Multi-Domain Touchscreen-Based Cognitive Assessment of C57BL/6J Female Mice Shows Whole-Body Exposure to 56Fe Particle Space Radiation in Maturity Improves Discrimination Learning Yet Impairs Stimulus-Response Rule-Based Habit Learning
Astronauts during interplanetary missions will be exposed to galactic cosmic radiation, including charged particles like 56Fe. Most preclinical studies with mature, “astronaut-aged” rodents suggest space radiation diminishes performance in classical hippocampal- and prefrontal cortex-dependent tasks...
Main Authors: | , , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Frontiers Media S.A.
2021-10-01
|
Series: | Frontiers in Behavioral Neuroscience |
Subjects: | |
Online Access: | https://www.frontiersin.org/articles/10.3389/fnbeh.2021.722780/full |
id |
doaj-d3740a78766c4917be9bb5e15ccaaa8c |
---|---|
record_format |
Article |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Ivan Soler Sanghee Yun Sanghee Yun Sanghee Yun Ryan P. Reynolds Ryan P. Reynolds Cody W. Whoolery Fionya H. Tran Priya L. Kumar Yuying Rong Matthew J. DeSalle Adam D. Gibson Ann M. Stowe Frederico C. Kiffer Amelia J. Eisch Amelia J. Eisch Amelia J. Eisch Amelia J. Eisch |
spellingShingle |
Ivan Soler Sanghee Yun Sanghee Yun Sanghee Yun Ryan P. Reynolds Ryan P. Reynolds Cody W. Whoolery Fionya H. Tran Priya L. Kumar Yuying Rong Matthew J. DeSalle Adam D. Gibson Ann M. Stowe Frederico C. Kiffer Amelia J. Eisch Amelia J. Eisch Amelia J. Eisch Amelia J. Eisch Multi-Domain Touchscreen-Based Cognitive Assessment of C57BL/6J Female Mice Shows Whole-Body Exposure to 56Fe Particle Space Radiation in Maturity Improves Discrimination Learning Yet Impairs Stimulus-Response Rule-Based Habit Learning Frontiers in Behavioral Neuroscience dentate gyrus prefrontal cortex striatum hippocampus behavioral pattern separation rodent touchscreen |
author_facet |
Ivan Soler Sanghee Yun Sanghee Yun Sanghee Yun Ryan P. Reynolds Ryan P. Reynolds Cody W. Whoolery Fionya H. Tran Priya L. Kumar Yuying Rong Matthew J. DeSalle Adam D. Gibson Ann M. Stowe Frederico C. Kiffer Amelia J. Eisch Amelia J. Eisch Amelia J. Eisch Amelia J. Eisch |
author_sort |
Ivan Soler |
title |
Multi-Domain Touchscreen-Based Cognitive Assessment of C57BL/6J Female Mice Shows Whole-Body Exposure to 56Fe Particle Space Radiation in Maturity Improves Discrimination Learning Yet Impairs Stimulus-Response Rule-Based Habit Learning |
title_short |
Multi-Domain Touchscreen-Based Cognitive Assessment of C57BL/6J Female Mice Shows Whole-Body Exposure to 56Fe Particle Space Radiation in Maturity Improves Discrimination Learning Yet Impairs Stimulus-Response Rule-Based Habit Learning |
title_full |
Multi-Domain Touchscreen-Based Cognitive Assessment of C57BL/6J Female Mice Shows Whole-Body Exposure to 56Fe Particle Space Radiation in Maturity Improves Discrimination Learning Yet Impairs Stimulus-Response Rule-Based Habit Learning |
title_fullStr |
Multi-Domain Touchscreen-Based Cognitive Assessment of C57BL/6J Female Mice Shows Whole-Body Exposure to 56Fe Particle Space Radiation in Maturity Improves Discrimination Learning Yet Impairs Stimulus-Response Rule-Based Habit Learning |
title_full_unstemmed |
Multi-Domain Touchscreen-Based Cognitive Assessment of C57BL/6J Female Mice Shows Whole-Body Exposure to 56Fe Particle Space Radiation in Maturity Improves Discrimination Learning Yet Impairs Stimulus-Response Rule-Based Habit Learning |
title_sort |
multi-domain touchscreen-based cognitive assessment of c57bl/6j female mice shows whole-body exposure to 56fe particle space radiation in maturity improves discrimination learning yet impairs stimulus-response rule-based habit learning |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Behavioral Neuroscience |
issn |
1662-5153 |
publishDate |
2021-10-01 |
description |
