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8
Long-Term Trends in Research
Chapters 3 through 6 identified and discussed near- to medium-term research opportunities that the committee judges could have high value for Army applications. The committee’s specific recommendations on these opportunities are presented in Chapter 9. Task 4 of the statement of task asks the committee to “determine trends in research and commercial development of neuroscience technologies that are likely to be of importance to the Army in the longer term.” Important long-term trends in technology development were discussed in Chapter 7, along with specific technology opportunities evaluated by the committee. This chapter presents important long-term trends in neuroscience research, including research aimed at expanding our fundamental understanding and applied research that has particular relevance for the Army. The committee believes the Army should monitor the progress of research in these areas and evaluate the results for promising Army-relevant applications. In addition to the research trends themselves, the chapter describes the type of mechanism needed for monitoring progress in both research and technology development.
The soldier is the centerpiece of every Army operation, and the Army will always depend on its soldiers to accomplish its missions. Just as physics and chemistry are the foundational sciences for military ballistics and platform systems, neuroscience as defined in this report is the foundational science for the soldier. The foremost research objectives of the Army should include increasing the survivability of soldiers, both in combat and under the other extreme conditions in which they operate, while sustaining and enhancing their performance.
With these soldier-focused objectives in mind, the committee has identified four trends to represent the breadth and potential importance of research in neuroscience:
Discovering and validating biomarkers for neural states linked to soldiers’ performance outcomes.
Using individual variability to optimize unit performance.
Recognizing opportunities from the vertical integration of neuroscience levels.
Gaining new insights into the behaviors of adversaries.
TREND 1:
DISCOVERING AND VALIDATING BIOMARKERS OF NEURAL STATES LINKED TO SOLDIERS’ PERFORMANCE OUTCOMES
As discussed in Chapters 3 through 6, the cognitive and behavioral performance of soldiers in many areas—training and learning, decision making, and responding to a variety of environmental stressors—has substantial neurological components. How the brain functions, even how it is functioning at a particular time, makes a difference in these and other types of performance essential to the Army’s missions. The techniques used to study and understand brain functioning at all levels—from the molecular and cellular biology of the brain to observable behavior and soldier interactions with other systems—are providing an ever-increasing number of potential indicators of neural status relevant to Army tasks. The Army will need to monitor these techniques and technologies for their potential to serve as biomarkers of differences in neural state that reliably correlate with changes in performance status. To illustrate this tendency for performance biomarkers to emerge from the methods of studying the brain, three broad kinds of such methods are discussed here: genomic and proteomic markers, neuroimaging techniques, and physiological indicators of neural state or behavioral outcome.
Genetic, Proteomic, and Small-Molecule Markers
The development and functioning of the central and peripheral nervous systems of all animals, including humans, are regulated by genomic and proteomic factors. The genomic factors are associated with the nucleic acids of every cell. From embryonic development through senescence, the
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inherited genome and epigenetic1 modifications of it regulate the expression of proteins critical for neural cell functions. This regulated gene expression produces signaling elements (transmitters), signal receivers (receptors), guidance of communication processes (axons and dendrites), and cell–cell recognition materials.
Known genetic markers may, for example, allow identification of individuals at greater risk of damage from exposure to chemical agents or more likely to succumb to post-traumatic stress disorder. The cost of genetic tests is likely to decrease substantially in the next decade, while their effectiveness will increase markedly. Of the 20,000-25,000 genes in the human genome, more than 100 are involved in axonal guidance alone (Sepp et al., 2008). At least 89 genes have been shown to be involved in the faulty formation of the axon’s myelin sheath (dysmyelination), associated with the development of schizophrenia (Hakak et al., 2001). Understanding the human genes associated with development of the brain and peripheral nervous system can shed light on differential human susceptibilities to brain injury and may aid in predicting which pharmacological agents will be useful for sustaining performance. The Army should position itself to take advantage of the continuing scientific progress in this area.
A proteomic marker (a type of biomarker) is a protein (generally an enzyme) whose concentration, either systemically or in specific tissues, can serve as a reliable and readily measurable indicator of a condition or state that is difficult or even impossible to assay directly. Small variations in gene structure (polymorphisms) are often associated with differences in concentration of a particular protein in a particular tissue of a particular individual, so there are important linkages between genetic factors and proteomic markers. However, specific enzyme concentrations (including tissue-specific concentration) can also be influenced (upregulated or downregulated) in response to environmental factors that vary on timescales of hours, or roughly the timescale of preparation for and conduct of an Army operation. Thus, proteomic markers can vary with recent or current conditions (environmental stressors, for example) and can also reflect the genetic traits of an individual soldier.
