OPPORTUNITIES IN NEUROSCIENCE FOR FUTURE ARMY APPLICATIONS

Committee on Opportunities in Neuroscience for Future Army Applications

Board on Army Science and Technology

Division on Engineering and Physical Sciences

NATIONAL RESEARCH COUNCIL OF THE NATIONAL ACADEMIES

THE NATIONAL ACADEMIES PRESS

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OppOrtunities in neurOscience fOr future Army ApplicAtiOns Committee on Opportunities in Neuroscience for Future Army Applications Board on Army Science and Technology Division on Engineering and Physical Sciences

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The NaTioNal academies Press 500 Fifth street, N.W. Washington, dc 20001 NOTICE: The project that is the subject of this report was approved by the Governing Board of the National Research Council, whose members are drawn from the councils of the National Academy of Sciences, the National Academy of Engineering, and the Institute of Medicine. The members of the committee responsible for the report were chosen for their special competences and with regard for appropriate balance. This study was supported by Contract No. W911NF-07-C-0117 between the National Academy of Sciences and the Department of Defense. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the views of the organizations or agencies that provided support for the project. International Standard Book Number-13: 978-0-309-12740-0 International Standard Book Number-10: 0-309-12740-8 Library of Congress Control Number: 2009927221 Limited copies of this report are available from Additional copies are available from Board on Army Science and Technology The National Academies Press National Research Council 500 Fifth Street, N.W. 500 Fifth Street, N.W., Room 940 Lockbox 285 Washington, DC 20001 Washington, DC 20055 (202) 334-3118 (800) 624-6242 or (202) 334-3313 (in the Washington metropolitan area) Internet, http://www.nap.edu Cover: Neuronal pathways in BrainBow mice. Neurons in the hippocampus, a brain area involved in memory, are labeled in different colors, with their neuronal outgoing projections pointing to the left. This is the first time so many different neurons have been separately visualized on such a large scale. Courtesy of Jean Livet, Joshua R. Sanes, and Jeff W. Lichtman, Harvard University, 2008. Copyright 2009 by the National Academy of Sciences. All rights reserved. Printed in the United States of America

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The National Academy of Sciences is a private, nonprofit, self-perpetuating society of distinguished scholars engaged in scientific and engineering research, dedicated to the furtherance of science and technology and to their use for the general welfare. Upon the authority of the charter granted to it by the Congress in 1863, the Academy has a mandate that requires it to advise the federal government on scientific and technical matters. Dr. Ralph J. Cicerone is president of the National Academy of Sciences. The National Academy of Engineering was established in 1964, under the charter of the National Academy of Sciences, as a parallel organization of outstanding engineers. It is autonomous in its administration and in the selection of its members, sharing with the National Academy of Sciences the responsibility for advising the federal government. The National Academy of Engineering also sponsors engineering programs aimed at meeting national needs, encourages education and research, and recognizes the superior achievements of engineers. Dr. Charles M. Vest is president of the National Academy of Engineering. The Institute of Medicine was established in 1970 by the National Academy of Sciences to secure the services of eminent members of appropriate professions in the examination of policy matters pertaining to the health of the public. The Institute acts under the responsibility given to the National Academy of Sciences by its con - gressional charter to be an adviser to the federal government and, upon its own initiative, to identify issues of medical care, research, and education. Dr. Harvey V. Fineberg is president of the Institute of Medicine. The National Research Council was organized by the National Academy of Sciences in 1916 to associate the broad community of science and technology with the Academy’s purposes of furthering knowledge and advis - ing the federal government. Functioning in accordance with general policies determined by the Academy, the Council has become the principal operating agency of both the National Academy of Sciences and the National Academy of Engineering in providing services to the government, the public, and the scientific and engineering communities. The Council is administered jointly by both Academies and the Institute of Medicine. Dr. Ralph J. Cicerone and Dr. Charles M. Vest are chair and vice chair, respectively, of the National Research Council. www.national-academies.org

