Effects of photon irradiation in the presence and absence of hindlimb unloading on the behavioral performance and metabolic pathways in the plasma of Fischer rats

Introduction: The space environment astronauts experience during space missions consists of multiple environmental challenges, including microgravity. In this study, we assessed the behavioral and cognitive performances of male Fisher rats 2 months after sham irradiation or total body irradiation wi...

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Main Authors: Jacob Raber, Sarah Holden, Kat Kessler, Breanna Glaeser, Chloe McQuesten, Mitali Chaudhari, Fiona Stenzel, Marek Lenarczyk, Scott Willem Leonard, Jeffrey Morré, Jaewoo Choi, Amy Kronenberg, Alexander Borg, Andy Kwok, Jan Frederik Stevens, Christopher Olsen, Jeffrey S. Willey, Gerd Bobe, Jessica Minnier, John E. Baker
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-01-01
Series:Frontiers in Physiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fphys.2023.1316186/full
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author Jacob Raber
Jacob Raber
Jacob Raber
Sarah Holden
Kat Kessler
Breanna Glaeser
Chloe McQuesten
Mitali Chaudhari
Fiona Stenzel
Marek Lenarczyk
Scott Willem Leonard
Jeffrey Morré
Jaewoo Choi
Amy Kronenberg
Alexander Borg
Andy Kwok
Jan Frederik Stevens
Jan Frederik Stevens
Christopher Olsen
Jeffrey S. Willey
Gerd Bobe
Gerd Bobe
Jessica Minnier
John E. Baker
author_facet Jacob Raber
Jacob Raber
Jacob Raber
Sarah Holden
Kat Kessler
Breanna Glaeser
Chloe McQuesten
Mitali Chaudhari
Fiona Stenzel
Marek Lenarczyk
Scott Willem Leonard
Jeffrey Morré
Jaewoo Choi
Amy Kronenberg
Alexander Borg
Andy Kwok
Jan Frederik Stevens
Jan Frederik Stevens
Christopher Olsen
Jeffrey S. Willey
Gerd Bobe
Gerd Bobe
Jessica Minnier
John E. Baker
author_sort Jacob Raber
collection DOAJ
description Introduction: The space environment astronauts experience during space missions consists of multiple environmental challenges, including microgravity. In this study, we assessed the behavioral and cognitive performances of male Fisher rats 2 months after sham irradiation or total body irradiation with photons in the absence or presence of simulated microgravity. We analyzed the plasma collected 9 months after sham irradiation or total body irradiation for distinct alterations in metabolic pathways and to determine whether changes to metabolic measures were associated with specific behavioral and cognitive measures.Methods: A total of 344 male Fischer rats were irradiated with photons (6 MeV; 3, 8, or 10 Gy) in the absence or presence of simulated weightlessness achieved using hindlimb unloading (HU). To identify potential plasma biomarkers of photon radiation exposure or the HU condition for behavioral or cognitive performance, we performed regression analyses.Results: The behavioral effects of HU on activity levels in an open field, measures of anxiety in an elevated plus maze, and anhedonia in the M&M consumption test were more pronounced than those of photon irradiation. Phenylalanine, tyrosine, and tryptophan metabolism, and phenylalanine metabolism and biosynthesis showed very strong pathway changes, following photon irradiation and HU in animals irradiated with 3 Gy. Here, 29 out of 101 plasma metabolites were associated with 1 out of 13 behavioral measures. In the absence of HU, 22 metabolites were related to behavioral and cognitive measures. In HU animals that were sham-irradiated or irradiated with 8 Gy, one metabolite was related to behavioral and cognitive measures. In HU animals irradiated with 3 Gy, six metabolites were related to behavioral and cognitive measures.Discussion: These data suggest that it will be possible to develop stable plasma biomarkers of behavioral and cognitive performance, following environmental challenges like HU and radiation exposure.
