Executive Function in Rats is Impaired by Low (20 cGy) Doses of 1 GeV/u56Fe Particles

Lonart, György; Parris, Brian; Johnson, Angela M.; Miles, Scott; Sanford, Larry D.; Singletary, Sylvia J.; Britten, Richard A.

doi:10.1667/rr2862.1

Cited by 70Spaceflight effects on biologyEffects of Radiation ExposureRadiation Therapy and Dosimetry

Executive Function in Rats is Impaired by Low (20 cGy) Doses of 1 GeV/u56Fe Particles

Lonart, György, Parris, Brian, Johnson, Angela M., Miles, Scott, Sanford, Larry D., Singletary, Sylvia J., Britten, Richard A.·2012·Radiation Research

DOI 10.1667/rr2862.1

Open this paper in CoChat — free account

Abstract

Exposure to galactic cosmic radiation is a potential health risk in long-term space travel and represents a significant risk to the central nervous system. The most harmful component of galactic cosmic radiation is the HZE [high mass, highly charged (Z), high energy] particles, e.g., (56)Fe particle. In previous ground-based experiments, exposure to doses of HZE-particle radiation that an astronaut will receive on a deep space mission (i.e., ∼20 cGy) resulted in pronounced deficits in hippocampus-dependent learning and memory in rodents. Neurocognitive tasks that are dependent upon other regions of the brain, such as the striatum, are also impaired after exposure to low HZE-particle doses. These data raise the possibility that neurocognitive tasks regulated by the prefrontal cortex could also be impaired after exposure to mission relevant HZE-particle doses, which may prevent astronauts from performing complex executive functions. To assess the effects of mission relevant (20 cGy) doses of 1 GeV/u (56)Fe particles on executive function, male Wistar rats received either sham treatment or were irradiated and tested 3 months later for their ability to perform attentional set shifting. Compared to the controls, rats that received 20 cGy of 1 GeV/u (56)Fe particles showed significant impairments in their ability to complete the attentional set-shifting test, with only 17% of irradiated rats completing all stages as opposed to 78% of the control rats. The majority of failures (60%) occurred at the first reversal stage, and half of the remaining animals failed at the extra-dimensional shift phase of the studies. The irradiated rats that managed to complete the tasks did so with approximately the same ease as did the control rats. These observations suggest that exposure to mission relevant doses of 1 GeV/u (56)Fe particles results in the loss of functionality in several regions of the cortex: medical prefrontal cortex, anterior cingulated cortex, posterior cingulated cortex and the basal forebrain. Our observation that 20 cGy of 1 GeV/u (56)Fe particles is sufficient to impair the ability of rats to conduct attentional set-shifting raises the possibility that astronauts on prolonged deep space exploratory missions could subsequently develop deficits in executive function.

Integrity signals

Registry

Crossref · 10.1667/rr2862.1

Cites

25 of 25 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

These findings raise the possibility that astronauts on prolonged deep space exploratory missions could develop deficits in executive function.
“These findings raise the possibility that astronauts on prolonged deep space exploratory missions could develop deficits in executive function [56].”
From Space Radiation: The number one risk to astronaut health beyond low earth orbit (2014) · cites this paper as [56]
Britten et al. have shown that doses as low as 20 cGy of simulated GCR radiation (1 GeV/u 56Fe particles) can significantly impair learning and memory in a rodent model.
“Britten et al. have shown that doses as low as 20 cGy of simulated GCR radiation (1 GeV/u 56Fe particles) can significantly impair learning and memory in a rodent model.”
From Space Radiation: The number one risk to astronaut health beyond low earth orbit (2014) · cites this paper as [56]
Mission-relevant doses of HZE particles may result in deficits in hippocampus-dependent neurocognitive tasks, most likely due to the perturbation of multiple processes, in addition to killing neuronal cells.
“These results demonstrate that mission-relevant doses of HZE particles may result in deficits in hippocampus-dependent neurocognitive tasks, most likely due to the perturbation of multiple processes, in addition to killing neuronal cells [55,56].”
From Space Radiation: The number one risk to astronaut health beyond low earth orbit (2014) · cites this paper as [56]

