The impact of deep space radiation on cognitive performance: From biological sex to biomarkers to countermeasures

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Abstract

Space radiation affects memory in male and not in female mice, and it is dependent on the innate immune system response.

Abstract

In the coming decade, astronauts will travel back to the moon in preparation for future Mars missions. Exposure to galactic cosmic radiation (GCR) is a major obstacle for deep space travel. Using multivariate principal components analysis, we found sex-dimorphic responses in mice exposed to accelerated charged particles to simulate GCR (GCRsim); males displayed impaired spatial learning, whereas females did not. Mechanistically, these GCRsim-induced learning impairments corresponded with chronic microglia activation and synaptic alterations in the hippocampus. Temporary microglia depletion shortly after GCRsim exposure mitigated GCRsim-induced deficits measured months after the radiation exposure. Furthermore, blood monocyte levels measured early after GCRsim exposure were predictive of the late learning deficits and microglia activation measured in the male mice. Our findings (i) advance our understanding of charged particle–induced cognitive challenges, (ii) provide evidence for early peripheral biomarkers for identifying late cognitive deficits, and (iii) offer potential therapeutic strategies for mitigating GCR-induced cognitive loss.

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Author and article information

Contributors

Karen Krukowski:

ORCID: https://orcid.org/0000-0003-0281-8917

Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Katherine Grue: Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

McKenna Becker:

ORCID: https://orcid.org/0000-0002-6009-0170

Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: ValidationRole: VisualizationRole: Writing - review & editing

Edward Elizarraras: Role: Data curationRole: Formal analysisRole: InvestigationRole: ResourcesRole: SoftwareRole: ValidationRole: Visualization

Elma S. Frias: Role: Formal analysisRole: InvestigationRole: Project administrationRole: ValidationRole: VisualizationRole: Writing - review & editing

Aaron Halvorsen:

ORCID: https://orcid.org/0000-0001-5553-7233

Role: Investigation

McKensie Koenig-Zanoff: Role: Data curationRole: Investigation

Valentina Frattini: Role: Investigation

Hasitha Nimmagadda: Role: Formal analysisRole: InvestigationRole: ResourcesRole: SoftwareRole: ValidationRole: Writing - review & editing

Xi Feng: Role: InvestigationRole: MethodologyRole: ValidationRole: VisualizationRole: Writing - review & editing

Tamako Jones: Role: Investigation

Gregory Nelson:

ORCID: https://orcid.org/0000-0002-0843-2444

Role: ConceptualizationRole: InvestigationRole: MethodologyRole: SupervisionRole: ValidationRole: Writing - review & editing

Adam R. Ferguson:

ORCID: https://orcid.org/0000-0001-7102-1608

Role: Data curationRole: Formal analysisRole: MethodologyRole: ResourcesRole: SoftwareRole: ValidationRole: VisualizationRole: Writing - review & editing

Susanna Rosi:

ORCID: https://orcid.org/0000-0002-9269-3638

Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing - original draftRole: Writing - review & editing

Journal

Journal ID (nlm-ta): Sci Adv

Journal ID (publisher-id): sciadv

Journal ID (hwp): advances

Title: Science Advances

Publisher: American Association for the Advancement of Science

ISSN (Electronic): 2375-2548

Publication date Collection: October 2021

Publication date (Electronic, pub): 15 October 2021

Volume: 7

Issue: 42

Electronic Location Identifier: eabg6702

Affiliations

[1 ]Department of Physical Therapy and Rehabilitation Science, University of California, San Francisco, San Francisco, CA, USA.

[2 ]Brain and Spinal Injury Center, University of California, San Francisco, San Francisco, CA, USA.

[3 ]Department of Basic Sciences, Division of Biomedical Engineering Sciences, Loma Linda University, Loma Linda, CA, USA.

[4 ]Department of Neurological Surgery, University of California, San Francisco, San Francisco, CA, USA.

[5 ]Weill Institute for Neuroscience, University of California, San Francisco, San Francisco, CA, USA.

[6 ]San Francisco Veterans Affairs Healthcare System, San Francisco, CA, USA.

[7 ]Kavli Institute of Fundamental Neuroscience, University of California, San Francisco, San Francisco, CA, USA.

Author notes

[* ]Corresponding author. Email: susanna.rosi@ 123456ucsf.edu

Author information

Karen Krukowski https://orcid.org/0000-0003-0281-8917

McKenna Becker https://orcid.org/0000-0002-6009-0170

Aaron Halvorsen https://orcid.org/0000-0001-5553-7233

Gregory Nelson https://orcid.org/0000-0002-0843-2444

Adam R. Ferguson https://orcid.org/0000-0001-7102-1608

Susanna Rosi https://orcid.org/0000-0002-9269-3638

Article

Publisher ID: abg6702

DOI: 10.1126/sciadv.abg6702

PMC ID: 8519563

PubMed ID: 34652936

SO-VID: f375d14c-8418-453e-9f06-7c78ebffa8a3

Copyright © Copyright © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.

History

Date received : 20 January 2021

Date accepted : 20 August 2021

Funding

Funded by: doi http://dx.doi.org/10.13039/100000001, National Science Foundation;

Award ID: Graduate Fellowship Program

Funded by: doi http://dx.doi.org/10.13039/100000065, National Institute of Neurological Disorders and Stroke;

Award ID: R01NS088475

Funded by: doi http://dx.doi.org/10.13039/100000065, National Institute of Neurological Disorders and Stroke;

Award ID: UG3NS106899

Funded by: doi http://dx.doi.org/10.13039/100000104, National Aeronautics and Space Administration;

Award ID: NNX14AC94G