Skilled movement and posture deficits in rat string-pulling behavior following low dose space radiation (28Si) exposure

Blackwell, Ashley A.; Schell, Brandi D.; Oltmanns, Jenna R. Osterlund; Whishaw, Ian Q.; Ton, Son T.; Adamczyk, Natalie S.; Kartje, Gwendolyn L.; Britten, Richard A.; Wallace, Douglas G.

doi:10.1016/j.bbr.2020.113010

Cited by 20 publications

(13 citation statements)

References 62 publications

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“…These studies have provided translational value for the use of behavioral tasks that involve skilled reaching movements, including bimanual string-pulling behavior. Separate recent studies with rodents and humans suggest that string-pulling behavior is organized similarly into reaches and withdraws to grasp and pull in a string with hand-over-hand motions (Blackwell et al, 2018c; Blackwell et al, 2021; Singh et al, 2019). Thus, this dynamic task affords the opportunity to investigate the effects of stroke and recovery of function in a way that may be more translational to behaviors that both rodents and patients engage in.…”

Section: Discussionmentioning

confidence: 99%

“…Rodents spontaneously engage in bimanually coordinated string-pulling behavior that involves hand-over-hand movements to pull in a string to retrieve a food reward (Blackwell et al, 2018ab). String-pulling behavior provides a robust assessment of fine motor control, including functional performance measures and (i.e., task time, contacts, misses) and details about movement organization related to distance and direction, that is sensitive to focal cortical damage in rats (Blackwell et al, 2018c) and simulated space radiation exposure (Blackwell et al, 2021). For example, following forelimb sensorimotor devascularization, rats exhibit increased misses with the impaired hand and persistent deficits in distance and direction of movement.…”

Section: Introductionmentioning

confidence: 99%

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String-Pulling as a Behavioral Assessment of Skilled Forelimb Motor Function in a Middle Cerebral Artery Occlusion Rat Model

Hart

Blackwell

Whishaw

et al. 2022

Preprint

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Stroke is a leading cause of long-term disability in humans and frequently results in bilateral impairments in fine motor control. Many behavioral tasks used to assess rodent models of stroke evaluate a single limb; however, recent work has demonstrated that bilateral hand-over-hand movements used to pull in a string assess skilled movement of both hands. Devascularization focused on the forelimb portion of sensorimotor cortex has been observed to produce persistent disruptions in the topographical organization of string-pulling behavior. The current study examined changes in string-pulling after a more clinically relevant rodent model of stroke via middle cerebral artery occlusion (MCAO). Detailed movement analyses revealed disruptions in the bilateral organization of string-pulling and fine motor control of both hands. Rats missed the string more often with both hands, and when the string was missed on the impaired side, rats continued to cycle through subcomponents of string-pulling behavior as if the string were grasped in the hand. Rats also failed to make a grasping motion with the impaired hand when the string was missed and instead, demonstrated an open-handed raking-like motion. No differences were found in time to approach or to complete the string-pulling task to obtain a reward, demonstrating the importance of using a detailed functional analysis of movement to detect changes in performance. String-pulling behavior is sensitive at detecting changes in bilateral rhythmical hand control following MCAO providing a foundation for future work to investigate other models of stroke and to evaluate the efficacy of therapeutic interventions that enhance neuroplasticity.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

String-Pulling as a Behavioral Assessment of Skilled Forelimb Motor Function in a Middle Cerebral Artery Occlusion Rat Model

Hart

Blackwell

Whishaw

et al. 2022

Preprint

Self Cite

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“…Deficits in fine motor control were recently identified for the first-time following SR exposure. Rats exposed to 5 cGy 28 Si exhibited longer pull durations and a reduced ability to contact the string ~7 months after SR exposure [19] similar to SR-exposed rats assessed 72 hours after irradiation. While multiple changes in movement kinematics related to distance and direction of reach and withdraw subcomponents were observed in 28 Si-exposed rats at a protracted time point, the same level of impairments were not present in the current study 72 hours after SR exposure.…”

Section: Discussionmentioning

confidence: 99%

“…During this behavior, both rodents and humans engage in highly organized bimanual hand-over-hand movements to pull in a string [17–18]. There has been a single study to establish the impact of SR exposure alone on fine motor skills [19]. This work showed that exposure to 5 cGy 28 Si significantly disrupted string-pulling behavior ~7 months after irradiation in rats that had no obvious loss of executive function performance.…”