Exploring the Central Executive
Baddeley, A. (1996) · The Quarterly Journal of Experimental Psychology Section A · doi:10.1080/713755608 · Cited by 2,390 · see citing works
A simple objective technique for measuring flexibility in thinking
Berg, E. A. (1948) · The Journal of General Psychology · doi:10.1080/00221309.1948.9918159 · Cited by 2,255 · see citing works
Medial Frontal Cortex Mediates Perceptual Attentional Set Shifting in the Rat
Birrell, J. M., & Brown, V. J. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-11-04320.2000 · Cited by 1,421 · see citing works
Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates
Dalley, J. W., Cardinal, R. N., & Robbins, T. W. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.09.006 · Cited by 1,329 · see citing works
Stress-Induced Alterations in Prefrontal Cortical Dendritic Morphology Predict Selective Impairments in Perceptual Attentional Set-Shifting
Liston, C., Miller, M. M., Goldwater, D. S., Radley, J. J., Rocher, A. B., Hof, P. R., Morrison, J. H., & McEwen, B. S. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.1184-06.2006 · Cited by 968 · see citing works
Synchronized activity between the ventral hippocampus and the medial prefrontal cortex during anxiety
Adhikari, A., Topiwala, M. A., & Gordon, J. A. (2010) · Neuron · doi:10.1016/j.neuron.2009.12.002 · Cited by 729 · see citing works
Extra-dimensional versus intra-dimensional set shifting performance following frontal lobe excisions, temporal lobe excisions or amygdalo-hippocampectomy in man
Owen, A. M., Roberts, A. C., Polkey, C. E., Sahakian, B. J., & Robbins, T. W. (1991) · Neuropsychologia · doi:10.1016/0028-3932(91)90063-e · Cited by 657 · see citing works
Catecholamine Influences on Dorsolateral Prefrontal Cortical Networks
Arnsten, A. F. T. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.01.027 · Cited by 493 · see citing works
Double dissociation of the effects of medial and orbital prefrontal cortical lesions on attentional and affective shifts in mice
Bissonette, G. B., Martins, G. J., Franz, T. M., Harper, E. S., Schoenbaum, G., & Powell, E. M. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.2820-08.2008 · Cited by 353 · see citing works
Aged Rats Are Impaired on an Attentional Set-Shifting Task Sensitive to Medial Frontal Cortex Damage in Young RatsPreprint
Barense, M. D., Fox, M. T., & Baxter, M. G. (2002) · Learning & Memory · doi:10.1101/lm.48602 · Cited by 183 · see citing works
Low (20 cGy) Doses of 1 GeV/u56Fe-Particle Radiation Lead to a Persistent Reduction in the Spatial Learning Ability of Rats
Britten, R. A., Davis, L. K., Johnson, A. M., Keeney, S., Siegel, A., Sanford, L. D., Singletary, S. J., & Lonart, G. (2012) · Radiation Research · doi:10.1667/rr2637.1 · Cited by 134 · see citing works
Self-citation
Low (60 cGy) Doses of56Fe HZE-Particle Radiation Lead to a Persistent Reduction in the Glutamatergic Readily Releasable Pool in Rat Hippocampal Synaptosomes
Machida, M., Lónárt, G., & Britten, R. A. (2010) · Radiation Research · doi:10.1667/rr1988.1 · Cited by 108 · see citing works
Self-citation
Double Dissociation of Attentional Resources: Prefrontal Versus Cingulate Cortices
Ng, C.-W., Noblejas, M. I., Rodefer, J. S., Smith, C. B., & Poremba, A. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2745-07.2007 · Cited by 105 · see citing works
Reversal-Specific Learning Impairments After a Binge Regimen of Methamphetamine in Rats: Possible Involvement of Striatal Dopamine
Izquierdo, A., Belcher, A. M., Scott, L., Cazares, V. A., Chen, J. C., O’Dell, S. J., Malvaez, M., Wu, T. Z., & Marshall, J. F. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.155 · Cited by 94 · see citing works
Exposure to16O-Particle Radiation Causes Aging-Like Decrements in Rats through Increased Oxidative Stress, Inflammation and Loss of Autophagy
Poulose, S. M., Bielinski, D. F., Carrihill-Knoll, K. L., Rabin, B. M., & Shukitt‐Hale, B. (2011) · Radiation Research · doi:10.1667/rr2605.1 · Cited by 77 · see citing works
Glutamate receptor binding in the frontal cortex and dorsal striatum of aged rats with impaired attentional set‐shifting
Nicolle, M. M., & Baxter, M. G. (2003) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2003.03077.x · Cited by 71 · see citing works
Lesions of the basal forebrain impair reversal learning but not shifting of attentional set in rats
Tait, D. S., & Brown, V. J. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.08.035 · Cited by 70 · see citing works
Managing Lunar and Mars Mission Radiation Risks Part I: Cancer Risks, Uncertainties, and Shielding Effectiveness
Cucinotta, F. A., & Johnson, L. B. (2005) · Cited by 63 · see citing works
Cosmic ray hit frequencies in critical sites in the central nervous system
Curtis, S. B., Vazquez, M. E., Wilson, J. W., Atwell, W., Kim, M. Y., & Capala, J. (1998) · Advances in Space Research · doi:10.1016/s0273-1177(98)80011-2 · Cited by 60 · see citing works
56Fe-Particle Radiation Reduces Neuronal Output and Attenuates Lipopolysaccharide-Induced Inhibition of Long-Term Potentiation in the Mouse Hippocampus
Vlkolinský, R., Krucker, T., Nelson, G. A., & Obenaus, A. (2008) · Radiation Research · doi:10.1667/rr1228.1 · Cited by 58 · see citing works
Effects of Lipopolysaccharide on56Fe-Particle Radiation-Induced Impairment of Synaptic Plasticity in the Mouse Hippocampus
Vlkolinský, R., Krucker, T., Smith, A., Lamp, T., Nelson, G. A., & Obenaus, A. (2007) · Radiation Research · doi:10.1667/rr1038.1 · Cited by 53 · see citing works
Operant responding following exposure to HZE particles and its relationship to particle energy and linear energy transfer
Rabin, B. M., Carrihill-Knoll, K. L., & Shukitt‐Hale, B. (2011) · Advances in Space Research · doi:10.1016/j.asr.2011.03.008 · Cited by 46 · see citing works
Effects of HZE particle on the nigrostriatal dopaminergic system in a future mars mission
Koike, Y., Frey, M., Sahiar, F., Dodge, R. E., & Mohler, S. R. (2004) · Acta Astronautica · doi:10.1016/j.actaastro.2004.05.068 · Cited by 21 · see citing works
The Effect of X-irradiation on the Amount of Catecholamines in Heart Atria and Hypothalamus of the Rabbit, and in Brain and Heart of the Rat
Varagić, V. M., Stepanović, S., Svecenski, N. B., & Hajduković, S. (1967) · International Journal of Radiation Biology and Related Studies in Physics Chemistry and Medicine · doi:10.1080/09553006714550511 · Cited by 19 · see citing works
Gamma Radiation and Release of Norepinephrine in the Hippocampus
Kandasamy, S. B. (1999) · Advances in experimental medicine and biology · doi:10.1007/978-1-4615-4793-8_94 · Cited by 4 · see citing works