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commiTTee oN oPPorTuNiTies iN NeuroscieNce For FuTure army aPPlicaTioNs FLOYD E. BLOOM, Chair, Professor Emeritus, The Scripps Research Institute RICHARD A. ANDERSON, Professor of Neuroscience, California Institute of Technology RONALD R. BLANCK, Vice Chairman, Martin, Blanck, & Associates EMERY N. BROWN, Professor of Anesthesia, Massachusetts General Hospital JOSEPH T. COYLE, Eben S. Draper Professor of Psychiatry and Neuroscience, Harvard University MARY “MISSY” CUMMINGS, Boeing Assistant Professor, Director of Humans and Automation Lab, Massachusetts Institute of Technology J. MARK DAVIS, Professor, Director of Psychoneuroimmunology, Division of Applied Physiology, University of South Carolina MICHAEL S. GAZZANIGA, Director, The Sage Center for the Study of the Mind, University of California at Santa Barbara RICHARD J. GENIK, II, Director, Emergent Technology Research Division, Wayne State University PAUL W. GLIMCHER, Professor of Neural Sciences, Economics, and Psychology, New York University PETER A. HANCOCK, Provost, Distinguished Research Professor, University of Central Florida STEVEN KORNGUTH, Director, Center for Strategic and Innovative Technologies, Professor of Pharmacy, University of Texas MARTIN P. PAULUS, Professor in Residence, Department of Psychology, University of California at San Diego JUDITH L. SWAIN, Executive Director, Singapore Institute of Clinical Sciences; Lien Ying Chow Professor of Medicine, National University of Singapore; Adjunct Professor of Medicine, University of California at San Diego PAUL J. ZAK, Director, Center for Neuroscience Studies, Professor of Economics and Clinical Professor of Neurology, Claremont Graduate University staff ROBERT J. LOVE, Study Director NIA D. JOHNSON, Senior Research Associate (through July 2008) JAMES C. MYSKA, Senior Research Associate ANGELA L. MARTIN, Senior Program Assistant v

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Board oN army scieNce aNd TechNoloGy MALCOLM R. O’NEILL, Chair, Lockheed Martin Corporation (retired), Vienna, Virginia ALAN H. EPSTEIN, Vice Chair, Pratt & Whitney, East Hartford, Connecticut DUANE ADAMS, Carnegie Mellon University (retired), Arlington, Virginia ILESANMI ADESIDA, University of Illinois at Urbana-Champaign RAJ AGGARWAL, Rockwell Collins, Cedar Rapids, Iowa SETH BONDER, The Bonder Group, Ann Arbor, Michigan JAMES CARAFANO, The Heritage Foundation, Washington, D.C. W. PETER CHERRY, Science Applications International Corporation (SAIC), Ann Arbor, Michigan DARRELL W. COLLIER, U.S. Army Space and Missile Defense Command (retired), Leander, Texas JAY C. DAVIS, Lawrence Livermore National Laboratory (retired), Livermore, California PATRICIA K. FALCONE, Sandia National Laboratories, Livermore, California RONALD P. FUCHS, The Boeing Company, Seattle, Washington PETER F. GREEN, University of Michigan, Ann Arbor CARL GUERRERI, Electronic Warfare Associates, Inc., Herndon, Virginia JOHN J. HAMMOND, Lockheed Martin Corporation (retired), Fairfax, Virginia M. FREDERICK HAWTHORNE, University of Missouri, Columbia MARY JANE IRWIN, Pennsylvania State University, University Park ELLIOT D. KIEFF, Channing Laboratory, Harvard University, Boston, Massachusetts LARRY LEHOWICZ, Quantum Research International, Arlington, Virginia ROBIN MURPHY, Texas A&M University, College Station RICHARD R. PAUL, Consultant, Bellevue, Washington EDWARD K. REEDY, Georgia Tech Research Institute (retired), Atlanta DENNIS J. REIMER, DFI International (retired), Arlington, Virginia JONATHAN M. SMITH, University of Pennsylvania, Philadelphia MARK J.T. SMITH, Purdue University, West Lafayette, Indiana MICHAEL A. STROSCIO, University of Illinois, Chicago JUDITH L. SWAIN, University of California at San Diego, La Jolla WILLIAM R. SWARTOUT, Institute for Creative Technologies, Marina del Rey, California EDWIN L. THOMAS, Massachusetts Institute of Technology, Cambridge ELLEN D. WILLIAMS, University of Maryland, College Park JOSEPH YAKOVAC, President, JVM LLC, Hampton, Virginia staff BRUCE A. BRAUN, Director CHRIS JONES, Financial Manager DEANNA P. SPARGER, Program Administrative Coordinator vi