Astronauts during interplanetary missions will be exposed to galactic cosmic radiation, including charged particles like 56Fe. Most preclinical studies with mature, “astronaut-aged” rodents suggest space radiation diminishes performance in classical hippocampal- and prefrontal cortex-dependent tasks. However, a rodent cognitive touchscreen battery unexpectedly revealed 56Fe radiation improves the performance of C57BL/6J male mice in a hippocampal-dependent task (discrimination learning) without changing performance in a striatal-dependent task (rule-based learning). As there are conflicting results on whether the female rodent brain is preferentially injured by or resistant to charged particle exposure, and as the proportion of female vs. male astronauts is increasing, further study on how charged particles influence the touchscreen cognitive performance of female mice is warranted. We hypothesized that, similar to mature male mice, mature female C57BL/6J mice exposed to fractionated whole-body 56Fe irradiation (3 × 6.7cGy 56Fe over 5 days, 600 MeV/n) would improve performance vs. Sham conditions in touchscreen tasks relevant to hippocampal and prefrontal cortical function [e.g., location discrimination reversal (LDR) and extinction, respectively]. In LDR, 56Fe female mice more accurately discriminated two discrete conditioned stimuli relative to Sham mice, suggesting improved hippocampal function. However, 56Fe and Sham female mice acquired a new simple stimulus-response behavior and extinguished this acquired behavior at similar rates, suggesting similar prefrontal cortical function. Based on prior work on multiple memory systems, we next tested whether improved hippocampal-dependent function (discrimination learning) came at the expense of striatal stimulus-response rule-based habit learning (visuomotor conditional learning). Interestingly, 56Fe female mice took more days to reach criteria in this striatal-dependent rule-based test relative to Sham mice. Together, our data support the idea of competition between memory systems, as an 56Fe-induced decrease in striatal-based learning is associated with enhanced hippocampal-based learning. These data emphasize the power of using a touchscreen-based battery to advance our understanding of the effects of space radiation on mission critical cognitive function in females, and underscore the importance of preclinical space radiation risk studies measuring multiple cognitive processes, thereby preventing NASA’s risk assessments from being based on a single cognitive domain. |
topic |
dentate gyrus prefrontal cortex striatum hippocampus behavioral pattern separation rodent touchscreen |
url |
https://www.frontiersin.org/articles/10.3389/fnbeh.2021.722780/full |
work_keys_str_mv |
AT ivansoler multidomaintouchscreenbasedcognitiveassessmentofc57bl6jfemalemiceshowswholebodyexposureto56feparticlespaceradiationinmaturityimprovesdiscriminationlearningyetimpairsstimulusresponserulebasedhabitlearning AT sangheeyun multidomaintouchscreenbasedcognitiveassessmentofc57bl6jfemalemiceshowswholebodyexposureto56feparticlespaceradiationinmaturityimprovesdiscriminationlearningyetimpairsstimulusresponserulebasedhabitlearning AT sangheeyun multidomaintouchscreenbasedcognitiveassessmentofc57bl6jfemalemiceshowswholebodyexposureto56feparticlespaceradiationinmaturityimprovesdiscriminationlearningyetimpairsstimulusresponserulebasedhabitlearning AT sangheeyun multidomaintouchscreenbasedcognitiveassessmentofc57bl6jfemalemiceshowswholebodyexposureto56feparticlespaceradiationinmaturityimprovesdiscriminationlearningyetimpairsstimulusresponserulebasedhabitlearning AT ryanpreynolds multidomaintouchscreenbasedcognitiveassessmentofc57bl6jfemalemiceshowswholebodyexposureto56feparticlespaceradiationinmaturityimprovesdiscriminationlearningyetimpairsstimulusresponserulebasedhabitlearning AT ryanpreynolds multidomaintouchscreenbasedcognitiveassessmentofc57bl6jfemalemiceshowswholebodyexposureto56feparticlespaceradiationinmaturityimprovesdiscriminationlearningyetimpairsstimulusresponserulebasedhabitlearning AT codywwhoolery