Flagged first, then by citations

Sorted by citations

Space Radiation: The number one risk to astronaut health beyond low earth orbit
Chancellor, J., Scott, G., & Sutton, J. (2014) · Life · doi:10.3390/life4030491 · Cited by 455 · see citing works
Space radiation risks to the central nervous system
Cucinotta, F. A., Alp, M., Sulzman, F. M., & Wang, M. (2014) · Life Sciences in Space Research · doi:10.1016/j.lssr.2014.06.003 · Cited by 262 · see citing works
Cosmic radiation exposure and persistent cognitive dysfunction
Parihar, V. K., Allen, B. D., Caressi, C., Kwok, S., Chu, E., Tran, K. K., Chmielewski, N. N., Giedzinski, E., Acharya, M. M., Britten, R. A., et al. (2016) · Scientific Reports · doi:10.1038/srep34774 · Cited by 221 · see citing works
Self-citation
What happens to your brain on the way to Mars
Parihar, V. K., Allen, B., Tran, K. K., Macaraeg, T. G., Chu, E. M., Kwok, S. F., Chmielewski, N. N., Craver, B. M., Baulch, J. E., Acharya, M. M., et al. (2015) · Science Advances · doi:10.1126/sciadv.1400256 · Cited by 217 · see citing works
Biological effects of space radiation and development of effective countermeasures
Kennedy, A. R. (2014) · Life Sciences in Space Research · doi:10.1016/j.lssr.2014.02.004 · Cited by 188 · see citing works
Persistent changes in neuronal structure and synaptic plasticity caused by proton irradiation
Parihar, V. K., Pasha, J., Tran, K. K., Craver, B. M., Acharya, M. M., & Limoli, C. L. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0709-9 · Cited by 165 · see citing works
Functional Consequences of Radiation-Induced Oxidative Stress in Cultured Neural Stem Cells and the Brain Exposed to Charged Particle Irradiation
Tseng, B. P., Giedzinski, E., Izadi, A., Suarez, T., Lan, M. L., Tran, K. K., Acharya, M. M., Nelson, G. A., Raber, J., Parihar, V. K., et al. (2013) · Antioxidants and Redox Signaling · doi:10.1089/ars.2012.5134 · Cited by 135 · see citing works
Persistent nature of alterations in cognition and neuronal circuit excitability after exposure to simulated cosmic radiation in mice
Parihar, V. K., Maroso, M., Syage, A., Allen, B. D., Angulo, M. C., Soltesz, I., & Limoli, C. L. (2018) · Experimental Neurology · doi:10.1016/j.expneurol.2018.03.009 · Cited by 127 · see citing works
Individual Differences in Attentional Deficits and Dopaminergic Protein Levels following Exposure to Proton Radiation
Davis, C. M., DeCicco-Skinner, K. L., Roma, P. G., & Hienz, R. D. (2014) · Radiation Research · doi:10.1667/rr13359.1 · Cited by 101 · see citing works
Behavioral effects of space radiation: A comprehensive review of animal studies
Kiffer, F. C., Boerma, M., & Allen, A. R. (2019) · Life Sciences in Space Research · doi:10.1016/j.lssr.2019.02.004 · Cited by 95 · see citing works
Targeted Overexpression of Mitochondrial Catalase Prevents Radiation-Induced Cognitive Dysfunction
Parihar, V. K., Allen, B. D., Tran, K. K., Chmielewski, N. N., Craver, B. M., Martirosian, V., Morganti, J. M., Rosi, S., Vlkolinský, R., Acharya, M. M., et al. (2014) · Antioxidants and Redox Signaling · doi:10.1089/ars.2014.5929 · Cited by 89 · see citing works
Exposure to Mission Relevant Doses of 1 GeV/Nucleon56Fe Particles Leads to Impairment of Attentional Set-Shifting Performance in Socially Mature Rats
Britten, R. A., Davis, L. K., Jewell, J. S., Miller, V. D., Hadley, M. M., Sanford, L. D., Machida, M., & Lónárt, G. (2014) · Radiation Research · doi:10.1667/rr3766.1 · Cited by 75 · see citing works
Self-citation
The Burden of Space Exploration on the Mental Health of Astronauts: A Narrative Review.
Arone, A., Ivaldi, T., Loganovsky, K., Palermo, S., Parra, E., Flamini, W., & Marazziti, D. (2021) · PubMed Central · doi:10.36131/cnfioritieditore20210502 · Cited by 70 · see citing works
Space–brain: The negative effects of space exposure on the central nervous system
Limoli, C., Jandial, R., Hoshide, R., & Waters, J. (2018) · Surgical Neurology International · doi:10.4103/sni.sni_250_17 · Cited by 66 · see citing works
Understanding the Effects of Deep Space Radiation on Nervous System: The Role of Genetically Tractable Experimental Models
Onorato, G., Schiavi, E. D., & Cunto, F. D. (2020) · Frontiers in Physics · doi:10.3389/fphy.2020.00362 · Cited by 60 · see citing works
Acute and Fractionated Exposure to High-LET56Fe HZE-Particle Radiation Both Result in Similar Long-Term Deficits in Adult Hippocampal Neurogenesis
Rivera, P. D., Shih, H.-Y., LeBlanc, J. A., Cole, M. G., Amaral, W. Z., Mukherjee, S., Zhang, S., Lucero, M. J., DeCarolis, N. A., Chen, B. P. C., et al. (2013) · Radiation Research · doi:10.1667/rr13480.1 · Cited by 61 · see citing works
Impact of spaceflight stressors on behavior and cognition: A molecular, neurochemical, and neurobiological perspective
Desai, R. I., Limoli, C. L., Stark, C. E. L., & Stark, S. M. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104676 · Cited by 55 · see citing works
Neurophysiology of space travel: energetic solar particles cause cell type-specific plasticity of neurotransmission
