Cognitive Performance in Spaceflight and Long Duration Analogs
Gary Strangman, PhD 1,2,3
1
Dept. of Psychiatry, Harvard Medical School / Massachusetts
General Hospital
2 Center for Space Medicine, Baylor College of Medicine
3 Smart Medical Systems & Technology Team Lead, NSBRI
strang@nmr.mgh.harvard.edu
Gary Beven, MD & Walter Sipes, PhD
Human Spaceflight Operations Branch
Johnson Space Center
Houston, TX
Mar 24, 2015
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Disclosure Information
I have no financial relationships to disclose.
I will not discuss off‐label use and/or investigational use in my presentation.
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Motivation
Human cognitive performance—and in particular our capability for flexible task performance—is a primary justification given for crewed spaceflight.
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Spaceflight Brain Risks
Fluid Shifts
Elevated CO2
Environmental Toxins
Dehydration
Nutrition
Hypoxia
Confinement
Social Isolation
Circadian Cues
Sleep Deprivation
Mechanical Injury
Radiation
Adverse
condition
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Chronic Stress
Altered brain
function
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Impaired
performance
Strangman
Astronaut Self‐Reports
•
•
•
•
•
Motor slowing
Trouble concentrating or focusing attention
Memory difficulties (e.g., checklist performance)
“Not myself” or “not all there”
Difficulty with multitasking
Source: unknown
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Explanations for Reported Symptoms
Sensory overload / excitement / stress?
Heavy workload / fatigue?
Space‐adaptation?
Sameness / monotony?
Unknown effect of microgravity?
Asthenia?
or … overblown?
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Relevant Reviews
– Spaceflight: Christensen JM, Talbot JM (1986) A review of the psychological aspects of space flight. Aviat Space Environ Med 57, 203‐212.
– Spaceflight: Casler JG, Cook JR (1999) Cognitive performance in space and analogous environments. Int J Cogn Ergon 3, 351‐372.
– Historical Expeditions: Stuster, J.W., 2000. Bold endeavors: behavioral lessons from polar and space exploration. Gravit Space Biol Bull 13, 49‐57.
– Space Adaptation Syndrome: Reschke, M.F., Kornilova, L.N., Harm, D.L., Bloomberg, J.J., Paloski, W.H., 1996. Neurosensory and sensory‐motor function. In: Huntoon, S.C.L., Antipov, V.V., Grigoriev, A.I. (Eds.), Humans in Spaceflight. AIAA, Reston, VA, pp. 135‐193.
– Submarines: Weybrew BB (1991) Three decades of nuclear submarine research: Implications for space and Antarctic research. In: Harrison, A.A., Clearwater, Y.A., McKay, C.P. (Eds.), From Antarctica to Outer Space: Life in Isolation and Confinement. Springer‐Verlag, New York, NY, pp. 103‐114.
– Bedrest: Lipnicki, D.M., Gunga, H.C., 2009. Physical inactivity and cognitive functioning: results from bed rest studies. Eur J Appl Physiol 105, 27‐35.
– Sensory Deprivation: Zubek JP (1964) Effects of Prolonged Sensory and Perceptual Deprivation. Br Med Bull 20, 38‐42.
– Radiation and the CNS: Cucinotta FA, Wang H, Huff JL (2009) Human Health and Performance Risks for Space Exploration Missions CH 6: Risk of Acute or Late Central Nervous System Effects from Radiation Exposure. In: JSC, N. (Ed.), Houston, TX.
– Stress: Lupien SJ, McEwen BS, Gunnar MR, Heim C (2009) Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10, 434‐445.
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Goals of this Review
1. Summarize cognitive performance in spaceflight, esp. long‐duration
2. Identify regularities & discrepancies across studies
3. Identify knowledge gaps
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Reviewed Environments
•
•
•
•
•
•
•
•
•
•
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Spaceflight
Antarctica
Isolation/confinement/bedrest
Historical expeditions
Submarines
Sensory deprivation/restriction
Environmental toxins/vibration/dehydration
Radiation
Chronic stress
[HERA, HiSeas]
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Literature Search Parameters
• PubMed, PsycInfo, Inspec, the NASA Technical Report Server, and the Defense Technical Information Center • Search terms: – cognition, cognitive, or performance along with spaceflight, flight, mission, Antarctic(a), submarine, deprivation, bedrest, etc.