multidomaintouchscreenbasedcognitiveassessmentofc57bl6jfemalemiceshowswholebodyexposureto56feparticlespaceradiationinmaturityimprovesdiscriminationlearningyetimpairsstimulusresponserulebasedhabitlearning AT fionyahtran multidomaintouchscreenbasedcognitiveassessmentofc57bl6jfemalemiceshowswholebodyexposureto56feparticlespaceradiationinmaturityimprovesdiscriminationlearningyetimpairsstimulusresponserulebasedhabitlearning AT priyalkumar multidomaintouchscreenbasedcognitiveassessmentofc57bl6jfemalemiceshowswholebodyexposureto56feparticlespaceradiationinmaturityimprovesdiscriminationlearningyetimpairsstimulusresponserulebasedhabitlearning AT yuyingrong multidomaintouchscreenbasedcognitiveassessmentofc57bl6jfemalemiceshowswholebodyexposureto56feparticlespaceradiationinmaturityimprovesdiscriminationlearningyetimpairsstimulusresponserulebasedhabitlearning AT matthewjdesalle multidomaintouchscreenbasedcognitiveassessmentofc57bl6jfemalemiceshowswholebodyexposureto56feparticlespaceradiationinmaturityimprovesdiscriminationlearningyetimpairsstimulusresponserulebasedhabitlearning AT adamdgibson multidomaintouchscreenbasedcognitiveassessmentofc57bl6jfemalemiceshowswholebodyexposureto56feparticlespaceradiationinmaturityimprovesdiscriminationlearningyetimpairsstimulusresponserulebasedhabitlearning AT annmstowe multidomaintouchscreenbasedcognitiveassessmentofc57bl6jfemalemiceshowswholebodyexposureto56feparticlespaceradiationinmaturityimprovesdiscriminationlearningyetimpairsstimulusresponserulebasedhabitlearning AT fredericockiffer multidomaintouchscreenbasedcognitiveassessmentofc57bl6jfemalemiceshowswholebodyexposureto56feparticlespaceradiationinmaturityimprovesdiscriminationlearningyetimpairsstimulusresponserulebasedhabitlearning AT ameliajeisch multidomaintouchscreenbasedcognitiveassessmentofc57bl6jfemalemiceshowswholebodyexposureto56feparticlespaceradiationinmaturityimprovesdiscriminationlearningyetimpairsstimulusresponserulebasedhabitlearning AT ameliajeisch multidomaintouchscreenbasedcognitiveassessmentofc57bl6jfemalemiceshowswholebodyexposureto56feparticlespaceradiationinmaturityimprovesdiscriminationlearningyetimpairsstimulusresponserulebasedhabitlearning AT ameliajeisch multidomaintouchscreenbasedcognitiveassessmentofc57bl6jfemalemiceshowswholebodyexposureto56feparticlespaceradiationinmaturityimprovesdiscriminationlearningyetimpairsstimulusresponserulebasedhabitlearning AT ameliajeisch multidomaintouchscreenbasedcognitiveassessmentofc57bl6jfemalemiceshowswholebodyexposureto56feparticlespaceradiationinmaturityimprovesdiscriminationlearningyetimpairsstimulusresponserulebasedhabitlearning |
_version_ |
1716828296161787904 |
spelling |
doaj-d3740a78766c4917be9bb5e15ccaaa8c2021-10-11T07:37:41ZengFrontiers Media S.A.Frontiers in Behavioral Neuroscience1662-51532021-10-011510.3389/fnbeh.2021.722780722780Multi-Domain Touchscreen-Based Cognitive Assessment of C57BL/6J Female Mice Shows Whole-Body Exposure to 56Fe Particle Space Radiation in Maturity Improves Discrimination Learning Yet Impairs Stimulus-Response Rule-Based Habit LearningIvan Soler0Sanghee Yun1Sanghee Yun2Sanghee Yun3Ryan P. Reynolds4Ryan P. Reynolds5Cody W. Whoolery6Fionya H. Tran7Priya L. Kumar8Yuying Rong9Matthew J. DeSalle10Adam D. Gibson11Ann M. Stowe12Frederico C. Kiffer13Amelia J. Eisch14Amelia J. Eisch15Amelia J. Eisch16Amelia J. Eisch17Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, United StatesPerelman School of Medicine, University of Pennsylvania, Philadelphia, PA, United StatesDepartment of Psychiatry, University of Texas Southwestern Medical Center, Dallas, TX, United StatesDepartment of Anesthesiology and Critical Care Medicine, Children’s Hospital of Philadelphia, Philadelphia, PA, United StatesDepartment of Psychiatry, University of Texas Southwestern Medical Center, Dallas, TX, United StatesDepartment of Anesthesiology and Critical Care Medicine, Children’s Hospital of Philadelphia, Philadelphia, PA, United StatesDepartment of Psychiatry, University of Texas Southwestern Medical