Lee, S.-H., Dudok, B., Parihar, V. K., Jung, K., Zöldi, M., Kang, Y., Maroso, M., Alexander, A., Nelson, G. A., Piomelli, D., et al. (2016) · Brain Structure and Function · doi:10.1007/s00429-016-1345-3 · Cited by 53 · see citing works
Mitochondrial-Targeted Human Catalase Affords Neuroprotection From Proton Irradiation
Liao, A. C., Craver, B. M., Tseng, B. P., Tran, K. K., Parihar, V. K., Acharya, M. M., & Limoli, C. L. (2013) · Radiation Research · doi:10.1667/rr3339.1 · Cited by 49 · see citing works
Noninvasive Brain Stimulation & Space Exploration: Opportunities and Challenges
Romanella, S. M., Sprugnoli, G., Ruffini, G., Seyedmadani, K., Rossi, S., & Santarnecchi, E. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.09.005 · Cited by 48 · see citing works
Risk of defeats in the central nervous system during deep space missions
Kokhan, V. S., Матвеева, М. И., Mukhametov, A., & Shtemberg, A. S. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.10.006 · Cited by 46 · see citing works
Impaired Spatial Memory Performance in Adult Wistar Rats Exposed to Low (5–20 cGy) Doses of 1 GeV/n56Fe Particles
Britten, R. A., Jewell, J. S., Miller, V. D., Davis, L. K., Hadley, M. M., & Wyrobek, A. J. (2016) · Radiation Research · doi:10.1667/rr14120.1 · Cited by 42 · see citing works
Self-citation
Exposure to ≤15 cGy of 600 MeV/n 56Fe Particles Impairs Rule Acquisition but not Long-Term Memory in the Attentional Set-Shifting Assay
Jewell, J. S., Duncan, V. D., Fesshaye, A. S., Tondin, A., Macadat, E., & Britten, R. A. (2018) · Radiation Research · doi:10.1667/rr15085.1 · Cited by 41 · see citing works
Self-citation
Space missions: psychological and psychopathological issues
Marazziti, D., Arone, A., Ivaldi, T., Kuts, K., & Loganovsky, K. (2021) · CNS Spectrums · doi:10.1017/s1092852921000535 · Cited by 39 · see citing works
Evaluation of deep space exploration risks and mitigations against radiation and microgravity
Dobney, W., Mols, L., Mistry, D., Tabury, K., Baselet, B., & Baatout, S. (2023) · Frontiers in Nuclear Medicine · doi:10.3389/fnume.2023.1225034 · Cited by 73 · see citing works
Progressive increase in the complexity and translatability of rodent testing to assess space-radiation induced cognitive impairment
Britten, R. A., Wellman, L. L., & Sanford, L. D. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.01.027 · Cited by 36 · see citing works
Self-citation
Exposure to Mission-Relevant Doses of 1 GeV/n48Ti Particles Impairs Attentional Set-Shifting Performance in Retired Breeder Rats
Hadley, M. M., Davis, L. K., Jewell, J. S., Miller, V. D., & Britten, R. A. (2015) · Radiation Research · doi:10.1667/rr14086.1 · Cited by 35 · see citing works
Self-citation
Impaired Attentional Set-Shifting Performance after Exposure to 5 cGy of 600 MeV/n28Si Particles
Britten, R. A., Jewell, J. S., Duncan, V. D., Hadley, M. M., Macadat, E., Musto, A. E., & Tessa, C. L. (2018) · Radiation Research · doi:10.1667/rr14627.1 · Cited by 35 · see citing works
Self-citation
Predictions of cognitive detriments from galactic cosmic ray exposures to astronauts on exploration missions
Cucinotta, F. A., & Cacao, E. (2020) · Life Sciences in Space Research · doi:10.1016/j.lssr.2019.10.004 · Cited by 34 · see citing works
Liver irradiation causes distal bystander effects in the rat brain and affects animal behaviour
KOVALCHUK, A. V., Mychasiuk, R., Muhammad, A., Hossain, S., Ilnytskyy, S., Ghose, A., Kirkby, C., Ghasroddashti, E., Kovalchuk, O., & Kolb, B. E. (2015) · Oncotarget · doi:10.18632/oncotarget.6596 · Cited by 33 · see citing works
Different Sequences of Fractionated Low-Dose Proton and Single Iron-Radiation-Induced Divergent Biological Responses in the Heart
Sasi, S. P., Yan, X., Zuriaga-Herrero, M., Gee, H., Lee, J., Mehrzad, R., Song, J., Onufrak, J., Morgan, J., Enderling, H., et al. (2017) · Radiation Research · doi:10.1667/rr14667.1 · Cited by 32 · see citing works
Comparison of the Effectiveness of Exposure to Low-LET Helium Particles (4He) and Gamma Rays (137Cs) on the Disruption of Cognitive Performance
Rabin, B. M., Carrihill-Knoll, K. L., & Shukitt‐Hale, B. (2015) · Radiation Research · doi:10.1667/rr14001.1 · Cited by 32 · see citing works
Combined effects of antiorthostatic suspension and ionizing radiation on the behaviour and neurotransmitters changes in different brain structures of rats
Kokhan, V. S., Матвеева, М. И., Bazyan, A. S., Кудрин, В. С., Mukhametov, A., & Shtemberg, A. S. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.10.032 · Cited by 33 · see citing works
Alterations in synaptic density and myelination in response to exposure to high‐energy charged particles
Dickstein, D. L., Talty, R., Bresnahan, E. R., Varghese, M., Perry, B. C., Janssen, W. G. M., Sowa, A., Giedzinski, E., Apodaca, L. A., Baulch, J. E., et al. (2018) · The Journal of Comparative Neurology · doi:10.1002/cne.24530 · Cited by 33 · see citing works
Consequences of space radiation on the brain and cardiovascular system
