Robert R. Hampton - US grants

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Animals; Behavioral Paradigm; CRISP; Clip; Cognition; Cognitive Discrimination; Complex; Computer Retrieval of Information on Scientific Projects Database; Development; Discrimination; Discrimination (Psychology); Film; Funding; Grant; Individual; Institution; Investigators; Libraries; Mammals, Primates; Monkeys; NIH; National Institutes of Health; National Institutes of Health (U.S.); Performance; Pressure; Pressure- physical agent; Primates; Process; Relative; Relative (related person); Research; Research Personnel; Research Resources; Researchers; Resources; Running; Social Behavior; Social Controls; Social Interaction; Source; Stimulus; Structure; Testing; Training; United States National Institutes of Health; insight; neurobehavioral; pressure; response; social; social cognition; sociobehavior; sociobehavioral

This subproject is one of many research subprojects utilizing the resources provided by a Center grant funded by NIH/NCRR. Primary support for the subproject and the subproject's principal investigator may have been provided by other sources, including other NIH sources. The Total Cost listed for the subproject likely represents the estimated amount of Center infrastructure utilized by the subproject, not direct funding provided by the NCRR grant to the subproject or subproject staff. Primate cognition may have evolved in response to selective pressures for the ability to process complex social information. This suggests that central insights into the structure and function of primate cognition will be achieved through the study of social cognition. However, few neurobehavioral studies of primate cognition have made use of social stimuli. There is a critical need for studies of social cognition in primates. One of the issues retarding the development of such studies in monkeys is the difficulty in presenting animals with experimentally-controlled social stimuli. Our objective in this project is to develop behavioral paradigms for studying primate social cognition that permit reliable experimental control of social stimuli using digitally-edited video clips. We have created a library of primate social behavior videos. We filmed individual monkeys engaged in a variety of social behaviors and have edited these clips together to make realistic artificial social interactions. Monkeys have been trained to make dominance discriminations using these video clips. Other tests have shown that the monkeys remember individuals seen in the videos. We have discovered close parallels with human face perception in monkeys. We have successfully trained monkeys on a transitive inference task thought to be similar to dominance hierarchy learning. We have shown that monkeys readily "link" ordered lists, indicating that associative strength cannot account for performance in transitive inference tasks. We have developed techniques for automatically testing monkey cognition in large social groups.

This subproject is one of many research subprojects utilizing the resources provided by a Center grant funded by NIH/NCRR. The subproject and investigator (PI) may have received primary funding from another NIH source, and thus could be represented in other CRISP entries. The institution listed is for the Center, which is not necessarily the institution for the investigator. Conscious memory in humans is divided into two types. Semantic memory consists of facts about the world: water is scarce in the desert;seafood must be fresh to be safe. Episodic memory sub-serves the ability to recall autobiographical events: once running out of water on a desert hiking trip, the time you were sickened by spoiled clams at a beach party. While many experiments show that monkeys and other animals remember, it has proven difficult to make this important distinction between semantic and episodic memory in nonhumans. Developing procedures for distinguishing between these two types of memory in monkeys will permit us to make more effective use of nonhuman model systems for understanding normal human cognition and the diseases that affect it. We changed our approach to this project and began emphasizing anticipation of future events. Our lab has completed a series of 5 behavioral experiments on anticipation of the future in rhesus monkeys and has earned her masters degree for this work.