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spelling doaj.art-1bb6f8739e9d45ff9ac8c715fc29053f2024-01-08T04:17:58ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2024-01-011410.3389/fphys.2023.13161861316186Effects of photon irradiation in the presence and absence of hindlimb unloading on the behavioral performance and metabolic pathways in the plasma of Fischer ratsJacob Raber0Jacob Raber1Jacob Raber2Sarah Holden3Kat Kessler4Breanna Glaeser5Chloe McQuesten6Mitali Chaudhari7Fiona Stenzel8Marek Lenarczyk9Scott Willem Leonard10Jeffrey Morré11Jaewoo Choi12Amy Kronenberg13Alexander Borg14Andy Kwok15Jan Frederik Stevens16Jan Frederik Stevens17Christopher Olsen18Jeffrey S. Willey19Gerd Bobe20Gerd Bobe21Jessica Minnier22John E. Baker23Department of Behavioral Neuroscience, Oregon Health & Science University, Portland, OR, United StatesDepartments of Neurology, and Radiation Medicine, Division of Neuroscience ONPRC, Oregon Health & Science University, Portland, OR, United StatesCollege of Pharmacy, Oregon State University, Corvallis, OR, United StatesDepartment of Behavioral Neuroscience, Oregon Health & Science University, Portland, OR, United StatesDepartment of Behavioral Neuroscience, Oregon Health & Science University, Portland, OR, United StatesNeuroscience Center and Department of Pharmacology and Toxicology, Medical College of Wisconsin, Milwaukee, WI, United StatesDepartment of Behavioral Neuroscience, Oregon Health & Science University, Portland, OR, United StatesDepartment of Behavioral Neuroscience, Oregon Health & Science University, Portland, OR, United StatesDepartment of Behavioral Neuroscience, Oregon Health & Science University, Portland, OR, United StatesRadiation Biosciences Laboratory, Medical College of Wisconsin, Milwaukee, WI, United StatesDepartment of Radiation Oncology, Wake Forest School of Medicine, Winston-Salem, NC, United StatesMass Spectrometry Core, Oregon State University, Corvallis, OR, United StatesLinus Pauling Institute, Oregon State University, Corvallis, OR, United StatesBiological Systems and Engineering Division, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesDepartment of Radiation Oncology, Wake Forest School of Medicine, Winston-Salem, NC, United StatesDepartment of Radiation Oncology, Wake Forest School of Medicine, Winston-Salem, NC, United StatesCollege of Pharmacy, Oregon State University, Corvallis, OR, United StatesLinus Pauling Institute, Oregon State University, Corvallis, OR, United StatesNeuroscience Center and Department of Pharmacology and Toxicology, Medical College of Wisconsin, Milwaukee, WI, United StatesDepartment of Radiation Oncology, Wake Forest School of Medicine, Winston-Salem, NC, United StatesLinus Pauling Institute, Oregon State University, Corvallis, OR, United States0Department of Animal Sciences, Oregon State University, Corvallis, OR, United States1Oregon Health & Science University-Portland State University School of Public Health, Knight Cancer Institute Biostatistics Shared Resource, The Knight Cardiovascular Institute, OR Health & Science University, Portland, OR, United StatesNeuroscience Center and Department of Pharmacology and Toxicology, Medical College of Wisconsin, Milwaukee, WI, United StatesIntroduction: The space environment astronauts experience during space missions consists of multiple environmental challenges, including microgravity. In this study, we assessed the behavioral and cognitive performances of male Fisher rats 2 months after sham irradiation or total body irradiation with photons in the absence or presence of simulated microgravity. We analyzed the plasma collected 9 months after sham irradiation or total body irradiation for distinct alterations in metabolic pathways and to determine whether changes to metabolic measures were associated with specific behavioral and cognitive measures.Methods: A total of 344 male Fischer rats were irradiated with photons (6 MeV; 3, 8, or 10 Gy) in the absence or presence of simulated weightlessness achieved using hindlimb unloading (HU). To identify potential plasma biomarkers of photon radiation exposure or the HU condition for behavioral or cognitive performance, we performed regression analyses.Results: The behavioral effects of HU on activity levels in an open field, measures of anxiety in an elevated plus maze, and anhedonia in the M&M consumption test were more pronounced than those of photon irradiation. Phenylalanine, tyrosine, and tryptophan metabolism, and phenylalanine metabolism and biosynthesis showed very strong pathway changes, following photon irradiation and HU in animals irradiated with 3 Gy. Here, 29 out of 101 plasma metabolites were associated with 1 out of 13 behavioral measures. In the absence of HU, 22 metabolites were related to behavioral and cognitive measures. In HU animals that were sham-irradiated or irradiated with 8 Gy, one metabolite was related to behavioral and cognitive measures. In HU animals irradiated with 3 Gy, six metabolites were related to behavioral and cognitive measures.Discussion: These data suggest that it will be possible to develop stable plasma biomarkers of behavioral and cognitive performance, following environmental challenges like HU and radiation exposure.https://www.frontiersin.org/articles/10.3389/fphys.2023.1316186/fullFischerratsphoton irradiationhindlimb unloadingopen fieldanhedonia
spellingShingle Jacob Raber
Jacob Raber
Jacob Raber
Sarah Holden
Kat Kessler
Breanna Glaeser
Chloe McQuesten
Mitali Chaudhari
Fiona Stenzel
Marek Lenarczyk
Scott Willem Leonard
Jeffrey Morré
Jaewoo Choi
Amy Kronenberg
Alexander Borg
Andy Kwok
Jan Frederik Stevens
Jan Frederik Stevens
Christopher Olsen
Jeffrey S. Willey
Gerd Bobe
Gerd Bobe
Jessica Minnier
John E. Baker
Effects of photon irradiation in the presence and absence of hindlimb unloading on the behavioral performance and metabolic pathways in the plasma of Fischer rats
Frontiers in Physiology
Fischer
rats
photon irradiation
hindlimb unloading
open field
anhedonia
title Effects of photon irradiation in the presence and absence of hindlimb unloading on the behavioral performance and metabolic pathways in the plasma of Fischer rats
title_full Effects of photon irradiation in the presence and absence of hindlimb unloading on the behavioral performance and metabolic pathways in the plasma of Fischer rats
title_fullStr Effects of photon irradiation in the presence and absence of hindlimb unloading on the behavioral performance and metabolic pathways in the plasma of Fischer rats
title_full_unstemmed Effects of photon irradiation in the presence and absence of hindlimb unloading on the behavioral performance and metabolic pathways in the plasma of Fischer rats
title_short Effects of photon irradiation in the presence and absence of hindlimb unloading on the behavioral performance and metabolic pathways in the plasma of Fischer rats
title_sort effects of photon irradiation in the presence and absence of hindlimb unloading on the behavioral performance and metabolic pathways in the plasma of fischer rats
topic Fischer
rats
photon irradiation
hindlimb unloading
open field
anhedonia
url https://www.frontiersin.org/articles/10.3389/fphys.2023.1316186/full
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