Davis, C. M., Allen, A. R., & Bowles, D. E. (2021) · Journal of Environmental Science and Health Part C · doi:10.1080/26896583.2021.1891825 · Cited by 30 · see citing works
Dose-Effects Models for Space Radiobiology: An Overview on Dose-Effect Relationships
Strigari, L., Strolin, S., MORGANTI, A. G., & Bartoloni, A. (2021) · Frontiers in Public Health · doi:10.3389/fpubh.2021.733337 · Cited by 31 · see citing works
Modeling Heavy-Ion Impairment of Hippocampal Neurogenesis after Acute and Fractionated Irradiation
Cacao, E., & Cucinotta, F. A. (2016) · Radiation Research · doi:10.1667/rr14569.1 · Cited by 29 · see citing works
Brains in space: impact of microgravity and cosmic radiation on the CNS during space exploration
Wuyts, F. L., Deblieck, C., Vandevoorde, C., & Durante, M. (2025) · Nature reviews. Neuroscience · doi:10.1038/s41583-025-00923-4 · Cited by 29 · see citing works
Whole-Body Oxygen (16O) Ion-Exposure-Induced Impairments in Social Odor Recognition Memory in Rats are Dose and Time Dependent
Mange, A., Cao, Y., Zhang, S., Hienz, R. D., & Davis, C. M. (2018) · Radiation Research · doi:10.1667/rr14849.1 · Cited by 28 · see citing works
Individual variations in dose response for spatial memory learning among outbred wistar rats exposed from 5 to 20 cGy of 56Fe particles
Wyrobek, A. J., & Britten, R. A. (2016) · Environmental and Molecular Mutagenesis · doi:10.1002/em.22018 · Cited by 26 · see citing works
Self-citation
The psychological consequences of (perceived) ionizing radiation exposure: a review on its role in radiation-induced cognitive dysfunction
Collett, G., Craenen, K., Young, W. R., Gilhooly, M., & Anderson, R. M. (2020) · International Journal of Radiation Biology · doi:10.1080/09553002.2020.1793017 · Cited by 26 · see citing works
Cortical Glutamate/GABA Imbalance after Combined Radiation Exposure: Relevance to Human Deep-Space Missions
Kokhan, V. S., Anokhin, P. K., Belov, O., & Gulyaev, M. V. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2019.08.009 · Cited by 26 · see citing works
Modeling Impaired Hippocampal Neurogenesis after Radiation Exposure
Cacao, E., & Cucinotta, F. A. (2016) · Radiation Research · doi:10.1667/rr14289.s1 · Cited by 24 · see citing works
Performance in hippocampus- and PFC-dependent cognitive domains are not concomitantly impaired in rats exposed to 20 cGy of 1 GeV/n 56Fe particles
Britten, R. A., Miller, V. D., Hadley, M. M., Jewell, J. S., & Macadat, E. (2016) · Life Sciences in Space Research · doi:10.1016/j.lssr.2016.06.005 · Cited by 23 · see citing works
Self-citation
Biophysics Model of Heavy-Ion Degradation of Neuron Morphology in Mouse Hippocampal Granular Cell Layer Neurons
Alp, M., & Cucinotta, F. A. (2018) · Radiation Research · doi:10.1667/rr14923.1 · Cited by 22 · see citing works
Spatial Memory Performance of Socially Mature Wistar Rats is Impaired after Exposure to Low (5 cGy) Doses of 1 GeV/n48Ti Particles
Britten, R. A., Jewell, J. S., Duncan, V. D., Davis, L. K., Hadley, M. M., & Wyrobek, A. J. (2017) · Radiation Research · doi:10.1667/rr14550.1 · Cited by 21 · see citing works
Self-citation
Lack of reliability in the disruption of cognitive performance following exposure to protons
Rabin, B. M., Heroux, N. A., Shukitt‐Hale, B., Carrihill-Knoll, K. L., Beck, Z., & Baxter, C. F. (2015) · Radiation and Environmental Biophysics · doi:10.1007/s00411-015-0597-2 · Cited by 20 · see citing works
Long-Term Sex- and Genotype-Specific Effects of 56Fe Irradiation on Wild-Type and APPswe/PS1dE9 Transgenic Mice
Schroeder, M. K., Liu, B., Hinshaw, R. G., Park, M., Wang, S., Dubey, S., Liu, G. G., Shi, Q., Holton, P., Reiser, V., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222413305 · Cited by 19 · see citing works
Whole-Body 12C Irradiation Transiently Decreases Mouse Hippocampal Dentate Gyrus Proliferation and Immature Neuron Number, but Does Not Change New Neuron Survival Rate
Zanni, G., Deutsch, H. M., Rivera, P. D., Shih, H.-Y., LeBlanc, J. A., Amaral, W. Z., Lucero, M., Redfield, R. L., DeSalle, M. J., Chen, B. P. C., et al. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19103078 · Cited by 18 · see citing works
Effects of x-ray radiation on complex visual discrimination learning and social recognition memory in rats
Davis, C. M., Roma, P. G., Armour, E., Gooden, V. L., Brady, J. V., Weed, M. R., & Hienz, R. D. (2014) · PLoS ONE · doi:10.1371/journal.pone.0104393 · Cited by 15 · see citing works
Differential organization of open field behavior in mice following acute or chronic simulated GCR exposure
Schaeffer, E. A., Blackwell, A. A., Oltmanns, J. R. O., Einhaus, R. M., Lake, R. I., Hein, C., Baulch, J. E., Limoli, C. L., Ton, S. T., Kartje, G. L., et al. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113577 · Cited by 15 · see citing works
56Fe irradiation-induced cognitive deficits through oxidative stress in mice
Yan, J., Liu, Y., Zhao, Q., Li, J., Mao, A., Li, H., Di, C., & Zhang, H. (2016) · Toxicology Research · doi:10.1039/c6tx00282j · Cited by 12 · see citing works