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Preface The study of the human brain, its capacities, and its who must make the hard decisions on which science and diseases remains one of the greatest scientific and philo- technology to pursue. sophical challenges ever undertaken. That said, compiling The committee examined the basis of new neuroscience- this report to consider aspects of what has been learned and based technologies and the likelihood that they could one day is being learned about the brain that can be useful to the have an impact on Army capabilities. I believe the report pro- operations of the U.S. Army has also proven to be extremely vides both a valuable snapshot of the nature of neuroscience challenging. First, the field of neuroscience is so dynamic today and a well-formulated conceptualization of how its that significant new findings are being announced almost growing number of facets could affect the Army. Although daily. The ability to define the systems of neurons that are the science is a moving target, actions could be taken now activated as a human learns, practices, and performs mental to track the progression of new concepts that will lead to tasks has allowed impressive integration of the constantly developments with high potential for Army use. accruing understanding of how neurons use their genes to I would like to thank the committee for its hard work create proteins that enable them to function together. The in interviewing numerous experts, assessing the pertinent ability to correlate brain images with function and behavior issues, and developing recommendations to address the has already translated into accelerated programs to develop many demands of its statement of task (see page 9). The yet more advanced imaging tools and techniques. I believe, committee, in turn, is grateful to the many Army personnel as many others do, that despite the almost constant growth engaged in related research and technology developments for of neuroscience over the past four decades, the future of the useful information they provided. We also greatly appre- neuroscience applications will grow at a rate that has not ciate the support and assistance of the National Research been seen since the birth of microprocessor-based personal Council (NRC) staff, which ably assisted the committee in computers. It was against this backdrop of a rapidly grow- its fact-finding activities and in the production of this report. ing science, and the even more rapidly changing translation In particular, I thank Robert Love and his staff, who success- of that science into useful applications, that the committee fully organized several major meetings in multiple locations. addressed the issues in this report. They also maintained a secure central Web forum, where our Second, along with the growing number of scientists guests’ messages accumulated, along with remote interviews engaged in neuroscience, the scope of neuroscience is also with people unable to attend our meetings, and through expanding at an ever-accelerating rate—so fast, in fact, that which we wrote, shared our expertises, and developed the scientists and engineers have difficulty reconciling their consensus for the report we present here. In addition, we also perceptions of what is and isn’t included. Several new sub- specifically recognize the essential role played by consulting disciplines have been created in the past few years, easily technical writer Robert Katt as he helped us communicate to identified by the “neuro-” prefix, linking neuroscience our intended audiences within the Army the richness of the knowledge with valuable applications and technologies both data and the often subtle nuances of how those data could be medical and nonmedical. Which of them have proven to be used by the Army for its current and future operations. substantive enough to be declared authentic components of The study was conducted under the auspices of the NRC applied neuroscience and to be deemed contributors to that Board on Army Science and Technology (BAST), which was future? Yet a third challenge has been to prepare a report established as a unit of the NRC in 1982 at the request of the that could satisfy and be understood by an audience of both U.S. Army. The BAST brings broad military, industrial, and generalists and specialists, as well as by those in the Army academic scientific, engineering, and management expertise vii vii