Imagine that you lacked autobiographical memory and could not recall what you did this morning or how you got to the room you are in now. It would certainly be difficult to organize your life and meet your obligations. Yet this is the situation faced by certain amnesic humans with damage to the temporal lobes of their brain. It is also the condition in which many scientists believe nonhuman animals exist; they are mentally "stuck" forever in the present. Studies of human amnesics have dramatically revealed the fact that apparently seamless human memory actually consists of distinct systems. Each memory system is specialized to process different information including habits and skills, general factual knowledge, and first-person autobiographical information. For example, human episodic memories are rich in contextual details that specify their source, or the occasion on which they were formed. One might experience detailed recollection of the smell of freshly mown grass as you talked to a well-dressed but unshaven young man at a wedding last August. By contrast, semantic memories lack contextual details. You know dogs have tails, but probably do not remember details of the occasion on which you learned this fact. The distinction between episodic and semantic memory in humans is central in cognitive neuroscience and has been established by the combination of behavioral studies, neuroimaging studies, and studies of patients with brain damage. In contrast, we know little about the extent to which these memory systems exist in nonhuman animals. Indeed many cognitive scientists argue that episodic memory may be uniquely human. It is impossible to evaluate this claim, or to develop appropriate animal models for the study of memory, without appropriate behavioral tests. With the support of the National Science Foundation, Dr. Robert Hampton and his students at Emory University will develop new memory tests capable of measuring aspects of episodic memory in nonhuman animals. Specifically, Dr. Hampton will develop tests to investigate whether subjects remember the source of their memories and whether they can recall as well as recognize previously experienced images. Performance on these tests will be contrasted with other memory performance and the brain basis for these types of memory will be determined. Development of these new cognitive tests, and training young scientists to use them, will enable future work on cognition and the biological mechanisms that underlie it.

In addition to advancing our understanding of memory and cognition in an important model of human cognition, this project will also have broader impacts in a number of ways: 1) Graduate students, including a large percentage of female students, are centrally involved in the research and share their enthusiasm for neuroscience through visits to high schools during events such as Brain Awareness Week. 2) Each summer, at least one student from the BRAIN program, which recruits undergraduates from groups underrepresented in science, will work on the proposed projects. 3) Undergraduate students from Dr. Hampton's introductory psychology class are recruited annually to work in the lab through research experience programs funded by Emory College. 4) Dr. Hampton and graduate students will perform docent activities at a cognition exhibit at Zoo Atlanta, thus conveying the content and excitement of their work to the public. 5) Dr. Hampton and his lab will share their findings through expansion of their existing website, which is aimed at an undergraduate level audience. One of the goals of the website is to aid in the recruitment of graduating students to neurocognitive research.

DESCRIPTION (provided by applicant): The human ability to consciously monitor the contents of memory has not been accessible to study in animal models. Memories that are accessible to monitoring are often called explicit or declarative. In contrast implicit or unconscious memories cannot be subjectively monitored, but are still evident in behavior. For example, a person who may not be able to verbally report the locations of the letters on a keyboard may nonetheless type accurately and rapidly without looking at the keys. The ability to monitor memory is a form of metacognition, which is impaired in autism, age-related cognitive decline, and attention and impulse control disorders such as ADHD. Loss of memory from stroke, Alzheimer?s disease, and other brain insults severely impairs higher cognitive processes including learning, planning, and adaptive decision-making. Animal models are needed to identify the specific brain structures involved in memory monitoring so that we can develop improved treatments for cognitive impairment in humans. In addressing these problems, the main challenge in the use of animal models is that animals cannot provide the verbal reports often used to identify memory monitoring in humans. To overcome this obstacle, we will implement new behavioral paradigms in which a ?decline test? option allows subjects to select which memory tests to take and which to avoid. Accurate memory monitoring is operationally defined as choosing to take tests when the item is remembered and avoiding tests when it is not remembered, thus providing a model of this crucial human capacity. The proposed work is the first to combine memory monitoring paradigms in an animal model with neuroanatomical techniques that will identify the neural basis of memories that are subject to monitoring. Because monitored and unmonitored memory operate simultaneously to produce adaptive behavior, the proposed studies are designed to determine how these memory types work together. Methodology called Process Dissociation Procedure is designed to quantify the simultaneous action of multiple memory systems and will be adapted from the human cognitive literature for use in the present project. I will use these new behavioral techniques to achieve three specific aims: 1) quantify the independent contributions of monitored and unmonitored memories to performance in memory tests, 2) determine whether monitored and unmonitored memories are neuroanatomically distinct, and 3) test the dual process/dual system theory of recognition memory performance. Development of this animal model system will advance work on the physiology, neurochemistry, and genetics of cognition and will contribute to the treatment of diseases affecting higher cognitive function. PUBLIC HEALTH RELEVANCE: This research is relevant to human health because it promises substantial progress in the study of memory in an important animal model of human cognition. Memory monitoring targets the type of memory most often compromised in stroke, Alzheimer's disease, and other brain insults affecting higher cognitive function. Development of this model system will permit further work on the physiology, neurochemistry, and genetics of memory that will contribute to the treatment of these devastating human conditions.