Proteomic markers known to signal a change in vigilance or cognitive behavior include salivary amylase, blood homovanillic acid (which correlates with dopamine metabolism), and lactic acid (a metabolic product of glucose metabolism that increases as a result of intense muscle exercise). Proteomic factors associated with fatigue resistance include microtubule-associated protein 2 and the muscarinic acetylcholine receptor. Comparison of an individual’s current concentration (titer) of one of these proteomic markers with his or her baseline titer could quantify one or more neural (cognitive/behavioral) states relevant to the status of the individual’s current abilities.
Neurohormones and neuropeptides—biologically active molecules much smaller than proteins or the nucleic acids of the genome—are another emerging class of markers of neurological and cognitive state and of psychophysiological response to stress. A study of candidates for the U.S. Navy Sea, Air, and Land Forces (SEALs) found that candidates with strong stress-hormone reactions to behavioral challenges like abrupt changes or interruptions are less likely to complete training successfully than those with weak reactions (Taylor et al., 2006, 2007). Another example is the work discussed in Chapter 3 on oxytocin, a neuropeptide signal, which is released when an individual experiences a sense of trust (Kosfeld et al., 2005; Zak et al., 2005). Hormonal markers are easily gathered with simple blood draws. The level in the bloodstream of a neural signaling molecule such as oxytocin has at best a very indirect relationship to its level in the brain; it may be necessary to figure out how to monitor its release in the hypothalamus. The monitoring of neurohormones and neuropeptides is likely to be a powerful means of identifying individuals who are well suited to particular tasks and may lend itself to assessing candidates for Special Operations training in particular.
Neuroimaging Techniques
Neuroimaging technologies available in the 2008-2010 time frame allow visualization of brain regions that are activated during action-guiding cognitive processes such as decision making. These activation patterns enable brain activity to be correlated with behavior. These imaging technologies and techniques include structural magnetic resonance imaging for volumetric analysis of brain regions, functional magnetic resonance imaging (fMRI) for cognitive control networks, diffusion tensor imaging for transcranial fibers, and hyperspectral electroencephalography (EEG).
Applications to Soldier Training
As an example relevant to evaluation of training, fMRI scans before and after training sessions can be compared to examine changes in the brain’s response to novel training-related stimuli. Novel visual and auditory inputs activate the brain in specific regions. An analysis of event-related potentials combined with fMRI before and after novel auditory cues revealed that a particular event-related potential (a P300-like potential, which is to say a positive potential occurring approximately 300 msec after a triggering stimulus) is associated with fMRI patterns of activity in the bilateral foci of the middle part of the superior temporal gyrus (Opitz et al., 1999). Only novel sounds evoke a contrasting event-related potential (an N400-like negative potential). Individuals with a strong response of the second type also have fMRI scans showing activation in the right prefrontal cortex. These
1
An epigenetic modification refers to changes in gene expression from mechanisms other than alteration of the underlying DNA sequence.
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observations suggest that an indicator based on combining fMRI and event-related potential could be used to assess training to criterion. At criterion—for example, when 90 percent of the appropriate responses are exhibited in response to a cue—effective training will no longer elicit a “novel-type” brain functional response or event-related potential response (Opitz et al., 1999).
Fear is a critical response to threat that can compromise appropriate action of an individual soldier or an entire Army unit. To incorporate desensitization to fear-invoking situations into soldier training, fMRI scans could be compared before and after training to determine which environments elicit fear-correlated neural activity patterns. A prime example is the response of soldiers in Operation Desert Shield and Operation Desert Storm when sensors for chemical warfare agents indicated that the environment might contain an active agent. These fear-invoking events led to significant disorganization of military units, even when the sensor warnings were false positives.
