2014217 NeuroNex: From Odor to Action - Discovering Principles of Olfactory-Guided Natural Behavior

This project addresses a central question of neuroscience: How do animals use information from stimuli in their environment to guide natural behav- iors? Several factors support our plan to address this question by focusing on the olfactory system. Olfaction is an evolutionarily ancient sense. Animals gather odors from their environments to inform survival-critical behaviors such as finding food and mates, or avoiding predators and toxins. These natural behaviors can be largely replicated in lab settings, using stimuli that are natural in composition, and dynamics. Olfactory systems of mammals and insects have independently evolved common structural elements at successive levels of processing in their central nervous systems. Olfactory systems share these structural elements likely due to convergent evolution towards a set of similar solutions to shared olfactory problems. This convergence suggests that the comparative approach that we propose will lead to the discovery of fundamental principles and constraints that could not be discovered by study of a single species-which highlights the importance of the planned theoretical work. Because this project is interdisciplinary, comparative, and theory-driven, it will require a well-integrated team, working synergistically to address overlapping questions. We will coordinate our efforts to achieve convergence and synergy between team members from diverse backgrounds, expertise, and interests, that are key to the transformative potential of this work.

Fundamental to the work that we propose is a comparative approach to understanding neural representations and behavior in a range of species including mice, flies (adults and larvae), bees and locusts. Each one of these species offers advantages including experimental tractability, behavioral complexity, relevance of the specific ethological niche, etc. Nonetheless we propose to identify common theoretical principles in the ways in which the nervous systems of these organisms represent and transform olfactory stimuli, as well as how their behavioral responses change as a function of odor identity and intensity.
Theories at different scales and levels of abstraction will inform and be tested in this project. To exploit the variety of data sources and species we propose to use will require that we identify common principles and test central theoretical ideas. Generally, neuroscience needs to bring experimentalists and theorists together in a more systematic and productive way to maximize the benefit of novel experimental approaches and make investments into complex and expensive experiments more valuable. However, despite widespread agreement on the general importance of theory and modeling in neuroscience, there is no consensus on which kind/level of theory will be most important for making progress. Traditional dynamical systems models of neurons and circuits have provided insights into the nature and limits of single neuron and local circuit computation. Statistical models provide important information about the information available to neurons for making decisions and generating actions. Therefore in this project we bring together computational/theoretical approaches in areas like dynamical systems, information theory, abstract geometry, machine learning/AI, and machine vision.

This coordinated project on the neuroscience of olfaction across species will have important societal impacts in science, technology, health, and policy. Given the complexity and high dimensionality of chemical space and its primacy in driving behavior among most species, studying how odor leads to action promises to provide insight into optimal biological solutions for encoding complex information about the external world. Biology far outstrips human engineered systems in identifying and processing our chemical world. This is why animal chemical detectors (e.g. scent dogs and explosive-detecting rats) are the best available solutions for applications like explosive and drug detection. Because it is a dominant mode of communication among plants and animals, chemical communication is critical to healthy ecosystems and productive agriculture, as well as for repelling pests. In humans, loss of the sense of smell is associated with loss of a sense of quality of life and the inability to identify danger signals, such as smoke and rotting food. Elucidating biological solutions to olfaction can inform the development of algorithms and engineered devices for detection and identification of chemicals in applications that span the range from homeland security to food safety.