Solving the Issue of Ionizing Radiation Induced Neurotoxicity by Using Novel Cell Models and State of the Art Accelerator Facilities
Schielke, C., Hartel, C., Durante, M., Ritter, S., & Schroeder, I. S. (2020) · Frontiers in Physics · doi:10.3389/fphy.2020.568027 · Cited by 9 · see citing works
A voyage to Mars: Space radiation, aging, and nutrition
Rabin, B. M., & Shukitt‐Hale, B. (2014) · Nutrition and Aging · doi:10.3233/nua-140045 · Cited by 10 · see citing works
Ion beams for space radiation radiobiological effect studies
Chew, M. T., Nisbet, A., Jones, B., Suzuki, M., Matsufuji, N., Murakami, T., & Bradley, D. A. (2019) · Radiation Physics and Chemistry · doi:10.1016/j.radphyschem.2019.108373 · Cited by 8 · see citing works
Nonhuman primate models in the study of spaceflight stressors: Past contributions and future directions
Desai, R. I., Kangas, B. D., & Limoli, C. L. (2021) · Life Sciences in Space Research · doi:10.1016/j.lssr.2021.03.008 · Cited by 8 · see citing works
Machine Learning Models to Predict Cognitive Impairment of Rodents Subjected to Space Radiation
Matar, M., Gökoğlu, S. A., Prelich, M. T., Gallo, C. A., Iqbal, A. K., Britten, R. A., Prabhu, R. K., & Myers, J. G. (2021) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2021.713131 · Cited by 7 · see citing works
Self-citation
Radiation neurobiology of long-term spaceflights
Олегович, С. А., Ушаков, И. Б., Sapetsky, N. V., Shtemberg, A. S., Kositsin, N. S., & Timofeev, N. N. (2017) · Biology Bulletin Reviews · doi:10.1134/s2079086417060068 · Cited by 6 · see citing works
Synergistic Effect of High Charge and Energy Particle Radiation and Chronological Age on Biomarkers of Oxidative Stress and Tissue Degeneration: A Ground-Based Study Using the Vertebrate Laboratory Model Organism Oryzias latipes
Zheng, X., Zhang, X., Ding, L., Lee, J. R., Weinberger, P., & Dynan, W. S. (2014) · PLoS ONE · doi:10.1371/journal.pone.0111362 · Cited by 6 · see citing works
Particle radiation-induced dysregulation of protein homeostasis in primary human and mouse neuronal cells
Shaler, T., Lin, H., Bakke, J. P., Chen, S., Grover, A., & Chang, P. Y. (2020) · Life Sciences in Space Research · doi:10.1016/j.lssr.2020.02.003 · Cited by 6 · see citing works
Neuroinflammatory Signaling and Immune Cell Infiltration Differ in Brains of Rats Exposed to Space Radiation and Social Isolation
Adkins, A. M., Luyo, Z. N. M., Boden, A. F., Heerbrandt, R. S., Britten, R. A., Wellman, L. L., & Sanford, L. D. (2025) · Life · doi:10.3390/life15050747 · Cited by 3 · see citing works
Self-citation
Impact of Breathing 100% Oxygen on Radiation-Induced Cognitive Impairment
Wheeler, K. T., Payne, V. S., D'Agostino, R. B., Walb, M. C., Munley, M. T., Metheny‐Barlow, L. J., & Robbins, M. E. C. (2014) · Radiation Research · doi:10.1667/rr13643.1 · Cited by 3 · see citing works
The Impact of Space Radiation on Brains of Future Martian and Lunar Explorers
Li, Y., Guo, J., Khaksarighiri, S., Dobynde, M. I., Zhang, J., Liu, B., & Wimmer-Schweingruber, R. F. (2023) · Space Weather · doi:10.1029/2023sw003470 · Cited by 2 · see citing works
Telemetry in Rats and Mice: Methodological Considerations and Example Studies of Stress and Anxiety in Ground-Based Spaceflight Analogs
Wellman, L. L., Adkins, A. M., Yoon, H., Britten, R. A., & Sanford, L. D. (2022) · Neuromethods · doi:10.1007/978-1-0716-2748-8_11 · Cited by 2 · see citing works
Self-citation
Elucidation of dose-dependent transcriptional events immediately following ionizing radiation exposurePreprint
Rouchka, E. C., Flight, R. M., Fasciotto, B. H., Estrada, R., Eaton, J. W., Patibandla, P. K., Waigel, S. J., Li, D., Kirtley, J. K., Sethu, P., et al. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/207951 · Cited by 2 · see citing works
A Two-Hit Model of Executive Dysfunction: Simulated Galactic Cosmic Radiation Primes Latent Deficits Revealed by Sleep Fragmentation
Britten, R. A., Tamgue, E. N., Arriaga, P. A., Fesshaye, A. S., & Sanford, L. D. (2025) · Life · doi:10.3390/life15111717 · Cited by 1 · see citing works
Self-citation
Effects of cancer therapies on the brain : from molecular mechanisms to behavioral outcomes
Kovalchuk, A. (2015) · Open ULeth Scholarship (OPUS) (University of Lethbridge)
NASA Space Radiation Program Element: Research Overview
Huff, J. L. (2014) · NASA STI Repository (National Aeronautics and Space Administration)
A Bibliometric Analysis of Research Examining How Space Radiation Affects Human and Rodent Cognition, 1990–2023
Simmons, P., Swinton, C., Simmons, S., McElroy, T., & Allen, A. R. (2024) · Radiation · doi:10.3390/radiation5010001
Sex Differences in Freezing Behavior and Extinction Learning Among Wistar Rats Exposed to Social Isolation and 15 cGy GCRsim Space Radiation Both Alone and in Combination
Luyo, Z. N. M., Heerbrandt, R. S., Boden, A. F., Keumeni, F. E. E., Britten, R. A., Wellman, L. L., & Sanford, L. D. (2026) · Life · doi:10.3390/life16101638
Self-citation