Tracking Change in the Visual Field
The ability to track dynamic changes in objects present in a soldier’s visual field is of great benefit to Army personnel. Examples include the sudden appearance of a potential threat on a Force XII Battle Command Brigade and Below display and the apparent change of terrain indicating recent placement of an improvised explosive device (IED). Jeremy Wolfe of Harvard has demonstrated that the visual system must focus on only a very limited region within the visual field to detect change (Angier, 2008). To accommodate human limitations, fMRI neurotechnology could be used to detect minor changes in the visual field and correlate them with activation events in the hippocampus (Bakker et al., 2008). Related research has shown that shifts in visual attention to objects in a field of view tend to occur either as a series of microsaccades (rapid naturally occurring eye movements) or in response to cueing signals in the field of view. Recent studies suggest that the latter is more important (Horowitz et al., 2007).
Leveraging Opportunities for Neuroimaging Techniques
EEG and EEG image processing will continue to advance, and EEG will be incorporated in multimodal imaging equipment with magnetic resonance imaging and magnetic encephalography. The high-payoff opportunity here is to leverage this work to develop a sensor array that can be used on a free-moving subject. A good initial goal for proof-of-concept would be the collection of stable trace data from a treadmill runner.
For neuroimaging with near-infrared spectroscopy (NIRS), DARPA has been active in R&D on NIRS sensor arrays that can be worn in situ. This is an opportunity to advance a noninvasive cerebral blood monitoring tool. Expected improvements in the next 5 years include advanced designs for multichannel data collection from cortical sources. In the 10- to 20-year time frame, one R&D opportunity is to use NIRS for more accurate imaging of the deeper brain.
Physiological Indicators of Neural-Behavioral State
Physiological indicators include individual characteristics such as age, gender, muscle power, neuroendocrine effects, neuromuscular function, vascular tone, and circadian cycling. While neural information processing is primarily a result of brain functioning and can be revealed by brain imaging, the general wellness and physiological condition of the entire human organism can affect combat capability and response to threat. This is true in large part because the brain depends on nutrient input (e.g., glucose and oxygen) via the circulatory system and on neuroendocrine function involving other organ systems. (The complex interactions between the brain and other organ systems of the body were discussed in Chapters 2 and 5.)
For Army applications, physiological indicators of neural state are important because they are often more readily accessible and measurable in the field than more direct indicators of neural state derived from neuroimaging techniques. As discussed in Chapter 2 in the section on reliable biomarkers for neurophysiological states and behavioral outcomes and in Chapter 7 in the section on field-deployable biomarkers, the idea is to find a monitorable physiological condition that correlates to a neural state with sufficient accuracy and precision to be useful as a reliable sign of that state. Often, the laboratory studies that define the neural state and establish the correlation will begin with neuroimaging techniques (such as fMRI).
TREND 2:
USING INDIVIDUAL VARIABILITY TO OPTIMIZE UNIT PERFORMANCE
Early systems neuroscience experiments used functional neuroimaging tools—fMRI, positron emission tomography, EEG, or magnetoencephalography—to learn how the various brain systems process cognitive and affective functions (Van Horn et al., 2004). It has become increasingly clear that individuals do not process tasks in the same way but instead engage different brain systems, with the particular systems engaged depending in part on the underlying default brain state (Greicius et al., 2003; Esposito et al., 2006). Neuroscientists are increasingly appreciating the importance of interindividual variability regarding which neural signals are operative during various tasks. Instead of being discouraged by this variability, investigators have begun to use its enormous potential for optimizing training and performance. Paying attention to this variability helps in understanding how different individuals learn differently when acquiring a skill or how they organize their behavior when faced with extreme conditions.
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How the Individual Variability Insight Affects the Army
The significance for the Army of this paradigm-shifting insight from neuroscience is profound. Understanding in a systematic way the variability among individuals in brain processing when performing the same task is an initial step toward understanding the systematic differences from one individual to another in how they respond in similar circumstances. For example, some individuals engage emotional processing areas even in simple but challenging cognitive tasks (McIntosh et al., 1996; Beauregard et al., 2001). It would be important to determine whether activation of these emotional processing areas helps or interferes with the cognitive task at hand. If it helps in performing the task, perhaps others can learn to enhance their performance on that type of task if they are trained by methods that activate the emotional processing areas. If such activation interferes with the cognitive task, one might implement training strategies that attenuate the effects of emotional processing. Most important, however, whether performance of a cognitive task is enhanced or degraded by emotional processing may differ across groups of individuals. In this case, an optimal training program would develop modulation strategies tailored for a particular group.