• Search limits:
– English language articles through January 2014
– Excluded sleep, sleep deprivation and chronobiology
– Published experiments/reviews only
• Additional literature sources recursively identified from primary source reference lists
• More limited searches on specific spaceflight stressors:
– radiation, chronic stress, noise, vibration, toxicology
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Spaceflight Overview & Gaps
(1) “Zero information gap”
(2) “Experiment availability gap”
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Spaceflight Experiment Categories
Mean testing day = day 60.5
Median testing day = day 16
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Summary of Identified Studies
• Spaceflight total:
– 32 studies
– 110 total subjects
– mean of 3.4 subj/study
• Breakdown by duration
Duration
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Studies
Subjects
Subjects/Study
Very Long: 90+ days
7
31
4.4
Long: 22‐89 days
4
11
2.7
Short: 0‐21 days
21
68
3.2
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Spaceflight Findings
•
•
•
•
Total Subjects: 110
Total Studies: 32
Mean # subjects/study: 3.4
Main findings
– no dramatic performance deficits
– performance reductions in tracking, attention, executive
function and processing emotional stimuli
– findings were often variable or not reliably replicated
– executive, emotion, and social processing were particularly
under-represented
• Limitations
– insufficient numbers of subjects
– confounding variables not measured (stress, sleep
deprivation, workload, etc.)
– often inadequate control groups
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Interlude 1: Statistics
• Single regressor
– E.g., in-flight vs. pre-flight performance
– need ~12 subjects for stable parameter estimate
• Two regressors
– E.g., in-flight vs. pre-flight, controlling for sleep
status
– need ~12 subjects per regressor = 24 data points
• N regressors
– need ~12*N subjects required
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Spaceflight Findings
•
•
•
•
Total Subjects: 110
Total Studies: 32
Mean # subjects/study: 3.4
Main findings
– no dramatic performance deficits
– performance reductions in tracking, attention, executive
function and emotion processing
– findings were often variable or not reliably replicated
– executive, emotion, and social processing were particularly
under-represented
• Limitations
– insufficient numbers of experimental subjects
– confounding variables not measured (stress, sleep
deprivation, workload, etc.)
– often inadequate control groups
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Spaceflight Studies
From: Strangman, G.E., Sipes, W., Beven, G., 2014. Human cognitive performance in spaceflight and analogue environments. Aviat Space Environ Med 85, 1033‐1048.
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Spaceflight Studies (cont.)
From: Strangman, G.E., Sipes, W., Beven, G., 2014. Human cognitive performance in spaceflight and analogue environments. Aviat Space Environ Med 85, 1033‐1048.
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Spaceflight Studies (cont.)
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Spaceflight Studies (cont.)
From: Strangman, G.E., Sipes, W., Beven, G., 2014. Human cognitive performance in spaceflight and analogue environments. Aviat Space Environ Med 85, 1033‐1048.
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Interlude 2: Need for Controls
Assume a longitudinal study …
Performance
Spaceflight Effect
Controls
• None
–
(23 studies)
Time
+
?
?
• Inadequate
Performance
Repetition Effect
–
(3 studies)
• Full controls
–
(5 studies)
Time
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Spaceflight Findings by
Cognitive Domain
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Spaceflight Studies
Category
Perception
Motor
Memory
Attention
Spatial transformation
“Complex”/Operational
Executive function
Emotional processing
Social processing
ALL STUDIES
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Total number
of studies
24
22
12
7
8
7
5
1
0
32
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Total number of subjects
62
53
42
37
28
11
11
2
0
110
Strangman
Perception
•
•
•
•
Subjects: 62
Studies: 24
Mean subj/study: 2.6
Topics/tasks:
– lines, faces, time, movement, mass, orientation
• Major findings:
– adaptation period, typically 1-3 weeks
– time estimation and head motion sensitivity remain
affected beyond L+30 days
– considerable inter-individual variability
• Limitations/needs:
– mechanisms and variability not fully understood
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Complex Motor Performance
•
•
•
•
Subjects: 50
Studies: 22
Mean subj/study: 2.4
Topics/tasks:
– tracking, pointing, grasping, timed tapping
• Major findings:
– adaptation period, typically 1-3 weeks
– motor slowing and motor variability remain affected
beyond L+30 days
– considerable inter-individual variability
• Limitations/needs:
– mechanisms and variability not fully understood
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Memory
•
•
•
•
Subjects: 42
Studies: 12