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viii PRefACe to bear on technical challenges of importance to senior bers nominated and appointed to serve as formal members Army leaders. The Board is not a study committee; rather, of the study committee, asked to endorse the committee’s it discusses potential study topics and tasks; ensures project conclusions or recommendations, nor did they review final planning; suggests potential experts to serve as committee drafts of the report before its release. members or reviewers; and convenes meetings to examine strategic issues for its sponsor, the Assistant Secretary of the Army (Acquisition, Logistics, and Technology). Floyd Bloom, Chair Although the Board members are listed on page vi of this Committee on Opportunities in Neuroscience report, they were not, with the exception of any Board mem- for Future Army Applications

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acknowledgments This report has been reviewed in draft form by indi- Edward G. Jones (NAS), University of California, viduals chosen for their diverse perspectives and technical Davis, expertise, in accordance with procedures approved by the Michael M. Merzenich (NAS), University of California, National Research Council’s Report Review Committee. The San Francisco, purpose of this independent review is to provide candid and Gregory J. Moore, Pennsylvania State University, and critical comments that will assist the institution in making its Daniel Schacter, Harvard University. published report as sound as possible and to ensure that the report meets institutional standards for objectivity, evidence, Although the reviewers listed above have provided and responsiveness to the study charge. The review com- many constructive comments and suggestions, they were not ments and draft manuscript remain confidential to protect asked to endorse the conclusions or recommendations, nor the integrity of the deliberative process. We wish to thank the did they see the final draft of the report before its release. following individuals for their review of this report: The review of this report was overseen by Dennis W. Choi of Emory University and Richard M. Shiffrin of Indiana Huda Akil, University of Michigan, University. Appointed by the National Research Council, Michael Bennett (NAS), Albert Einstein College of they were responsible for making certain that an independent Medicine, examination of this report was carried out in accordance with John Cacioppo, University of Chicago, institutional procedures and that all review comments were David Dinges, University of Pennsylvania, carefully considered. Responsibility for the final content of Stephen Drew, Science Partners, this report rests entirely with the authoring committee and Christopher Green, Wayne State University, the institution. ix

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contents SUMMARY 1 1 INTRODUCTION 8 Study Background, 8 Statement of Task, 8 Study Approach, 9 Report Organization, 10 Chapter Structure, 10 Response to Statement of Task, 10 References, 11 2 NEUROSCIENCE AND THE ARMY 12 History, Scope, and Definition of Neuroscience, 12 Hierarchical Levels of Neuroscience, 13 Neuroscience Technologies, 13 Reliable Biomarkers for Neuropsychological States and Behavioral Outcomes, 16 Army Application Areas, 18 Societal Issues, 19 Ethical Considerations, 19 Cultural Impediments, 20 The Use and Abuse of Socially Sensitive Demographic Categories as Indicators of Neural State and Performance Capability, 20 References, 21 3 TRAINING AND LEARNING 23 Evaluating the Efficiency of Training Regimes and Learning Paradigms, 23 Neuroscience-Based Models of Learning, 23 Subject Populations for Army-Specific Studies of Learning and Training, 24 Individual Capability and Response to Training, 25 Individual Variability in Brain Activity, 25 Identifying Conceptual Change in Individual Learning, 26 Monitoring and Predicting Changes in Individual Performance Efficiency, 27 The Effects of Environmental Stressors on Individual Performance, 27 Soldier Selection and Assessment, 28 Current Enlisted Soldier Selection, 29 Advanced Soldier Selection Tools, 29 Neuropsychological Testing in the Army: The Automated Neuropsychological Assessment Metrics, 30 xi

