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Auricular transcutaneous vagus nerve stimulation acutely modulates brain connectivity in mice

Cecilia Brambilla-Pisoni, Emma Muñoz-Moreno, Ianire Gallego-Amaro, Rafael Maldonado, Antoni Ivorra, Guadalupe Soria, Andrés Ozaita
doi: https://doi.org/10.1101/2021.11.15.468252
Cecilia Brambilla-Pisoni
1Laboratory of Neuropharmacology. Department of Experimental and Health Sciences, Universitat Pompeu Fabra, Barcelona, Spain
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Emma Muñoz-Moreno
4Experimental 7T MRI Unit, Magnetic Resonance Imaging Core Facility, Institut d’Investigacions Biomediques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
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Ianire Gallego-Amaro
1Laboratory of Neuropharmacology. Department of Experimental and Health Sciences, Universitat Pompeu Fabra, Barcelona, Spain
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Rafael Maldonado
1Laboratory of Neuropharmacology. Department of Experimental and Health Sciences, Universitat Pompeu Fabra, Barcelona, Spain
3IMIM Hospital del Mar Research Institute, Barcelona, Spain
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Antoni Ivorra
2Department of Information and Communication Technologies, Universitat Pompeu Fabra, Barcelona, Spain
6Serra Húnter Fellow Programme, Universitat Pompeu Fabra, Barcelona, Spain
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Guadalupe Soria
4Experimental 7T MRI Unit, Magnetic Resonance Imaging Core Facility, Institut d’Investigacions Biomediques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
5Laboratory of Surgical Neuroanatomy, Faculty of Medicine and Health Sciences, Institute of Neurosciences, University of Barcelona, Barcelona, Spain
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Andrés Ozaita
1Laboratory of Neuropharmacology. Department of Experimental and Health Sciences, Universitat Pompeu Fabra, Barcelona, Spain
3IMIM Hospital del Mar Research Institute, Barcelona, Spain
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  • For correspondence: andres.ozaita@upf.edu
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Abstract

Background Brain electrical stimulation techniques take advantage of the intrinsic plasticity of the nervous system, opening a wide range of therapeutic applications. Vagus nerve stimulation (VNS) is an approved adjuvant for drug-resistant epilepsy and depression. Its non-invasive form, auricular transcutaneous VNS (atVNS), is under investigation for applications, including cognitive improvement.

Objective We aimed to study the effects of atVNS on brain connectivity, under conditions that improved memory persistence in CD-1 male mice.

Methods Acute atVNS in the cymba conchae of the left ear was performed using a standard stimulation protocol under light isoflurane anesthesia, immediately or 3 h after the training/familiarization phase of the novel object-recognition memory test (NORT). Another cohort of mice was used for bilateral c-Fos analysis after atVNS administration. Spearman correlation of c-Fos density between each pair of the thirty brain regions analyzed allowed obtaining the network of significant functional connections in stimulated and non-stimulated control brains.

Results NORT performance was enhanced when atVNS was delivered just after, but not 3 h after, the familiarization phase of the task. No alterations in c-Fos density were associated to electrostimulation, but a significant effect of atVNS was observed on c-Fos-based functional connectivity. atVNS induced a clear reorganization of the network, increasing the inter-hemisphere connections and the connectivity of locus coeruleus.

Conclusion Our results provide new insights in the effects of atVNS on memory performance and brain connectivity extending our knowledge of the biological mechanisms of bioelectronics in medicine.

Highlights

  • atVNS, delivered immediately after NORT training phase, improves memory persistence

  • atVNS did not promote significant changes in brain c-Fos density

  • atVNS induced a significant reorganization of c-Fos-based functional brain network

  • atVNS produced an enhancement in correlated activity between hemispheres

  • atVNS did not engage the prefrontal-retrosplenial axis, characteristic of the DMN

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Declaration of interest: none

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted November 17, 2021.
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Auricular transcutaneous vagus nerve stimulation acutely modulates brain connectivity in mice
Cecilia Brambilla-Pisoni, Emma Muñoz-Moreno, Ianire Gallego-Amaro, Rafael Maldonado, Antoni Ivorra, Guadalupe Soria, Andrés Ozaita
bioRxiv 2021.11.15.468252; doi: https://doi.org/10.1101/2021.11.15.468252
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Auricular transcutaneous vagus nerve stimulation acutely modulates brain connectivity in mice
Cecilia Brambilla-Pisoni, Emma Muñoz-Moreno, Ianire Gallego-Amaro, Rafael Maldonado, Antoni Ivorra, Guadalupe Soria, Andrés Ozaita
bioRxiv 2021.11.15.468252; doi: https://doi.org/10.1101/2021.11.15.468252

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