Verner P. Bingman - US grants

The ability of animals and human beings to learn and remember is an adaptation that permits organisms to change their behavior when confronted with changing environmental conditions. The ability to learn and remember is a consequence of having a brain that can change in response to new experiences. One of the major goals for researchers studying the nervous system is to identify particular brain areas or structures that are important for specific kinds of learning and memory. To do so, a variety of animals are studied. In choosing an experimental animal, one generally looks for specialized behavior that may simplify the task of linking brain regions with particular functions. Dr. Bingman's research tries to take advantage of the specialized navigational skills of homing pigeons to identify brain regions important for spatial learning and spatial memory. The basic design of the research project is to surgically remove specific brain regions and then examine what effect such treatment has on homing-pigeon navigational behavior. By examining homing-pigeon behavior following surgical manipulation of the brain, one can begin to construct how various brain regions contribute to the spatial learning and spatial memory used by pigeons to navigate home. Dr. Bingman's research should result in a better understanding of the relationship between memory/learning and the brain. By clarifying how changes in the brain may lead to memory impairments, this research may also help to enhance our understanding of memory disorders in humans.

The behavioral and neural organization of learning and memory, and the relationship among brain, cognition and behavior, pose many important questions, with significant theoretical and clinical implications. Investigating these questions, will require analysis of both the behavioral and neural structure of learning and memory. The proposed research will investigate these issues by taking advantage of the exceptional spatial navigation ability of homing pigeons, which makes these birds an excellent, ecologically valid model for the study of the neurobiology of learning and memory. Studies examining the role of the hippocampal formation in homing pigeon navigation have revealed a complex picture that emphasizes the importance of this brain structure for the learning of navigational mechanisms. Results from a recently completed study suggest that the specific role of the hippocampal formation for spatial learning can be traced to its critical participation in a learning process in which the location of stimuli in space is learned using a directional reference system. The proposed research is designed to more completely explore this hypothesis by examining more broadly the effects of hippocampal lesions on learning. Spatial and nonspatial tasks will be employed. Some of the tasks require the use of directional reference if learning is to take place. The prediction is that hippocampal lesions will disrupt learning on only those tasks that involve a spatial reference. Because of the superb spatial learning ability of homing pigeons, the results will produce a great deal of basic information about the relationship among brain, behavior and cognition.

9807476 Bingman A large body of research has established the crucial role of the hippocampus in learning and memory. In animals, the hippocampus is particularly important for learning about space. Of special interest are electrophysiological studies in rats that have demonstrated the existence of "place cells", cells that respond when an animal is in a particular location in its environment. It is generally believed that these place cells participate in the neural representation (map) of environmental space that enables animals to efficiently navigate among goal locations. Given the importance of this research for understanding brain/behavior relations, it is surprising that place cells have only been intensively studied in rats. But to what extent do the properties of place cells in rats generalize to other vertebrate species and to what extent are they a necessary design feature of hippocampal mediated spatial representations? The proposed research is designed to investigate the possible existence and eventual properties of cells in the bird hippocampus that display space specificity (i.e. place-like cells). Electrophysiological recordings of single units in the hippocampus will be taken from pigeons allowed to freely move in an open field environment. Unit activity data will then be correlated with simultaneously recorded location information from pigeons to determine if a unit responds preferentially when a pigeon is in a particular location. The data will then be used to determine whether rats and pigeons, species that have a hippocampus used for spatial learning but otherwise very different in terms of lifestyle, behavior and brain organization, represent space similarly at the neural level. The study could fundamentally change how we view the hippocampus and the spatial representations it constructs, the environmental/beha vioral features that control the activity of hippocampal cells, and the evolution of the relationship between brain and cognition.

Vertebrate animals, including man, are able to experience past events in their lives as memory because the nerve cells of the brain are able to create a physical record of those past events. A large body of experimental research has identified one brain structure, the hippocampus, as being critically important for the formation of new memories. However, how the physiological activity of nerve cells in the hippocampus are able to contribute to the physical record of past events we call memory remains uncertain. The problem to be studied in the proposed research exploits the remarkable spatial memory ability of homing pigeons and the important role of the hippocampus in that spatial memory. Electrodes, which permit the recording of activity from single nerve cells, will be surgically implanted in the hippocampus of homing pigeons. The electrodes will be used to observe how nerve cell activity changes as a consequence of exploration and the formation of new memory in pigeons allowed to freely move in an open environment. Changes in nerve cell activity as a consequence of behavior and memory would provide important information on how the hippocampus creates a physical record of past events.
How the brain creates a physical record of past experiences is one critical dimension that contributes to the uniqueness of each individual. This is apparent and tragically evident in people who suffer memory loss as a consequence of brain disease, brain trauma or just aging, and gradually or quickly experience a loss of identity. Basic research using animal models is a fundamental part of unraveling the mystery of how the brain creates memories and what goes wrong when an unhealthy brain loses its ability to create new memories. By studying how activity in the nerve cells of the bird hippocampus participates in memory formation, valuable insight may be gained regarding the relationship between the hippocampus, including the human hippocampus, and memory, and help in understanding how dysfunction in the hippocampus can lead to memory loss.