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xii CONTeNTS Summary: Status of Soldier Selection and Assessment and the Potential for Neuroscience-Based Improvements, 30 Monitoring and Predicting Social and Group Interactions, 31 The Scope of Social Neuroscience, 31 Relevance of Social Neuroscience to the Army, 31 Summary, 33 References, 33 4 OPTIMIZING DECISION MAKING 36 The Sources of Suboptimal Decision Making, 36 Errors in Assessing Relative Risk, 36 Loss Aversion in Decision Making, 37 Making Optimal Use of Individual Variability, 37 Tools for Characterizing Individual Decision Makers, 38 Personality as a Factor in Decision Making, 38 Emotional Reactivity in Decision Making, 39 Emerging Tools: Genetics, Neurohormones, and Brain Imaging, 39 Neuroscience-Related Theories of Decision Making, 39 Belief-Based Decision Making, 40 Intuitive Decision Making and Recognition-Primed Decisions, 42 References, 43 5 SUSTAINING SOLDIER PERFORMANCE 45 Measures to Counter Performance Degradation, 45 Fatigue, 45 Brain Response to Metabolic Stressors, 52 Sleep Deprivation, 53 Pharmaceutical Countermeasures to Neurophysiological Stressors, 54 Brain Injury, 56 Stress Disorders, Including PTSD, 56 Major Depressive Disorder in the Military Context, 58 Resilience, 58 Longer-Term Performance Deficits Linked to Traumatic Brain Injury, 59 Prospective Interventions, 61 References, 61 6 IMPROVING COGNITIVE AND BEHAVIORAL PERFORMANCE 67 Hours of Boredom and Moments of Terror, 67 Neuroegonomics, 69 Specificity of Brain Signals as Control Inputs to a Brain–Machine Interface, 69 A Pragmatic Approach to Neuroergonomics Applications, 70 Leveraging External Research to Enhance Soldier Performance, 70 Driver Workload Research, 70 NASA Neuroscience Research, 71 Neuropharmacological Approaches to Performance Enhancement, 71 References, 71 7 NEUROSCIENCE TECHNOLOGY OPPORTUNITIES 74 Managing the Soldier’s Physical Load, 74 Mission-Enabling Technologies, 75 Field-Deployable Biomarkers of Neural State, 76 EEG-Based Brain–Computer Interfaces, 76 Haptic Feedback Technology for Virtual Reality, 77 Augmented Reality Technologies, 77

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xiii CONTeNTS Information Workload Management via Physiological and Neural Feedback (Including Augmented Cognition), 79 Technologies to Optimize Sensor-Shooter Latency and Target Discrimination, 79 Research-Enabling Technologies, 81 Signal Processing Challenges, 81 Fatigue and Sleep Models for Soldiers, 82 Functional MRI and Hardware to Support fMRI Research on Army Applications, 82 Transferring Laboratory Neuroimaging Technologies to Field Applications in the Far Term, 84 Optimal Control Strategies for Brain–Machine Interfaces, 85 Scientific and Technical Barriers to Neuroscience Technologies, 87 Trends in Neuroscience Technology, 87 Cognitive Psychology and Functional Imaging, 87 Targeted Delivery of Neuropharmacological Agents for Operational Purposes, 87 Multimodel Fusion of Neural Imagery and Physiological Data, 88 New Types of Averaging in fMRI, 88 Database Aggregation and Translation for Meta-analyses, 89 Default Mode Networks, 89 Priorities for Army Investment, 89 References, 91 8 LONG-TERM TRENDS IN RESEARCH 93 Trend 1: Discovering and Validating Biomarkers of Neural States Linked to Soldiers’ Performance Outcomes, 93 Genetic, Proteomic, and Small-Molecule Markers, 93 Neuroimaging Techniques, 94 Physiological Indicators of Neural-Behavioral State, 95 Trend 2: Using Individual Variability to Optimize Unit Performance, 95 How the Individual Variability Insight Affects the Army, 96 Neural Correlates for Cultural Differences in Behavior, 96 Trend 3: Recognizing Opportunities from the Vertical Integration of Neuroscience Levels, 96 Trend 4: Gaining New Insights into Adversary Response, 97 A Mechanism for Monitoring Neuroscience Research and Technology, 97 References, 98 9 CONCLUSIONS AND RECOMMENDATIONS 99 Recommendations on Neuroscience Research for Behavioral Science Applications, 99 Training and Learning, 99 Optimizing Decision Making, 100 Sustaining Soldier Performance, 100 Improving Cognitive and Behavioral Performance, 102 Recommendations on Neuroscience Technology Development, 102 Overarching Recommendations, 103 A Mechanism for Monitoring New Opportunities in Neuroscience Research and Technology, 103 Individual Variability as a Future Force Multiplier, 103 APPENDIXES A Biographical Sketches of Committee Members 107 B Committee Meetings 110 C Sampling of Behavioral and Neuropsychological Literature (2001-2007) on 112 High-Performance Athletes D Research on Managing Information Overload in Soldiers Under Stress 117

