A neuroscience approach to optimizing brain resources for human performance in extreme environments

Extreme environments requiring optimal cognitive and behavioral performance occur in a wide variety of situations ranging from complex combat operations to elite athletic competitions. Although a large literature characterizes psychological and other aspects of individual differences in performances in extreme environments, virtually nothing is known about the underlying neural basis for these differences. This review summarizes the cognitive, emotional, and behavioral consequences of exposure to extreme environments, discusses predictors of performance, and builds a case for the use of neuroscience approaches to quantify and understand optimal cognitive and behavioral performance. Extreme environments are defined as an external context that exposes individuals to demanding psychological and/or physical conditions, and which may have profound effects on cognitive and behavioral performance. Examples of these types of environments include combat situations, Olympic-level competition, and expeditions in extreme cold, at high altitudes, or in space. Optimal performance is defined as the degree to which individuals achieve a desired outcome when completing goal-oriented tasks. It is hypothesized that individual variability with respect to optimal performance in extreme environments depends on a well "contextualized" internal body state that is associated with an appropriate potential to act. This hypothesis can be translated into an experimental approach that may be useful for quantifying the degree to which individuals are particularly suited to performing optimally in demanding environments.

[1]  A. Craig A new view of pain as a homeostatic emotion , 2003, Trends in Neurosciences.

[2]  Timothy Heeren,et al.  Neuropsychological outcomes of army personnel following deployment to the Iraq war. , 2006, JAMA.

[3]  H. Selye The Stress of Life , 1958 .

[4]  J R Augustine,et al.  The insular lobe in primates including humans. , 1985, Neurological research.

[5]  L A Palinkas,et al.  Psychological functioning among members of a small polar expedition. , 1995, Aviation, space, and environmental medicine.

[6]  R. Hauger,et al.  The CRF peptide family and their receptors: yet more partners discovered. , 2002, Trends in pharmacological sciences.

[7]  J Sauer,et al.  Cognitive fatigue and complex decision making under prolonged isolation and confinement. , 1996, Advances in space biology and medicine.

[8]  A. Shekhar,et al.  Interactions between NPY and CRF in the amygdala to regulate emotionality , 2004, Neuropeptides.

[9]  Richard Hoffman,et al.  Predictors of Success in Basic Underwater Demolition/SEAL (BUD/S) Training - Part 1: What Do We Know and Where Do We Go From Here? , 2006 .

[10]  Gunderson Ek,et al.  Adaptation to extreme environments: prediction of performance. Rep No. 66-17. , 1966 .

[11]  M. Paulus,et al.  An Insular View of Anxiety , 2006, Biological Psychiatry.

[12]  Philip J. Niro,et al.  Severe decrements in cognition function and mood induced by sleep loss, heat, dehydration, and undernutrition during simulated combat , 2005, Biological Psychiatry.

[13]  Philip J. Niro,et al.  Cognition during sustained operations: comparison of a laboratory simulation to field studies. , 2006, Aviation, space, and environmental medicine.

[14]  Matthew D. Lieberman,et al.  Does Rejection Hurt? An fMRI Study of Social Exclusion , 2003, Science.

[15]  B. Shukitt-Hale,et al.  Effects of caffeine, sleep loss, and stress on cognitive performance and mood during U.S. Navy SEAL training , 2002, Psychopharmacology.

[16]  R. Peyron,et al.  Functional imaging of brain responses to pain. A review and meta-analysis (2000) , 2000, Neurophysiologie Clinique/Clinical Neurophysiology.

[17]  G. R. Leon,et al.  Men and women in space. , 2005, Aviation, space, and environmental medicine.

[18]  G. Koob,et al.  Corticotropin-releasing factor, norepinephrine, and stress , 1999, Biological Psychiatry.

[19]  L. Palinkas The psychology of isolated and confined environments. Understanding human behavior in Antarctica. , 2003, The American psychologist.

[20]  M. Botvinick,et al.  The Contribution of the Anterior Cingulate Cortex to Executive Processes in Cognition , 1999, Reviews in the neurosciences.

[21]  Maria L. Thomas,et al.  Monitoring and predicting cognitive state and performance via physiological correlates of neuronal signals. , 2005, Aviation, space, and environmental medicine.