Collaborative Research: Sleep in nocturnal bird migrants, an interdisciplinary study

Verner P. Bingman
Bowling Green State University
Animals spend their lives either awake or asleep. Wakefulness allows animals to interact effectively with their environment, while waking performance is contingent on sleep, the function of which remains largely unknown. An animal may mitigate the conflict between sleep and wakefulness by engaging in unihemispheric sleep, a unique state during which one cerebral hemisphere sleeps while the other remains awake. This interdisciplinary, collaborative project takes advantage of nocturnal bird migrants as a natural model system to study the behavioral and physiological properties of sleep, the consequences of naturally occurring sleep loss, and the compensatory adjustments that accompany sleep loss. Most bird species are active during the day and sleep at night, exceQt during migration when their migratory flights occur at night. By traveling at night a migrating bird experiences reduced threat of predation, improved atmospheric conditions for flight, and more time to feed during the day. Advantages of nocturnal migration aside, birds necessarily lose sleep by migrating at night and changes in sleep behavior could have adverse consequences. Laboratory and field studies of sleep in the Swainson' s Thrush, an intercontinental bird migrant, are combined to ask how seasonally sleep deprived birds compensate for that deprivation at the behavioral and physiological level. The contribution of the study is measured in terms of both application of methodology to the study of sleep and understanding the function of sleep.

Many animal species are capable of migrating or homing over great distances, but understanding how they are able to find their way has been one of the biggest unsolved mysteries in the fields of animal behavior and sensory perception. It has been long suspected that homing pigeons, and possibly other animals, have a map based on the earth's magnetic field that allows the to return to their loft even from distant places where they have never been before. The researchers will use a novel approach which combines behavioral, neuropysiological and molecular techniques in the laboratory and the field to confirm the existence of a magnetic map in homing pigeons and to determine how it functions. The researchers will track the flight paths of pigeons with GPS units in the field to determine how they respond to changes in the earth's magnetic field on the way home to their loft. By disrupting the pigeons' magnetic sense, which is located in the upper beak, the researchers will test and refine a model that explains how the earth's magnetic field could provide latitude and longitude coordinates for navigation. In the laboratory, the researchers will train pigeons to navigate using a virtual magnetic map. With this new approach it will be possible to study how the pigeons perceive the magnetic field and how such information is processed in the brain during homing behavior. This project will provide a better understanding of fundamental questions in animal navigation, sensory perception, and animal learning. It also has direct relevance to other fields such as conservation (effects of climate change on stop-over sites and thus migration routes), human health (control of disease transmission by migratory animals), and the development of a satellite-independent backup Global Positioning System (GPS). The researchers will involve undergraduate students in the experiments (especially from underrepresented groups as part of the NSF-funded SetGo program) as well as provide summer research internships for talented high school students in support of K-12 initiatives and a workshop for local high school teachers.

The ability of many animals to navigate through their environment far exceeds what humans are able to do without the help of technology. Exceptional navigation is not limited to animals with large brains, like birds and mammals. It can also be found in animals with simpler nervous systems. The tropical amblypygid, a scorpion-like animal, is able to find its way home at night through dense, tropical forest understory. The study of how different types of sensory information (visual, chemical, tactile) are processed by amblypygids as they solve navigation problems can reveal fundamental design properties of simple nervous systems that are somehow capable of controlling complex, learned behavior. These design properties can inspire engineering solutions applicable to robotic and artificial intelligence systems. The study of charismatic tropical amblypygids also serves as an alluring gateway for teachers to introduce K-12 students to the importance of neuroscience for understanding how organisms acquire and process information from their environment and how this information influences learning and memory. To support engagement with K-12 students, their teachers and the general public, researchers supported by this grant will develop internet-based educational materials in both English and Spanish.

By conducting behavioral experiments that assess amblypygid (Phrynus pseudoparvulus) movements after displacement from a home refuge, researchers will assess the relative importance of visual, chemical and mechanical information in supporting navigation. These experiments will either involve manipulation of animal sense organs or the sensory cues in their environment. The neurobiological work will focus on a brain area known as "mushroom bodies", which are thought to support spatial memory. In parallel with the behavioral work, researchers will explore the nervous system routes by which information from different sensory stimuli is sent to the mushroom bodies. Particular attention will be given to how the mushroom bodies "engineer" or "integrate" the different sensory inputs. The integration of sensory inputs is hypothesized to be necessary to support complex navigation and will likely have applied potential for design of sophisticated artificial systems. Finally, the importance of the mushroom bodies in navigation, and their capacity to combine different sources of sensory information, will be tested under the same conditions of the behavioral experiments noted above, except using animals whose mushroom bodies are impaired.