Lucia F. Jacobs - US grants

The size of the hippocampus, a brain structure known to mediate spatial learning, is correlated with spatial behavior in wild rodents. In this career advancement award, a comparison will be made of the spatial learning ability of different species on abstract learning tasks. Using operant methods, pairs of species, known to differ in hippocampal size, will be compared on two operant tasks known to involve the hippocampus (spatial delayed- nonmatch-to-sample, simultaneous odor discrimination) and two tasks that do not require an intact hippocampus (auditory discrimination, successive olfactory discrimination). Two species of kangaroo rats (Dipodomys) and two species of voles (Microtus) will be compared. It is predicted that, within each genus, the species with a larger hippocampus will show superior learning ability on hippocampal tasks, particularly the spatial task, but that there should be no species differences on nonhippocampal tasks. The proposed study will be significant for several reasons. It will be the first comparative study of different types of memory in wild rodents. Because our understanding of the physiology of memory in mammals is largely based on the laboratory rat, it is important to know if laboratory rats show typical rodent behavior. More importantly, comparative studies of closely related rodent species can identify what features of a species's habitat can lead to increases in learning and memory capacity. Not only can this study help us to understand the evolution of animal memory, but it can also help us to understand the hippocampus, a structure critical in both animal and human memory. For example, no other animal study has attempted to compare performance of different tasks involving the hippocampus (maze learning, odor discrimination). Thus, this study will shed light not only on the evolution of memory, but on the function of the hippocampus, a structure of clinical importance.

Seasonal changes in learning ability have been described in various vertebrate species. Studies of changes in sexually dimorphic learning abilities and its neural basis in birds have yielded important new insights to our understanding of the vertebrate brain. Yet much of the significance of this work remains limited to the special case of song learning in birds. I propose a mammalian model for the seasonal modulation of cognitive sex differences: spatial learning ability in rodents. Recent work on several species of wild rodents, in particular the meadow vole, Microtus pennsylvanicus, has shown that sex differences in spatial learning are modulated by seasonal cues, such as day length. Moreover, there is preliminary evidence that the size of the brain structure underlying this behavior, the hippocampus, also changes seasonally. Seasonal changes in spatial learning have also been reported in humans, and as the hippocampus plays a key role in human memory, a rodent model of this phenomenon would have important theoretical and clinical implications. Until now, the further development of such a rodent model has been hampered by insufficient knowledge of natural spatial behavior in these species, particularly in the winter. In the past, understanding the function of natural space use in rodents has proved critical to predicting the patterns of learning and brain structure observed in the laboratory. The gap in our knowledge of winter behavior has been due to the technical difficulties of using radiotelemetry to track small mammals in this season. I propose here a novel use of an existing technology, passive integrated transponders, to solve this technical problem. Using an array of scanners to detect the movements of wild meadow voles tagged with transponders, I propose to document seasonal changes in space use. Although this novel technology could spawn numerous applications for the study of behavior, its present purpose would be to collect detailed movement data during the critical transition period between nonbreeding and breeding status in late winter and early spring. The array will be installed in a preexisting meadow vole study enclosure, so that the entire population can be marked and monitored. Finally, to relate sex differences in natural movements to changes in learning ability, voles from six density-matched control populations from similar study enclosures, will be shipped to my laboratory for measurement of spatial learning ability, using standard assays.

Intellectual Merit
This project mixes results and methods from cognitive psychology, computational vision and learning, neuromechanical systems biology, and robotics to develop a computer assisted environment for studying animal sensorimotor strategies, discovering how they undergird animal cognitive capabilities, and using those insights to inspire new algorithms for robot navigation, localization and situational awareness. We observe live, intact, highly mobile terrestrial invertebrate predators such as ghost crabs, desert scorpions and tiger beetles in carefully constructed habitats that challenge their ability to negotiate terrain and navigate space. We automate the collection, annotation and mathematical model extraction of their behavior from massive, parallel real-time recordings of visual, muscle, neural, and biomechanical recordings. We mine these data sets to develop intuitive hypotheses as well as formal mathematical representations of the basis on which these animals organize their own sensorimotor data streams to compile novel behaviors from previously consolidated constituents in a process of autonomous mental development. We add numerous existing sensor suites to highly agile existing robot bodies and instantiate algorithmically the hypothesized animal models to develop supporting or refuting evidence that challenges and refines them.
Broader Impacts
Scientifically, the new computational tools and ideas we identify in the interrelations we set up promise a bridge between whole areas of disciplines that have long been divided by spatiotemporal scale and the concomitant gap in analytical tradition, terminology and methods. For example, the study of these complex competencies in simpler species offers a new glimpse at the building blocks of cognition in species more closely related to humans. From the perspective of technological invention, algorithms pioneered in this research could lend an animal-like quality to a machine?s proximal tenacity in engaging its environment and even its overall situational awareness within unstructured worlds. For example, the team is inspired to imagine what it might be like to have a search and rescue robot with the (taskable) capabilities of a ghost crab. From the perspective of training and education, the automated database collection and management tools developed in this project bring to a mass audience the conceptual and computational building blocks that have heretofore been the exclusive province of a small group of experts. For example, a universally accessible (?cloud-based?) tool for unifying the design, parsing, display, and cross comparison of robots and animals searchable at will from the most intimate to the broadest scale of design and operation would have a profound impact on the ability of teachers at many different levels to motivate the fascination and unity of both synthetic and biological science.