Low (20 cGy) Doses of 1 GeV/u56Fe-Particle Radiation Lead to a Persistent Reduction in the Spatial Learning Ability of Rats
Britten, R. A., Davis, L. K., Johnson, A. M., Keeney, S., Siegel, A., Sanford, L. D., Singletary, S. J., & Lonart, G. (2012) · Radiation Research · doi:10.1667/rr2637.1 · Cited by 134 · see citing works
Self-citation
Impaired Spatial Memory Performance in Adult Wistar Rats Exposed to Low (5–20 cGy) Doses of 1 GeV/n56Fe Particles
Britten, R. A., Jewell, J. S., Miller, V. D., Davis, L. K., Hadley, M. M., & Wyrobek, A. J. (2016) · Radiation Research · doi:10.1667/rr14120.1 · Cited by 42 · see citing works
Self-citation
Performance in hippocampus- and PFC-dependent cognitive domains are not concomitantly impaired in rats exposed to 20 cGy of 1 GeV/n 56Fe particles
Britten, R. A., Miller, V. D., Hadley, M. M., Jewell, J. S., & Macadat, E. (2016) · Life Sciences in Space Research · doi:10.1016/j.lssr.2016.06.005 · Cited by 23 · see citing works
Self-citation
Spatial Memory Performance of Socially Mature Wistar Rats is Impaired after Exposure to Low (5 cGy) Doses of 1 GeV/n48Ti Particles
Britten, R. A., Jewell, J. S., Duncan, V. D., Davis, L. K., Hadley, M. M., & Wyrobek, A. J. (2017) · Radiation Research · doi:10.1667/rr14550.1 · Cited by 21 · see citing works
Self-citation
Exposure to ≤15 cGy of 600 MeV/n 56Fe Particles Impairs Rule Acquisition but not Long-Term Memory in the Attentional Set-Shifting Assay
Jewell, J. S., Duncan, V. D., Fesshaye, A. S., Tondin, A., Macadat, E., & Britten, R. A. (2018) · Radiation Research · doi:10.1667/rr15085.1 · Cited by 41 · see citing works
Self-citation