[22]  L A Palinkas,et al.  Going to extremes: the cultural context of stress, illness and coping in Antarctica. , 1992, Social science & medicine.

[23]  E. Stein,et al.  Right hemispheric dominance of inhibitory control: an event-related functional MRI study. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[24]  P. Terry,et al.  Mood responses to athletic performance in extreme environments , 2004, Journal of sports sciences.

[25]  A. Craig How do you feel? Interoception: the sense of the physiological condition of the body , 2002, Nature Reviews Neuroscience.

[26]  Monica Martinussen,et al.  Psychological Measures As Predictors of Military Training Performance , 2003 .

[27]  F M Siem,et al.  Personality factors affecting pilot combat performance: a preliminary investigation. , 1994, Aviation, space, and environmental medicine.

[28]  E. Cadenas,et al.  Physiology and Neurobiology of Stress and Adaptation: Central Role of the Brain , 2007 .

[29]  L A Palinkas,et al.  Psychosocial issues in long-term space flight: overview. , 2001, Gravitational and space biology bulletin : publication of the American Society for Gravitational and Space Biology.

[30]  P. Maruff,et al.  Cognitive deterioration associated with an expedition in an extreme desert environment , 2006, British Journal of Sports Medicine.

[31]  R. Valentino,et al.  Long-term regulation of locus ceruleus sensitivity to corticotropin-releasing factor by swim stress. , 1999, The Journal of pharmacology and experimental therapeutics.

[32]  M. Patil,et al.  Behavioral / Systems / Cognitive Corticotrophin Releasing Factor-Induced Synaptic Plasticity in the Amygdala Translates Stress into Emotional Disorders , 2004 .

[33]  Shigenori Watanabe,et al.  Hippocampal serotonergic system is involved in anxiety-like behavior induced by corticotropin-releasing factor , 2003, Brain Research.

[34]  C. Olson,et al.  Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions. , 1992, Cerebral cortex.

[35]  L A Palinkas,et al.  Stages of Change in Mood and Behavior During a Winter in Antarctica , 2000, Environment and behavior.

[36]  L A Palinkas,et al.  Predictors of behavior and performance in extreme environments: the Antarctic space analogue program. , 2000, Aviation, space, and environmental medicine.

[37]  J. R. Augustine Circuitry and functional aspects of the insular lobe in primates including humans , 1996, Brain Research Reviews.

[38]  B. Vogt,et al.  Contributions of anterior cingulate cortex to behaviour. , 1995, Brain : a journal of neurology.

[39]  N. Kanas,et al.  Summary of research issues in personal, interpersonal, and group dynamics. , 2000, Aviation, space, and environmental medicine.

[40]  L A Palinkas,et al.  Impairment in cognitive and exercise performance during prolonged antarctic residence: effect of thyroxine supplementation in the polar triiodothyronine syndrome. , 2001, The Journal of clinical endocrinology and metabolism.

[41]  M. Yașargil,et al.  Topographic anatomy of the insular region. , 1999, Journal of neurosurgery.

[42]  B. Largent,et al.  Immunohistochemical visualization of corticotropin‐releasing factor type 1 (CRF1) receptors in monkey brain , 2004, The Journal of comparative neurology.

[43]  S. Shelton,et al.  The Role of the Central Nucleus of the Amygdala in Mediating Fear and Anxiety in the Primate , 2004, The Journal of Neuroscience.

[44]  Desmond J Lugg,et al.  Team climate at Antarctic research stations 1996-2000: leadership matters. , 2004, Aviation, space, and environmental medicine.

[45]  L. Palinkas,et al.  Sleep and mood during a winter in Antarctica. , 2000, International journal of circumpolar health.

[46]  Saul Santiago,et al.  Visual perception, psychomotor performance, and complex motor performance during an overnight air refueling simulated flight. , 2005, Aviation, space, and environmental medicine.

[47]  Bruce Mcewen,et al.  Stress, Adaptation, and Disease: Allostasis and Allostatic Load , 1998, Annals of the New York Academy of Sciences.

[48]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[49]  C. Nemeroff,et al.  The role of corticotropin-releasing factor in depression and anxiety disorders. , 1999, The Journal of endocrinology.