This project was developed at an NSF Ideas Lab on "Cracking the Olfactory Code" and is jointly funded by the Physics of Living Systems program in the Physics Division, the Mathematical Biology program in the Division of Mathematical Sciences, the Chemistry of Life Processes program in the Chemistry Division, and the Neural Systems Cluster in the Division of Integrative Organismal Systems. The project is a synergistic combination of laboratory experiments and computer modeling that will lead to better understanding of how animals use the sense of smell to navigate in the real world. Almost universally, from flies to mice to dogs, animals use odors to find critical resources, such as food, shelter, and mates. To date, no engineered device can replicate this function and understanding the code used by the brain will lead to many novel applications. Cracking codes, from neural codes to the Enigma code of WWII, is aided by a deep understanding of the content of messages that are being transmitted and how they will be used by their intended receivers. To crack the olfactory code, the team will focus on how odors move in landscapes, how animals extract spatial and temporal cues from odor landscapes, and how they use movement for enhancing these cues while progressing towards their targets. The proposed work encompasses physical measurement of odor plumes, behavioral measurement of animals' paths through olfactory environments, electrophysiological and optical measurement of neural activity during olfactory navigation, perturbations of the environment via virtual reality and of neuronal hardware via genetics, and multilevel mathematical modeling. The PIs will teach and work with undergraduate, graduate and postdoctoral students and especially recruit students from underrepresented groups in science. The project's results may lead to improved methods for the detection of explosives, new olfactory robots to replace trained animals, and new theoretically-grounded advances in robotic control. The project will inform the development of technologies that interfere with the ability of flying insects (including disease vectors and crop pests) to locate their odor target, thus opening a new door for developing 'green' technologies to solve problems that are of global economic and humanitarian importance.

This proposal is a synergistic combination of laboratory experiments and computational modeling that will probe how animals use olfaction to navigate in their environment. Specifically, this effort seeks to solve the difficult problem of olfactory navigation through the following aims: (i) Generate and quantify standardized, naturalistic odor environments that can be used to perform empirical and theoretical tests of navigation strategies; (ii) Determine phenomenological algorithms for odor-guided navigation through behavioral experiments in diverse animal species; (iii) Determine how odor cues for navigation are encoded and used in the nervous system by recording neuronal data and simulating putative neural circuits that implement these processes; (iv) Manipulate olfactory environments and neural circuitry, to evaluate model robustness. In contrast to previous attempts to understand olfactory navigation, the present strategy emphasizes mechanisms that are biologically feasible and explores the wide range of temporal and spatial scales in which animals successfully navigate. The project will generate datasets of immediate use and importance to scientists in theoretical biology and mathematics, engineering (fluid mechanics, electronic olfaction, and robotics) and biology (neuroscience, ecology and evolution).

Many animals hoard their food, hiding food items in various locations in order to retrieve them at a later date, for example, when resources are scarce. Scatter-hoarding animals store each food item in a different location and often engage in protective behaviors that may prevent their food stores (caches) from being stolen. These behaviors include handling food items extensively before burying them, travelling away from competitors to bury food, and carefully covering caches. Scatter-hoarding fox squirrels (Sciurus niger) perform unique behaviors (head flicks, paw manipulations) that allow them to determine the weight and value of individual food items and protect their caches accordingly. By using Global Positioning System (GPS) and tracking technology, behavioral observations, and DNA testing, the researchers will explore how these food protection behaviors contribute to successful cache retrieval or prevent theft of caches by other squirrels. This study also will explore whether individuals are more or less likely to steal from their relatives. The proposed research will fill a gap in the animal behavior literature by advancing our understanding of how animals recover food they have buried, and illuminating whether scatter-hoarding animals provide for their offspring or close relatives by allowing theft of their caches.

Studies of scatter-hoarding animals have yet to address key questions: do cache protection strategies deter theft by pilferers and help scatter-hoarding animals recover their caches? Fox squirrels (Sciurus niger) perform unique assessment behaviors (head flicks, paw manipulations) that allow them to adjust investments in caches. The proposed studies will determine how a squirrel's assessment of food is related to its investment in a cache, and whether these behaviors reduce pilferage. This study will use GPS data and radio-telemetry/passive transponders to measure caching and pilfering behavior. They will also amplify and sequence established microsatellite loci to estimate genetic relatedness and incorporate relatedness into models of cache retrieval and pilferage. Food-storing animals engage in cache protection behaviors because theft is common. Previous studies have failed to examine the complex relationship between food assessment, cache protection, social context and the long-term fate of caches. Moreover, most studies utilize artificial caches made by humans or laboratory animals. This field study will use an innovative, interdisciplinary approach to examine the pilferage of caches made by free-ranging squirrels. This study also will examine the relationship between kin selection and pilferage tolerance, support for which would have major implications for our understanding of scatter-hoarding and social behavior. All data and analyses will be made available via published manuscripts, conference presentations, reports to the NSF and otherwise as suggested by NSF guidelines.