This subproject is one of many research subprojects utilizing the resources provided by a Center grant funded by NIH/NCRR. The subproject and investigator (PI) may have received primary funding from another NIH source, and thus could be represented in other CRISP entries. The institution listed is for the Center, which is not necessarily the institution for the investigator. Have you ever been unable to bring to mind the full route to a recently visited restaurant, but nonetheless could recognize the correct turns as they came up along the way? This experience captures the distinction between two modes of memory retrieval. "Recall" is when you "bring to mind" things that are not currently present, such as when you remember all the turns you must take to get to your destination before setting out. By contrast "recognition" is when you can tell that something you currently experience is familiar, such as a given intersection where you must turn right, and is comparatively easier than recall. Many tests for nonhuman animals show that they can recognize something seen before as familiar, just as your dog or cat recognizes you when you come home. There is no doubt that animals have memory. But humans have different types of memory that depend on different parts of the brain, and we do not yet know whether monkeys or other animals share most of these different types of memory. We have discovered that rhesus monkeys can remember simple shapes and reproduce them later on a touchscreen computer, an ability that may show that they can "bring to mind" images that are physically absent, a powerful skill in humans. The development of this new technique for studying memory in monkeys will lead to more accurate characterization our cognitive evolution over the 30 million years that separate humans from our shared ancestor with rhesus monkeys. We have also documented factors that regulate memory for lists of stimuli, and have begun studies of memory for the source of information in monkeys. Studies of memory in monkeys will also help us understand what biological factors are responsible for the erosion of recall abilities that occurs in human amnesia and normal aging.

This subproject is one of many research subprojects utilizing the resources provided by a Center grant funded by NIH/NCRR. Primary support for the subproject and the subproject's principal investigator may have been provided by other sources, including other NIH sources. The Total Cost listed for the subproject likely represents the estimated amount of Center infrastructure utilized by the subproject, not direct funding provided by the NCRR grant to the subproject or subproject staff. The human ability to consciously monitor the contents of memory has not been accessible to study in animal models. Because humans talk about memories that are accessible to monitoring, such memories are called declarative. In contrast, nondeclarative memories cannot be subjectively monitored, but are inferred from their influence on behavior. For example, a person who may not be able to verbally report the locations of the letters on a keyboard may nonetheless type accurately and rapidly without looking at the keys. Loss of declarative memory from stroke, Alzheimer's disease, and other brain insults severely impairs higher cognitive processes including learning, planning, and adaptive decision-making. Memory monitoring is also a form of metacognition. Impaired metacognition is implicated in autism, age-related cognitive decline, and attention and impulse control disorders such as ADHD. Animal models are needed to identify the specific brain structures involved in memory monitoring and declarative memory so that we can develop improved treatments for cognitive impairment in humans. We trained 6 monkeys in a delayed-response task and replicated all the major findings from previous research in monkey metamemory. This work is summarized in the MA thesis of Victoria Templer and is currently being prepared for publication. Twelve monkeys have been trained in the matching-to-sample and classification task necessary for the next experiments in this project. Several monkeys have begun training in the metamemory task.