The significance of individual variability for optimizing task performance extends to areas other than training and learning. Chapter 4, for example, noted that individuals show traitlike (i.e., stable for the individual over time) differences in decision-making styles. Chapter 5 emphasized the importance of individual variability in neurophysiological responses to stressors typical in Army mission environments and in responses to countermeasures to those stressors. Given that what needs to be optimized from the standpoint of Army operations is performance of the unit, not the individual, the insight from neuroscience is that a higher optimum may be achievable and sustainable by learning to work with and exploit individual variability rather than treating soldiers as interchangeable parts to be mass-produced on a training assembly line.
Neural Correlates for Cultural Differences in Behavior
Even as it comes to accept this insight into the substantial neurological basis for interindividual variability, the Army will still need to look for some general patterns in variability from which to draw statistically valid general conclusions—that is, the conclusions might be expressed in terms of a distribution in a given population or culture rather than as single-point characterizations or predictions. As a simple example, there are cultural differences in attitudes to deception that often depend on the social role of the individual. There are also well-established gender differences in neural correlates of behaviors, such as social responsiveness (Proverbio et al., 2008) and reward anticipation (Hoeft et al., 2008), and some differences are linked to proteomics (e.g., levels of brain-derived neurotrophic factors or other factors expressed in brain tissue). Western and Eastern cultures process mathematics differently (Tang et al., 2006), and there is every reason to expect that such cultural differences will also exist in other cognitive processing tasks. Identifying and understanding these differences will be critical in such applications as interacting with noncombatants in peacekeeping or in security and stability operations (SASO) missions, as well as in predicting adversary responses and decision making.
A still-open question is whether such cultural and individual differences exist all the way down to the genetic/cellular level or whether they disappear at some level. To use the deception example, even if cultural conditioning (or specific training) means that some individuals do not show “normal” physiological or neural indicators of deliberate lying, is there some type of monitoring that could detect if a subject being interrogated is responding in a “contrary-to-truth” manner?
TREND 3:
RECOGNIZING OPPORTUNITIES FROM THE VERTICAL INTEGRATION OF NEUROSCIENCE LEVELS
As discussed in Chapter 2, neuroscience exists on four hierarchical levels, which are now being vertically integrated, from the levels of molecules and cells to the levels of behavior and systems. Increasingly, discoveries and advances at one level are leading directly to discoveries and advances at levels higher and lower in the hierarchy. Given this trend, the Army needs to remain cognizant of research in multiple fields that could impact neuroscience applications on multiple levels.
One such opportunity will serve as a simple example: At the level of behavioral research, a variety of methodologies can be used to assess soldier response. Among these are measures of the efficiency with which a task is performed, subjective self-assessments, and psychophysiological correlates. Often the outcomes from these separate methodologies more or less converge. For instance, as an individual’s performance of a task degrades, the individual also subjectively feels more stressed by the demands of the task. Convergence of the assessment results increases confidence that we understand the responses. However, what happens when methodologies from the same or different levels in the hierarchy produce results that do not converge? Divergence raises the question of which technique is a better indicator of the subject’s real condition, that is, of the “ground truth” (Yeh and Wickens, 1988; Hancock, 1996). Often the question can be answered by moving up or down in the hierarchy of integrated levels to determine, for example, which of the divergent neuroimaging results is consistent with a behavior conventionally used to define a neural state of interest. Or, one might test whether seemingly similar behaviors are truly the same by examining activation patterns from one or more neuroimaging techniques.
Another example of an opportunity derived from the vertical integration hierarchy is this: The neuroscience literature
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contains many cases in which neurological signals indicate that an attentive brain has processed a signal but the subject, when asked, denies any conscious knowledge of such processing. Are such cases of divergence between assessments also exhibited at different levels—perhaps a general pattern of response divergence—or are they a function of the task that is imposed, of differences in the assessment methods, of characteristics of the individual being tested, or of some other combination of factors?
Divergence of results is likely to become more frequent, at least for a time, as neuroscience assessment methods proliferate. When results from multiple neuroimaging techniques diverge, is this evidence that the physical signal to which a neuroimaging technique is responding is inherently different from the signal to which another technique is responding? Or, is it instead an idiographic characteristic of the individual being tested, or perhaps just an artifact of nuances in the imposed task and the task environment? As they have throughout the history of any scientific discipline, such divergences spur and orient further inquiry into the methodologies themselves and whether the phenomena they transduce as an information signal are in fact correlates of the same underlying reality (here, brain function or processing event). The Army can leverage the ongoing research efforts on neuroscience methods, especially with regard to the method(s) it selects for field implementation. In short, as neuroscience applications come to use two or more neuroimaging techniques, the Army can benefit from the natural direction of inquiry, which is to investigate and resolve seemingly divergent results.