[50]  Zhen Yan,et al.  Corticotropin-releasing Factor and Acute Stress Prolongs Serotonergic Regulation of Gaba Transmission in Prefrontal Cortical Pyramidal Neurons , 2022 .

[51]  J Blascovich,et al.  Cognitive and physiological antecedents of threat and challenge appraisal. , 1997, Journal of personality and social psychology.

[52]  M. Doppelmayr,et al.  Changes in Cognitive Performance during a 216 Kilometer, Extreme Endurance Footrace: A Descriptive and Prospective Study , 2005, Perceptual and motor skills.

[53]  R. Silberstein,et al.  Evaluation of cognitive performance in the heat by functional brain imaging and psychometric testing. , 2001, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[54]  Robert D O'Donnell,et al.  Generating performance test batteries relevant to specific operational tasks. , 2005, Aviation, space, and environmental medicine.

[55]  Stephen M Kosslyn,et al.  The minicog rapid assessment battery: developing a "blood pressure cuff for the mind". , 2005, Aviation, space, and environmental medicine.

[56]  E K Gunderson,et al.  ADAPTATION TO EXTREME ENVIRONMENTS: PREDICTION OF PERFORMANCE , 1966 .

[57]  N. Kanas Group interactions during space missions. , 2004, Aviation, space, and environmental medicine.

[58]  P. Tikuisis,et al.  Physical and cognitive performance during long-term cold weather operations. , 2005, Aviation, space, and environmental medicine.

[59]  David Borsook,et al.  Noxious hot and cold stimulation produce common patterns of brain activation in humans: a functional magnetic resonance imaging study , 2000, Neuroscience Letters.

[60]  Daniel S Weiss,et al.  Crewmember and mission control personnel interactions during International Space Station missions. , 2007, Aviation, space, and environmental medicine.

[61]  Sian L. Beilock,et al.  When High-Powered People Fail , 2005, Psychological science.

[62]  G F Koob,et al.  The role of corticotropin-releasing factor in behavioural responses to stress. , 1993, Ciba Foundation symposium.

[63]  Rebecca A. Grier,et al.  Fundamental dimensions of subjective state in performance settings: task engagement, distress, and worry. , 2002, Emotion.

[64]  J. Boster,et al.  Social roles and the evolution of networks in extreme and isolated environments , 2003, The Journal of mathematical sociology.

[65]  N Kanas,et al.  Social and cultural issues during Shuttle/Mir space missions. , 2000, Acta astronautica.

[66]  H. Critchley,et al.  Neural systems supporting interoceptive awareness , 2004, Nature Neuroscience.

[67]  Claude Bachelard,et al.  Mixed-gender groups: coping strategies and factors of psychological adaptation in a polar environment. , 2004, Aviation, space, and environmental medicine.

[68]  Dennis C. Choi,et al.  Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo–pituitary–adrenocortical responsiveness , 2003, Frontiers in Neuroendocrinology.

[69]  L. Lumeng,et al.  Corticotropin-releasing factor gene expression is down-regulated in the central nucleus of the amygdala of alcohol-preferring rats which exhibit high anxiety: a comparison between rat lines selectively bred for high and low alcohol preference , 2004, Brain Research.

[70]  M Martinussen,et al.  Psychological measures as predictors of pilot performance: a meta-analysis. , 1996, The International journal of aviation psychology.

[71]  Gregory McCarthy,et al.  Dynamic and strategic aspects of executive processing , 2004, Brain Research.

[72]  June J. Pilcher,et al.  Effects of hot and cold temperature exposure on performance: a meta-analytic review , 2002, Ergonomics.

[73]  W. Bardwell,et al.  Negative mood endures after completion of high-altitude military training , 2005, Annals of behavioral medicine : a publication of the Society of Behavioral Medicine.

[74]  A R Damasio,et al.  Descartes' error and the future of human life. , 1994, Scientific American.

[75]  A. Adler,et al.  Dimensions of psychological stress in peacekeeping operations. , 1998, Military medicine.

[76]  K. Luan Phan,et al.  Functional Neuroanatomy of Emotion: A Meta-Analysis of Emotion Activation Studies in PET and fMRI , 2002, NeuroImage.