Mean subj/study: 3.5
Topics/tasks:
– Sternberg WM, spatial WM, sequence learning,
continuous recognition memory
• Major findings:
– little evidence of memory deficits
• Limitations/needs:
– confounds in many studies
– should assess: implicit vs. explicit memory, long-term
memory, learning studies without confounds
– interactions re: radiation and chronic stress
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Attention
•
•
•
•
Subjects: 37
Studies: 7
Mean subj/study: 5.3
Topics/tasks:
– unstable tracking plus Sternberg WM (divided attention)
• Major findings:
– dual-task performance adversely affected in spaceflight
• Limitations/needs:
– not really assessed separate from motor performance
– need tests for sustained attention, selective attention,
and more divided attention
–
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Spatial Transformations
•
•
•
•
Subjects: 28
Studies: 8
Mean subj/study: 3.5
Topics/tasks:
– mental rotation
• Major findings:
– stable or improving mental rotation, but confounds in
most studies
• Limitations/needs:
– learning effects observed
– absence of suitable control groups
– modest numbers of subjects
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Operational Tasks
•
•
•
•
Subjects: 11
Studies: 7
Mean subj/study: 1.6
Topics/tasks:
– operational task performance efficiency
• Major findings:
– performance tended to improve as missions
progressed
• Limitations/needs:
– performance confounded with learning
– no established learning profiles on the tasks
– lack of suitable control groups
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Executive Function
•
•
•
•
Subjects: 11
Studies: 5
Mean subj/study: 2.2
Topics/tasks:
– Stroop (blue), grammatical reasoning
• Major findings:
– some studies revealed no deficits, others revealed
executive function deficits
• Limitations/needs:
– inadequate numbers of studies and participants
– no work on inhibitory control, set alternation, error
monitoring
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Emotion Processing
•
•
•
•
Subjects: 2
Studies: 1
Mean subj/study: 2.0
Topics/tasks:
– emotional Stroop
• Major findings:
– personally- or mission-relevant emotional words
interfered with rapid processing
• Limitations/needs:
– inadequate numbers of studies and participants
– particular concern about cognitive processing of
emotional stimuli in spaceflight settings
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Social Processing
•
•
•
•
Subjects: 0
Studies: 0
Mean subj/study: 0
Topics/tasks:
– none
• Major findings:
– none
• Limitations/needs:
– despite past observations and future expectations of
social tensions, existing task batteries lack validated
task(s) for cognitive processing of social stimuli
– consider game theory/social decision making tasks
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Interlude 3: Social Cognition
• Game Theory
– E.g., Ultimatum game (#1 divides money; #2 accepts
or not) … Nash equilibrium ~90/10, but actual ~50/50
– Most “social” games do not lead to Nash equilibria
– Provide insights into risk-taking behavior / empathy
• Coordination/Anti-Coordination Games
– E.g., swerve to avoid oncoming car vs. Chicken
– Involve choices between risk levels
• Neurobiology
– Social decision making involves reward system (esp.
basal ganglia)
– Basal ganglia known to be particularly sensitive to
both chronic stress and radiation
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Analog Cognitive Studies
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Overview of Analog Studies
• Antarctica (21-370 days)
– 15 studies
– 422 total subjects
– mean of 28.1 subj/study
• Isolation/Confinement (7-520 days)
– 20 studies
– 124 total subjects
– mean of 6.2 subj/study
• Bedrest (7-90 days)
– 20 studies
– 299 total subjects
– mean of 14.9 subj/study
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Antarctic Studies
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Antarctic Studies
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Antarctic Studies (cont.)
From: Strangman, G.E., Sipes, W., Beven, G., 2014. Human cognitive performance in spaceflight and analogue environments. Aviat Space Environ Med 85, 1033‐1048.
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Antarctic Findings
•
•
•
•
Subjects: 422
Studies: 15
Mean subj/study: 28.1
Main findings
– generally only few or mild decrements observed
– evidence for role of hypothyroidism as a mechanism
for cognitive changes during winter-over
– variable cognitive effects and replication problems
• Limitations
– often inadequate control groups
– inadequate measures of potential confounding
variables (stress, sleep deprivation, circadian
disruption, etc.)
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Isolation/Confinement and Bedrest Cognitive Studies
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Confinement Studies
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520
6 male participants
None
520
6 male participants
None
520
6 male participants
None
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weekly
(morning and evening) for 17 mo.
IIB
PVT
variable
8 tests (every
~2 months)
IIB
IAPS emotion ratings
yes
15 testing
periods, 3 with each exercise type
IIB
Lumosity.com tests: memory matrix,
brain speed, chalkboard challenge
no?
actigraphy
Significant behavioral hypokinesis, circadian desynchrony, vigilance deficits
(Basner et al. 2013)
POMS, 4 hormones
Negative‐valence Images rated more positive (defense
mechanism?); 3rd quarter phenomenon?
(Wang et al., 2014)
EEG, exercise manipulation
Running exercise improved cognitive performance, but no significant effect of time
(Schneider et al. 2013)
Confinement Studies
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Confinement Studies (cont.)
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Confinement Studies (cont.)
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Confinement Findings
•
•
•
•
Subjects: 124
Studies: 20
Mean subj/study: 6.2
Main findings
– generally only few or mild decrements observed
– behavioral slowing in longest (520 day) study
– considerable inter-individual variability
• Limitations
–
–
–
–
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problems with replication, cause unclear
often insufficient numbers of subjects
often inadequate control groups
inadequate concomitant measures of potential
confounding variables
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Bedrest Findings
•
•
•
•
Subjects: 299
Studies: 20
Mean subj/study: 14.9
Main findings
– considerable inter-individual and inter-study variability
– Lipnicki: “cognitive effects remain to be established”
– suggestions of executive function deficits
• Limitations
– problems with replication, cause unclear
– modest numbers of subjects for behavioral studies
– often inadequate control groups
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Other Domains
• Submarines (mostly classified/unpublished)
–
–
–
–
impaired declarative memory, time overestimation
mixed results on other cognitive tests
[found diaries to be helpful identifying problems/concerns]
[long-term performance predicted by emotion/social/motivation factors]
• Sensory deprivation/restriction (short, <14 days)
– variable effects, immobilization effects similar
– serendipitous heat stress comparison
• Dehydration
– clearly demonstrated deficits in perceptuomotor skill, memory,
arithmetic, not confounded with inactivity (as in confinement studies)
• Environmental (vibration, noise, temperature, toxins)
– heat, cold and vibration impair working memory
– CO2 up to 175x more narcotic than N2 (no minimum threshold) and
resulted in (1) motor slowing, not more errors, (2) more difficulty
concentrating, and (3) headaches (Fothergill 1991)
–
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Other Domains
• Submarines (mostly classified/unpublished)
–
–
–
–
impaired declarative memory, time overestimation
mixed results on other cognitive tests
[found diaries to be helpful identifying problems/concerns]
[long-term performance predicted by emotion/social/motivation factors]
• Sensory deprivation/restriction (short, <14 days)
– variable effects, immobilization effects similar
– serendipitous heat stress comparison
• Dehydration
– clearly demonstrated deficits in perceptuomotor skill, memory,
arithmetic, not confounded with inactivity (as in confinement studies)
• Environmental (vibration, noise, temperature, toxins)
– heat, cold and vibration impair working memory
– CO2 up to 175x more narcotic than N2 (no minimum threshold) and
resulted in (1) motor slowing, not more errors, (2) more difficulty
concentrating, and (3) headaches (Fothergill 1991)
– CO2 >2500ppm led to impaired decision making (Satish2012)
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Interlude 4: Low-Level CO2
[See Figure 1 in Satish et al. (2012)]
0.25% CO2
Satish U, Mendell MJ, Shekhar K, Hotchi T, Sullivan D, Streufert S, Fisk WJ (2012) Is CO2 an Indoor Pollutant? Direct Effects of Low‐to‐Moderate CO2 Concentrations on Human Decision‐Making Performance. Environ. Health Persp. 120: 1671‐1677.
Other Domains Investigated
• Radiation
– affects hippocampus and basal ganglia (memory,
learning)
– LEO radiation much lower dose (and different
quality) from deep space radiation
• Chronic stress
– affects hippocampus, basal ganglia and prefrontal
cortex (memory, learning, executive function)
– stress varies greatly across individuals, even for
exact same stressor
• Drug effects (sleep meds, effective dose, interactions)
– largely unknown pharmacokinetics and
pharmacodynamics in-flight
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Synergistic Effects
SEE TABLE 6 IN: Ushakov, I.B., Antipov, V.V., Fyodorov, V.P., Gorlov, V.G., 1996. Analyzing the combined effects of multiple spaceflight stressors. In: Huntoon, C.S.L., Antipov, V.V., Grigoriev, A.I. (Eds.), U.S. and Russian Cooperation in Space Biology and Medicine. America Institute of Aeronautics and Astronautics, Reston, VA, Vol. 3: 445‐474. (Originally from: Antipov VV, Davydov BI. (1977) Combined effects of space flight factors. Kosmicheskiye
Issledovaniya 15:2, 286-297 [Russian])
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Self‐Report vs. Evidence
Cognitive symptoms are still reported, yet there is weak experimental evidence for cognitive changes.