Section: Introductionmentioning

confidence: 99%

Rapid loss of fine motor skills after low dose space radiation exposure

Blackwell

Fesshaye

Tidmore

et al. 2022

Preprint

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Sensorimotor function, motivation, and attentional processes are fundamental aspects of behavioral organization during skilled tasks. NASA's planned expedition to Mars will expose astronauts to space radiation that has the potential to impair performance in mission critical tasks. Impairments in task accuracy and movement kinematics have been previously reported during string-pulling behavior approximately 7 months after space radiation exposure. If similar space radiation-induced sensorimotor deficits emerge at earlier times, then astronauts may have compromised in-flight performance disruptions while performing skilled tasks in critical situations, such as when manipulating controls or performing seat egress. Due to the possibility that such performance losses may compromise mission success, it is critical to determine if performance deficits occur acutely after space radiation exposure at a time point that corresponds to in-flight performance. Male Wistar rats were thus exposed to either 10 centigray simplified galactic cosmic radiation, 10 centigray Helium, or no radiation at all (Sham), and string-pulling behavior was assessed approximately 72 hours later. Following exposure to space radiation, rats (Helium) took more time to approach the string to initiate string-pulling behavior and to pull in the string to reach the Cheerio (Helium and GCRsim) relative to Sham rats. Helium-exposed rats also exhibited a greater number of misses and less contacts relative to both Sham and GCRsim-exposed rats. Further, rats exposed to Helium demonstrated less concentrated reach endpoints with both the left and right hands compared to GCR-exposed rats. This work suggests that sensorimotor function and motivation and/or attentional processes were impaired 72 hours after Helium-radiation exposure.

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“…Various potential countermeasures have been proposed. Unlike candidates for systemic benefits to neuromuscular function and neuronal health, like nutraceuticals (Kumar and Sharma, 2010;Mortreux et al, 2019) or enhanced radiation shielding (Parihar et al, 2018;Blackwell et al, 2020), many training countermeasures appear to target similar specific mechanisms. Thus, we present evidence supporting the inclusion of four promising modalities in an in-flight proprioceptive countermeasure: axial body loading, postural/proprioceptive challenges, tactile input, and sensory feedback.…”

Section: Promising Modalities For An In-flight Proprioceptive Countermeasurementioning

confidence: 99%

Developing Proprioceptive Countermeasures to Mitigate Postural and Locomotor Control Deficits After Long-Duration Spaceflight

Macaulay

Peters

Wood

et al. 2021

Front. Syst. Neurosci.

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Astronauts experience post-flight disturbances in postural and locomotor control due to sensorimotor adaptations during spaceflight. These alterations may have adverse consequences if a rapid egress is required after landing. Although current exercise protocols can effectively mitigate cardiovascular and muscular deconditioning, the benefits to post-flight sensorimotor dysfunction are limited. Furthermore, some exercise capabilities like treadmill running are currently not feasible on exploration spaceflight vehicles. Thus, new in-flight operational countermeasures are needed to mitigate postural and locomotor control deficits after exploration missions. Data from spaceflight and from analog studies collectively suggest that body unloading decreases the utilization of proprioceptive input, and this adaptation strongly contributes to balance dysfunction after spaceflight. For example, on return to Earth, an astronaut’s vestibular input may be compromised by adaptation to microgravity, but their proprioceptive input is compromised by body unloading. Since proprioceptive and tactile input are important for maintaining postural control, keeping these systems tuned to respond to upright balance challenges during flight may improve functional task performance after flight through dynamic reweighting of sensory input. Novel approaches are needed to compensate for the challenges of balance training in microgravity and must be tested in a body unloading environment such as head down bed rest. Here, we review insights from the literature and provide observations from our laboratory that could inform the development of an in-flight proprioceptive countermeasure.

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Skilled movement and posture deficits in rat string-pulling behavior following low dose space radiation (28Si) exposure

Cited by 20 publications

References 62 publications

String-Pulling as a Behavioral Assessment of Skilled Forelimb Motor Function in a Middle Cerebral Artery Occlusion Rat Model

String-Pulling as a Behavioral Assessment of Skilled Forelimb Motor Function in a Middle Cerebral Artery Occlusion Rat Model

Rapid loss of fine motor skills after low dose space radiation exposure

Developing Proprioceptive Countermeasures to Mitigate Postural and Locomotor Control Deficits After Long-Duration Spaceflight

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