Authors: Lonart, G., Parris, B., Johnson, A. M., Miles, S., Sanford, L. D., Singletary, S. J., & Britten, R. A.
Affiliations: Eastern Virginia Medical School (US)
Corresponding author: Britten, Richard A.
ORCID: Miles, Scott
Sanford, Larry D.
Britten, Richard A.
Venue: Radiation Research
Publisher: Radiation Research Society
Published: 2012-10
Volume: 178
Issue: 4
Pages: 289-294
ISSN: 0033-7587 (ISSN-L)
1938-5404
DOI: 10.1667/rr2862.1
OpenAlex: W2146022936
Cited by: 70
References: 25
Citations by year: 2026: 1 · 2025: 3 · 2024: 1 · 2023: 2 · 2022: 2 · 2021: 9 · 2020: 5 · 2019: 4 · 2018: 8 · 2017: 4 · 2016: 10 · 2015: 6 · 2014: 12 · 2013: 3
FWCI: 4.50
Type: journal article
Language: en
Open access: closed
Locations: Radiation Research (publishedVersion)
PubMed (publishedVersion)
BioOne Complete (BioOne) (submittedVersion)
Funders: Pfizer
Topics: Health Sciences › Medicine › Physiology › Spaceflight effects on biology
Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Effects of Radiation Exposure
Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Radiation Therapy and Dosimetry
Keywords: executive function, HZE particles, 56Fe ions, galactic cosmic rays, set-shifting, prefrontal cortex, astronaut health, radiation-induced cognitive impairment, rats
MeSH terms: Animals, Cosmic Radiation, Male, Radiation Dosage, Rats, Wistar, Rats, Executive Function

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Executive Function in Rats is Impaired by Low (20 cGy) Doses of 1 GeV/u56Fe Particles

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks