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Functional and multiscale 3D structural investigation of brain tissue through correlative in vivo physiology, synchrotron micro-tomography and volume electron microscopy

View ORCID ProfileCarles Bosch, View ORCID ProfileTobias Ackels, View ORCID ProfileAlexandra Pacureanu, View ORCID ProfileYuxin Zhang, Christopher J Peddie, View ORCID ProfileManuel Berning, View ORCID ProfileNorman Rzepka, View ORCID ProfileMarie-Christine Zdora, View ORCID ProfileIsabell Whiteley, View ORCID ProfileMalte Storm, View ORCID ProfileAnne Bonnin, Christoph Rau, View ORCID ProfileTroy Margrie, View ORCID ProfileLucy Collinson, View ORCID ProfileAndreas T Schaefer
doi: https://doi.org/10.1101/2021.01.13.426503
Carles Bosch
1Sensory Circuits and Neurotechnology Lab., The Francis Crick Institute, London, UK
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  • For correspondence: carles.bosch@crick.ac.uk andreas.schaefer@crick.ac.uk
Tobias Ackels
1Sensory Circuits and Neurotechnology Lab., The Francis Crick Institute, London, UK
2Department of Neuroscience, Physiology and Pharmacology, University College London, UK
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Alexandra Pacureanu
1Sensory Circuits and Neurotechnology Lab., The Francis Crick Institute, London, UK
2Department of Neuroscience, Physiology and Pharmacology, University College London, UK
3ESRF, The European Synchrotron, Grenoble, France
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Yuxin Zhang
1Sensory Circuits and Neurotechnology Lab., The Francis Crick Institute, London, UK
2Department of Neuroscience, Physiology and Pharmacology, University College London, UK
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Christopher J Peddie
4Electron Microscopy STP, The Francis Crick Institute, London, UK
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Manuel Berning
5Department of Connectomics, Max Planck Institute for Brain Research, Frankfurt am Main, Germany
6scalable minds GmbH, Potsdam, Germany
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Norman Rzepka
6scalable minds GmbH, Potsdam, Germany
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Marie-Christine Zdora
7Department of Physics and Astronomy, University College London, London, UK
8Diamond Light Source, Harwell Science and Innovation Campus, Didcot, UK
9School of Physics and Astronomy, University of Southampton, Highfield Campus, Southampton, UK
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Isabell Whiteley
1Sensory Circuits and Neurotechnology Lab., The Francis Crick Institute, London, UK
2Department of Neuroscience, Physiology and Pharmacology, University College London, UK
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Malte Storm
8Diamond Light Source, Harwell Science and Innovation Campus, Didcot, UK
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Anne Bonnin
10Paul Scherrer Institut, Villigen, Switzerland
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Christoph Rau
8Diamond Light Source, Harwell Science and Innovation Campus, Didcot, UK
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Troy Margrie
11Sainsbury Wellcome Centre, University College London, London, UK
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Lucy Collinson
4Electron Microscopy STP, The Francis Crick Institute, London, UK
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Andreas T Schaefer
1Sensory Circuits and Neurotechnology Lab., The Francis Crick Institute, London, UK
2Department of Neuroscience, Physiology and Pharmacology, University College London, UK
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  • For correspondence: carles.bosch@crick.ac.uk andreas.schaefer@crick.ac.uk
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Abstract

Attributing in vivo neurophysiology to the brains’ ultrastructure requires a large field of view containing contextual anatomy. Electron microscopy (EM) is the gold standard technique to identify ultrastructure, yet acquiring volumes containing full mammalian neural circuits is challenging and time consuming using EM. Here, we show that synchrotron X-ray computed tomography (SXRT) provides rapid imaging of EM-prepared tissue volumes of several cubic millimetres. Resolution was sufficient for distinguishing cell bodies as well as for tracing apical dendrites in olfactory bulb and hippocampus, for up to 350 μm. Correlating EM with SXRT allowed us to associate dendritic spines on pyramidal cell apical dendrites in the stratum radiatum to their corresponding soma locations. Superficial pyramidal neurons had larger spine apparatus density compared to deeper ones, implying differential synaptic plasticity for superficial and deeper cells. Finally, we show that X-ray tomography and volume EM can be reliably correlated to prior in vivo imaging. Thus, combining functional measurements with multiscale X-ray microscopy and volume EM establishes a correlative workflow that enables functional and structural investigation of subcellular features in the context of cellular morphologies, tissues and ultimately whole organs.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted January 14, 2021.
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Functional and multiscale 3D structural investigation of brain tissue through correlative in vivo physiology, synchrotron micro-tomography and volume electron microscopy
Carles Bosch, Tobias Ackels, Alexandra Pacureanu, Yuxin Zhang, Christopher J Peddie, Manuel Berning, Norman Rzepka, Marie-Christine Zdora, Isabell Whiteley, Malte Storm, Anne Bonnin, Christoph Rau, Troy Margrie, Lucy Collinson, Andreas T Schaefer
bioRxiv 2021.01.13.426503; doi: https://doi.org/10.1101/2021.01.13.426503
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Functional and multiscale 3D structural investigation of brain tissue through correlative in vivo physiology, synchrotron micro-tomography and volume electron microscopy
Carles Bosch, Tobias Ackels, Alexandra Pacureanu, Yuxin Zhang, Christopher J Peddie, Manuel Berning, Norman Rzepka, Marie-Christine Zdora, Isabell Whiteley, Malte Storm, Anne Bonnin, Christoph Rau, Troy Margrie, Lucy Collinson, Andreas T Schaefer
bioRxiv 2021.01.13.426503; doi: https://doi.org/10.1101/2021.01.13.426503

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