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Tables, Figures, and Boxes TaBles S-1 High-Priority Opportunities for Army Investment in Neuroscience Technologies (Recommendation 14), 2 S-2 Priority Opportunities for Army Investment in Neuroscience Technologies (Recommendation 15), 2 S-3 Possible Future Opportunities (Neuroscience Areas Worthy of Monitoring for Future Army Investment), 3 2-1 Prospective Army Applications for Neuroscience, 19 7-1 High-Priority Opportunities for Army Investment in Neuroscience Technologies (Recommendation 14), 89 7-2 Priority Opportunities for Army Investment in Neuroscience Technologies (Recommendation 15), 90 7-3 Possible Future Opportunities (Neuroscience Areas Worthy of Monitoring for Future Army Investment), 90 FiGures 2-1 Various noninvasive imaging technologies provide insight into the brain (anatomy) and mind (function), 14 5-1 Schematic diagram illustrating the likely interactions between central and peripheral components of fatigue, 47 5-3-1 Neuronal pathways in BrainBow mice, 60 7-1 Various noninvasive imaging technologies provide insight into the brain (anatomy) and mind (function), 75 BoXes 1-1 Statement of Task, 9 2-1 Computational Processes in the Human Brain, 16 3-1 Predicting Future Behavior in Extreme Environments, 28 3-2 Theory of Mind, 32 5-1 Is Salivary Cortisol a Reliable Biomarker?, 55 5-2 Pharmaco-imaging with fMRI to Predict Drug Effects, 56 5-3 Connectomics and Neural Pathway Degeneration, 60 xiv

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acronyms and abbreviations AFAST Alternative Flight Aptitude Selection Test LCD liquid crystal display AFQT Armed Forces Qualification Test lfp local field potential AIM assessment of individual motivation ANAM Automated Neuropsychological Assessment MEG magnetoencephalography Metrics MRI magnetic resonance imaging AR augmented reality ARI Army Research Institute NASA National Aeronautics and Space Administration ASVAB Armed Services Vocational Aptitude Battery NIRS near-infrared spectroscopy ATP adenosine triphosphate NMDA N-methyl-d-aspartic acid AugCog augmented cognition NonREM nonrapid eye movement NRC National Research Council BAST Board on Army Science and Technology NSBRI National Space and Biomedical Research BCAA branched-chain amino acid Institute BMI brain–machine interface BOLD blood oxygen level–dependent OEM original equipment manufacturer OT oxytocin CNS central nervous system CRT cathode ray tube PET positron emission tomography CSF cerebral spinal fluid PFC prefrontal cortex C2V command and control vehicle PTSD post-traumatic stress disorder PVT Psychomotor Vigilance Test DARPA Defense Advanced Research Projects Agency DOT diffuse optical tomography R&D research and development DSI diffusion spectrum imaging REM rapid eye movement DTI diffusion tensor imaging RPD recognition-primed decision EEG electroencephalography SAT standardized assessment test ERP event-related potential SIFT Selection Instrument for Flight Training FDA Food and Drug Administration T tesla fMRI functional magnetic resonance imaging TBI traumatic brain injury TMS transcranial magnetic stimulation GSR galvanic skin response ToM theory of mind TPJ temporoparietal junction HMI human–machine interface HPA hypothalamic-pituitary-adrenal VR virtual reality IED improvised explosive device xv

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