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Cited by 39Effects of Radiation ExposureSpaceflight effects on biologyRadiation Therapy and Dosimetry

Effects of Six Sequential Charged Particle Beams on Behavioral and Cognitive Performance in B6D2F1 Female and Male Mice

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Raber, Jacob, Fuentes Anaya, Andrea, Torres, Eileen Ruth S., Lee, Joanne, Boutros, Sydney, Grygoryev, Dmytro, Hammer, Austin, Kasschau, Kristin D. +3 more·2020·Frontiers in Physiology
DOI 10.3389/fphys.2020.00959PMC PMC7485338
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Abstract

The radiation environment astronauts are exposed to in deep space includes galactic cosmic radiation (GCR) with different proportions of all naturally occurring ions. To assist NASA with assessment of risk to the brain following exposure to a mixture of ions broadly representative of the GCR, we assessed the behavioral and cognitive performance of female and male C57BL/6J x DBA2/J F1 (B6D2F1) mice two months following rapidly delivered, sequential 6 beam irradiation with protons (1 GeV, LET = 0.24 keV, 50%), 4He ions (250 MeV/n, LET = 1.6 keV/m, 20%), 16O ions (250 MeV/n, LET= 25 keV/m 7.5%), 28Si ions (263 MeV/n, LET = 78 keV/m, 7.5%), 48Ti ions (1 GeV/n, LET =107 keV/m, 7.5%), and 56Fe ions (1 GeV/n, LET = 151 keV/m, 7.5%) at 0, 25, 50, or 200 cGy) at 4-6 months of age. When the activity over three days of open field habituation were analyzed in female mice, those irradiated with 50 cGy moved less and spent less time in the center than sham-irradiated mice. Sham-irradiated female mice and those irradiated with 25 cGy showed object recognition. However, female mice exposed to 50 or 200 cGy did not show object recognition. When fear memory was assessed in passive avoidance tests, sham-irradiated mice and mice irradiated with 25 cGy showed memory retention while mice exposed to 50 or 200 cGy did not. The effects of radiation passive avoidance memory retention were not sex-dependent. There was no effect of radiation on depressive-like behavior in the forced swim test. There was a trend towards an effect of radiation on BDNF levels in the cortex of males, but not for females, with higher levels in male mice irradiated with 50 cGy than sham-irradiated. Finally, sequential 6-ion irradiation impacted the composition of the gut microbiome in a sex-dependent fashion. Taxa were uncovered whose relative abundance in the gut was associated with the radiation dose received. Thus, exposure to sequential six-beam irradiation significantly affects behavioral and cognitive performance and the gut microbiome.

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  • Prior work has associated the relative abundance of ASVs from Muribaculaceae to various measures of mouse cognition.

    “While the linkage between Muribaculaceae and neurophysiology has been less well documented relative to other mouse microbiome taxa, prior work has associated the relative abundance of ASVs from this group to various measures of mouse cognition48,56.”

    From Integrated analysis of behavioral, epigenetic, and gut microbiome analyses in AppNL-G-F, AppNL-F, and wild type mice (2021) · cites this paper as [48]

  • These genotype-dependent associations include members of the Lachnospiraceae and Ruminococcaceae families.

    “These genotype-dependent associations include members of the Lachnospiraceae and Ruminococcaceae families.”

    From Integrated analysis of behavioral, epigenetic, and gut microbiome analyses in AppNL-G-F, AppNL-F, and wild type mice (2021) · cites this paper as [48]

    The Results > Microbiome passages report sex- and radiation-dose-dependent associations, including some involving Lachnospiraceae, but do not report genotype-dependent associations. The passages found for “genotype” and “Ruminococcaceae” do not identify Ruminococcaceae as part of such an association; our copy therefore does not verify the claim. (LLM, conf=0.74)

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Research works printed but not linked: 2

  1. Kronenberg A. Gauny S. Grossi G. Grygoryev D. Yamazaki J. Torres E. (2018). GDCR Simulation Studies with Human and Mouse Models. Galveston, TX: NASA Human Research Program Investigators’ Workshop.
  2. Liu G. Liu B. Lorello P. McKinney P. Caldarone B. Lemere C. (2017). Short- and long-term sex-specific neurobehavioral effects of 56Fe particle radiation on neurobehavior in WT and AD Tg mice. Paper preseted at the NASA Human Research Program Investigators’ Workshop, (Galveston, TX: NASA).

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Authors
Raber, J., Fuentes Anaya, A., Torres, E. R. S., Lee, J., Boutros, S., Grygoryev, D., Hammer, A., Kasschau, K. D., Sharpton, T. J., Turker, M. S., & Kronenberg, A.
Affiliations
  • Oregon Health & Science University (US)
  • Oregon State University (US)
  • Lawrence Berkeley National Laboratory (US)
Corresponding author
Raber, Jacob
ORCID
Venue
Frontiers in Physiology
Publisher
Frontiers Media SA
Published
2020-08-28
Volume
11
Pages
959-959
ISSN
1664-042X (ISSN-L)
DOI
10.3389/fphys.2020.00959
PMC
PMC7485338
OpenAlex
W3081857396
Cited by
39
References
90
Citations by year
2026: 5 · 2025: 5 · 2024: 9 · 2023: 8 · 2022: 7 · 2021: 5
FWCI
2.44
Type
journal article
Language
en
Open access
Licence
Locations
  • Frontiers in Physiology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • eScholarship (California Digital Library) (submittedVersion)
Funders
  • U.S. Department of Energy (-AC02-05CH11231, Contract No. DE-AC02-05-CH11231, 05CH11231, No. DE-AC02-05-CH11231, DE AC02 05CH11231, DE-AC02-)
  • National Aeronautics and Space Administration (NNX15AK13G, NNJ16HP23I, DE-AC02-05CH11231, 80NSSC19K0498, 80NSSC19K0498-P00001, NSCOR G-00066-4)
  • Nuclear Safety and Security Commission
  • National Synchrotron Radiation Laboratory
  • National Institute on Aging (T32AG055378)
Topics
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Effects of Radiation Exposure
  • Health Sciences › Medicine › Physiology › Spaceflight effects on biology
  • Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Radiation Therapy and Dosimetry
Keywords
galactic cosmic rays, charged particle beams, proton irradiation, helium ions, oxygen ions, silicon ions, titanium ions, iron ions, linear energy transfer, cognitive performance, object recognition memory, fear memory, passive avoidance, depression-like behavior, forced swim test, brain-derived neurotrophic factor, gut microbiota, sex differences, radiation-induced brain injury, space radiation risk

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