WHY?
• Inadequate power
– Too few subjects, poor controls
– Confounds related to learning / timeline
• Inter‐individual variability
– Subjects (incl. stress‐response), missions, and measures
• Small effect size
• Symptoms related to cognitive reserve/perceived effort
• Symptoms related to some “other” psychological effect
– Reduced motivation, initiative, or behavioral activation
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Standardized Behavioral Measures Tool (SBMT) to Detect Behavioral Health Risks during Exploration Missions
David F. Dinges, PhD, Principal Investigation
Goal: Develop and test a standardized suite of behavioral health measurement tools for spaceflight research, ground‐based analogs (both short‐ and long‐duration), and prolonged missions in isolated, confined, extreme environments. Include the following:
Mar 24, 2015
•
Performance tests via “COGNITION” battery (Basner et al.)
•
VAS ratings (e.g., fatigue, stress, sleep quality) from Reaction Self test (Dinges et al.)
•
Personal audio journals (Stuster)
•
Wrist actigraphy for sleep/wake activity (Pulsar Informatics)
•
A task simulating a relevant operational measure (Strangman et al.)
•
Additional non‐invasive measures relevant to behavioral medicine (based on literature review)
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David F. Dinges, PhD, Principal Investigation
SBMT for detecting Behavioral Health Risks during exploration missions will be evaluated in HERA, HI‐SEAS, & ISS missions
Summary / Conclusions
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Summary of All Findings
Spaceflight
Antarctica
Isolation & Confinement
Bedrest
5‐438
21‐370
7‐365
7‐90
Dramatic performance deficits
No
No
No
No
High inter‐individual variability




Inter‐study variability




Attention
Variable


Variable
Memory
Variable
Variable

Variable
Executive functioning
Variable



Emotion processing
?
?
?
?
Social processing
?
?
?
?
Problems with controls




Cognitive Condition
Durations investigated (days)
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Significant Knowledge Gaps
• Cause(s) of inter‐individual variability (!!)
• Cognitive processing of emotional stimuli
–
•
other crewmembers, info from the ground/home
Cognitive processing of social stimuli
–
other crewmembers, mission control personnel
• Sensory restriction
• Long‐duration data (>90 days) is scant
– Concerns about chronic exposures (stress, radiation, CO2, isolation)
– MARS‐520 suggests declines are progressive, so sensitive tests in shorter‐duration studies (with strong controls) may be adequate
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Research Recommendations
1. Compile and analyze available WinSCAT data
2. Broaden cognitive tests, including emotional and social processing (Basner, Seidler)
3. Longer duration experiments (Mars520, ISS, Antarctica)
4. Individual variability investigations
5. Effect size comparisons
6. Chronic stress investigations
7. Protective/countermeasure investigations
8. Test areas of concern (CO2, radiation)
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Areas of Potential Concern
•
Memory / attention
–
–
•
Executive function
–
–
•
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few/no studies conducted, but numerous reports of alterations in ICE environments
Dehydration
–
–
•
known concern, concentrations chronically elevated
Emotional / Social processing
–
•
core rationale for human spaceflight
prefrontal cortex function at particular risk
Carbon dioxide
–
•
astronaut and Antarctic self‐reports
chronic stress, radiation, CO2, dehydration, heat/cold
known physiological adaptation to spaceflight
potent modulator of cognitive function
Chronic low‐dose radiation (long missions / beyond LEO)
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Acknowledgements
Supported by: NASA’s Behavioral Health and Performance (BHP) program element through Wyle Integrated Science and Engineering
Special thanks go to:
Ellen Baker
Camille Shea
Vladimir Ivkovic
Lauren Leveton
Sandra Whitmire
Sarah Hebert‐Seropian
Christian Otto
Thomas Zeffiro
Michael Barratt
… for their varied and important assistance in developing and refining this review.
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