Center, Dallas, TX, United StatesDepartment of Anesthesiology and Critical Care Medicine, Children’s Hospital of Philadelphia, Philadelphia, PA, United StatesUniversity of Pennsylvania, Philadelphia, PA, United StatesPerelman School of Medicine, University of Pennsylvania, Philadelphia, PA, United StatesDepartment of Anesthesiology and Critical Care Medicine, Children’s Hospital of Philadelphia, Philadelphia, PA, United StatesDepartment of Anesthesiology and Critical Care Medicine, Children’s Hospital of Philadelphia, Philadelphia, PA, United StatesDepartment of Neurology and Neurological Therapeutics, University of Texas Southwestern Medical Center, Dallas, TX, United StatesDepartment of Anesthesiology and Critical Care Medicine, Children’s Hospital of Philadelphia, Philadelphia, PA, United StatesPerelman School of Medicine, University of Pennsylvania, Philadelphia, PA, United StatesDepartment of Psychiatry, University of Texas Southwestern Medical Center, Dallas, TX, United StatesDepartment of Anesthesiology and Critical Care Medicine, Children’s Hospital of Philadelphia, Philadelphia, PA, United StatesDepartment of Neuroscience, Perelman School of Medicine, Mahoney Institute for Neurosciences, University of Pennsylvania, Philadelphia, PA, United StatesAstronauts during interplanetary missions will be exposed to galactic cosmic radiation, including charged particles like 56Fe. Most preclinical studies with mature, “astronaut-aged” rodents suggest space radiation diminishes performance in classical hippocampal- and prefrontal cortex-dependent tasks. However, a rodent cognitive touchscreen battery unexpectedly revealed 56Fe radiation improves the performance of C57BL/6J male mice in a hippocampal-dependent task (discrimination learning) without changing performance in a striatal-dependent task (rule-based learning). As there are conflicting results on whether the female rodent brain is preferentially injured by or resistant to charged particle exposure, and as the proportion of female vs. male astronauts is increasing, further study on how charged particles influence the touchscreen cognitive performance of female mice is warranted. We hypothesized that, similar to mature male mice, mature female C57BL/6J mice exposed to fractionated whole-body 56Fe irradiation (3 × 6.7cGy 56Fe over 5 days, 600 MeV/n) would improve performance vs. Sham conditions in touchscreen tasks relevant to hippocampal and prefrontal cortical function [e.g., location discrimination reversal (LDR) and extinction, respectively]. In LDR, 56Fe female mice more accurately discriminated two discrete conditioned stimuli relative to Sham mice, suggesting improved hippocampal function. However, 56Fe and Sham female mice acquired a new simple stimulus-response behavior and extinguished this acquired behavior at similar rates, suggesting similar prefrontal cortical function. Based on prior work on multiple memory systems, we next tested whether improved hippocampal-dependent function (discrimination learning) came at the expense of striatal stimulus-response rule-based habit learning (visuomotor conditional learning). Interestingly, 56Fe female mice took more days to reach criteria in this striatal-dependent rule-based test relative to Sham mice. Together, our data support the idea of competition between memory systems, as an 56Fe-induced decrease in striatal-based learning is associated with enhanced hippocampal-based learning. These data emphasize the power of using a touchscreen-based battery to advance our understanding of the effects of space radiation on mission critical cognitive function in females, and underscore the importance of preclinical space radiation risk studies measuring multiple cognitive processes, thereby preventing NASA’s risk assessments from being based on a single cognitive domain.https://www.frontiersin.org/articles/10.3389/fnbeh.2021.722780/fulldentate gyrusprefrontal cortexstriatumhippocampusbehavioral pattern separationrodent touchscreen |