DESCRIPTION (provided by applicant): The human ability to consciously monitor the contents of memory has not been accessible to study in animal models. Memories that are accessible to monitoring are often called explicit or declarative. In contrast implicit or unconscious memories cannot be subjectively monitored, but are still evident in behavior. For example, a person who may not be able to verbally report the locations of the letters on a keyboard may nonetheless type accurately and rapidly without looking at the keys. The ability to monitor memory is a form of metacognition, which is impaired in autism, age-related cognitive decline, and attention and impulse control disorders such as ADHD. Loss of memory from stroke, Alzheimer?s disease, and other brain insults severely impairs higher cognitive processes including learning, planning, and adaptive decision-making. Animal models are needed to identify the specific brain structures involved in memory monitoring so that we can develop improved treatments for cognitive impairment in humans. In addressing these problems, the main challenge in the use of animal models is that animals cannot provide the verbal reports often used to identify memory monitoring in humans. To overcome this obstacle, we will implement new behavioral paradigms in which a ?decline test? option allows subjects to select which memory tests to take and which to avoid. Accurate memory monitoring is operationally defined as choosing to take tests when the item is remembered and avoiding tests when it is not remembered, thus providing a model of this crucial human capacity. The proposed work is the first to combine memory monitoring paradigms in an animal model with neuroanatomical techniques that will identify the neural basis of memories that are subject to monitoring. Because monitored and unmonitored memory operate simultaneously to produce adaptive behavior, the proposed studies are designed to determine how these memory types work together. Methodology called Process Dissociation Procedure is designed to quantify the simultaneous action of multiple memory systems and will be adapted from the human cognitive literature for use in the present project. I will use these new behavioral techniques to achieve three specific aims: 1) quantify the independent contributions of monitored and unmonitored memories to performance in memory tests, 2) determine whether monitored and unmonitored memories are neuroanatomically distinct, and 3) test the dual process/dual system theory of recognition memory performance. Development of this animal model system will advance work on the physiology, neurochemistry, and genetics of cognition and will contribute to the treatment of diseases affecting higher cognitive function. PUBLIC HEALTH RELEVANCE: This research is relevant to human health because it promises substantial progress in the study of memory in an important animal model of human cognition. Memory monitoring targets the type of memory most often compromised in stroke, Alzheimer's disease, and other brain insults affecting higher cognitive function. Development of this model system will permit further work on the physiology, neurochemistry, and genetics of memory that will contribute to the treatment of these devastating human conditions.

This subproject is one of many research subprojects utilizing the resources provided by a Center grant funded by NIH/NCRR. Primary support for the subproject and the subproject's principal investigator may have been provided by other sources, including other NIH sources. The Total Cost listed for the subproject likely represents the estimated amount of Center infrastructure utilized by the subproject, not direct funding provided by the NCRR grant to the subproject or subproject staff. "Recall" is when you "bring to mind" things that are not currently present, such as when you remember all the turns you must take to get to your destination before setting out. By contrast "recognition" is when you can tell that something you currently experience is familiar, such as a given intersection where you must turn right, and is comparatively easier than recall. Many tests for nonhuman animals show that they recognize something seen before as familiar, but no previous work has shown that monkeys or other animals share the ability to recall with humans. We have discovered that rhesus monkeys remember simple shapes and reproduce them later on a touchscreen computer, an ability that may show that they can "bring to mind" images that are physically absent. The development of this new technique for studying memory in monkeys will lead to more accurate characterization our cognitive evolution. We have also documented factors that regulate memory for lists of stimuli. We have developed new techniques for interfering with memory in monkeys that show that familiar, repeated items are actively maintained in memory, while novel items are remembered well, but not using active memory. We have established a new paradigm for studying order memory in monkeys and shown that monkeys discriminate which image was viewed first. Accuracy is a function of temporal distance and recency. These studies of memory in monkeys help us understand what biological factors are responsible for the erosion of recall abilities in human amnesia and normal aging.

Cognitive evolution in humans has likely been influenced by selection for adept social behavior. Determining the ways in which social and nonsocial cognition share common representational and brain systems is therefore critical for understanding cognition. Transitive inference (TI) is the ability to infer the relation between two items based on relations with a third (e.g. Dave is taller than Sue, Sue is taller than Jake, therefore Dave is taller than Jake). Transitive inference, while useful in many domains, may have been selected specifically for learning social dominance relationships. The researchers have created infrastructure for remote computerized cognitive testing of monkeys in large social groups as well as in laboratory housed subjects. This infrastructure allows them to study naturally acquired social knowledge and compare it with social and non-social knowledge acquired in the laboratory. They anticipate that this research will determine the ways in which social and nonsocial transitive inference depend on the same cognitive systems, will document mechanisms of logical inference in TI, and will identify the contribution of a part of the primate brain, the hippocampus, to TI. This research is important because it will advance our understanding of the brain mechanisms critical for social behavior and those critical for more abstract reasoning. The researchers? unique remotely accessible cognitive testing system is being used to provide Emory University undergraduate students with hands on experience designing and conducting primate cognition experiments. In the future it may allow members of groups underrepresented in science, such as physically disabled persons and students at institutions with few scientific resources, to participate in the scientific process, thus promoting diversity in the professional scientific community. The investigators also share findings with the public through their active website and activities a Zoo Atlanta.