TREND 4:
GAINING NEW INSIGHTS INTO ADVERSARY RESPONSE
Negative social interactions, such as the emergence and growth of distrust or the initiation of hostile behavior, are a relevant aspect of social neuroscience. The neural correlates of these types of social behavior are not yet well understood. However, fairly simple interventions at the neural level can have substantial, if temporary, effects on higher-level functioning, such as the administration of thiopental sodium (Pentothal), a medical anesthetic for psychotherapy under sedation in order to recover repressed memories together with the emotion that accompanied the repressed experience.
The work with the neuropeptide oxytocin, described in Chapter 3, indicates that this neural signaling agent is associated with the bonding of offspring and parents and of intimate couples and that it is released under conditions that evoke trust between individuals. Similarly, recent neuroscience experiments have revealed that individuals show specific brain-related changes when engaging in altruistic behavior (Moll et al., 2006). Understanding how the human brain changes as individuals turn to confrontation from cooperation or turn an adversarial relationship into a friendly one provides an important scientific opportunity for the Army in terms of both the overarching implications of such understanding and the concrete mechanisms of neurological changes. Understanding the neural correlates of this change may, for example, help an intelligence analyst to predict when responses of potential adversaries (or of non-combatants potentially allied with the Blue or Red force) will reverse direction.
A MECHANISM FOR MONITORING NEUROSCIENCE RESEARCH AND TECHNOLOGY
Neuroscience research and applications are advancing at a lightning-like pace, and the Army needs to continually assess the potential of these advances. The growing knowledge base will have many direct and indirect applications to soldiers, applications that will increase their operational effectiveness. A neuroscience monitoring group, consisting of recognized leaders in neuroscience research in both the academic and business communities, would help those making Army science and technology funding decisions to assess the relevance of progress in nonmilitary neuroscience to Army applications. Research results and emerging technology can be relevant, whether through direct adaptation for Army use or as a starting point for further Army-oriented R&D, funded or otherwise fostered by the Army. To ensure that this monitoring group remains sensitive to and keeps abreast of Army needs, its membership should include Army civilians and soldiers with appropriate backgrounds and interests to participate meaningfully in the group’s deliberations.
The committee envisions that such a monitoring group would operate mainly by attending and reporting on the presentations at conferences and other meetings of professional societies for the neuroscience-relevant disciplines. Of course, the journals of these societies are also important sources of information, but they may not contain ideas, research accomplishments, or information on commercial products, all of which can be gathered by participation in and interactions at professional meetings. Once the nascent and emerging hot topics are identified, the published literature becomes a useful tool for documenting them and covering their progress. The monitoring group would be alert to neuroscience advances and opportunities reported through national and international societies and organizations promoting neuroscience and neuroscience-related research and collaborations of value to the Army. Examples of such organizations include these:
Cognitive Neuroscience Society,
Federation of European Neuroscience,
Human Factors and Ergonomics Society,
International Society for Magnetic Resonance in Medicine,
Organization for Human Brain Mapping,
Radiological Society for North America (focuses on commercial imaging),
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Society for Neuroscience, and
Society of Automotive Engineers.
There are also regular conferences that the Army can monitor to track the rapidly developing field of computational neuroscience. These include the Neural Information Processing (NIPS) conference, the biannual Statistical Analysis of Neural Data (SAND) workshop, the annual Computational and Systems Neuroscience (Cosyne) meeting, the annual Computational Neuroscience meeting, and the annual Dynamical Neuroscience meeting. The meetings are a venue for discussions on recent work in the fields of computational neuroscience modeling and signal processing.
The number of Army representatives attending a conference should be large enough to allow coverage of simultaneous sessions that may contain relevant research: two or three persons for smaller conferences, six or more for large gatherings. Each attendee could generate a report to the Army and one of them could summarize the advances and identify possible Army applications. At least yearly, the entire monitoring group would gather, together with additional military guests, to share new Army needs and to discuss the group’s recent findings and expectations for Army-relevant neuroscience.
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