location. In contrast, LC axons displayed a pre-movement signal predictive of the animal’s transition from immobility to movement. Interestingly, a marked divergence emerged following a switch from the familiar to novel VR environments. Many LC axons showed large increases in activity that remained elevated for over a minute, while the previously observed VTA axon ramping-to-reward dynamics disappeared during the same period. In conclusion, these findings highlight distinct roles of VTA and LC catecholaminergic inputs in the dorsal CA1 hippocampal region. These inputs encode unique information, with reward information in VTA inputs and novelty and kinematic information in LC inputs, likely contributing to differential modulation of hippocampal activity during behavior and learning.