DESCRIPTION (provided by the applicant): The proposed Training Program will train predoctoral students in the mechanisms of learning across development and species. Learning is fundamental to adaptive behavior. It involves acquiring and modifying information, behaviors, and skills. Learning also is productive: it extends itself through induction, deduction, and integration. Mechanisms of learning is a critical area to target for predoctoral research training because learning has pervasive impacts in both adaptive and maladaptive behavior, and must be an integral part of any successful mental health or educational intervention. The Training Faculty is drawn from the Department of Psychology, the Yerkes National Primate Research Center, and the interdisciplinary Neuroscience Graduate Program, all of Emory University. The primary training sites are the Department of Psychology and the Yerkes National Primate Research Center. The 16- member Training Faculty approach study of the mechanisms of learning as they manifest from birth to old age in healthy and clinical populations using genetic, comparative, computational, developmental, neurobiological, and neuropsychological techniques. They examine how changes in the brain during infancy and childhood relate to developmental changes in learning, how the elderly adapt with their aging brains, and how diverse species acquire and modify knowledge ranging from simple associations to culturally-mediated rituals and traditions. The diversity of ages, species, and circumstances in which learning mechanisms are studied at Emory provides rich opportunities for accumulation of converging evidence about these mechanisms, and thus for equipping the next generation of scientists with the skills necessary for understanding basic mechanisms of learning. The training site affords a uniquely well- suited environment in which to accomplish one of the goals of the NIH-to unite the study of developmental change from infancy to senescence with the study of adult cognition within a neurobiological framework. We request four predoctoral trainees per year, each of whom will be trained for 3 years. Trainees will be drawn from among students in Emory's highly-selective Laney Graduate School. Trainees will complete all departmental or program requirements for the Ph.D. This training program will provide added value through at least five training enhancements: 1) explicit co-mentoring and collaborative research experiences across species, ages or methodologies; 2) intensive training in grant writing, 3) advanced training in ethics and the responsible conduct of research; 4) participation in courses, workshops and research fairs specific to research on learning across development and species; and 5) application of empirically supported best practices in graduate student training.

Metacognition is the ability to think about one's own thought processes, which is critical for sophisticated cognition. For example, understanding how well you know a new vocabulary word allows you to decide when to stop studying words as they are learned. Metacognition involves both monitoring one's own ongoing cognitive processes and exerting cognitive control over them. The proposed research is significant because it will identify the role of cognitive monitoring and control in complex nonhuman primate cognition. This comparative research will advance knowledge of the evolution of complex cognition and of what makes humans unique. The investigators will promote public education about cognitive science and primate cognition through visits to K-12 classrooms and developing an interactive kiosk at the local zoo that allows visitors to experience the same cognitive tests performed by the primates on exhibit. Throughout the research project, undergraduate and graduate students will receive training for careers in science.

Evidence from psychophysical and memory tests indicates that nonhuman primates introspectively monitor some cognitive processes, for example showing selective avoidance of difficult tests. This research will determine the role of cognitive monitoring for cognitive control in primates by examining which cognitive systems are accessible to cognitive monitoring and which are not. Cognitive systems accessible to cognitive monitoring will be distinguished from those that are not by testing for dissociations between accuracy and confidence in tasks involving multiple memory systems contributing to accuracy, and by using psychophysical tests that dissociate motor and perceptual processes. Specific studies address these goals through consideration of 1) the extent to which primates regulate the amount of information they acquire prior to taking tests; 2) what information primates monitor when making metacognitive judgments; 3) the extent to which primates strategically exercise cognitive control only when necessary and adaptively allocate monitoring among competing tasks; and 4) the role of language-like mental representations in cognitive monitoring and control. These comparative studies will determine the extent to which there have been changes in cognitive monitoring and cognitive control through primate evolution.