CRCNS: Multimodal integration for spatial navigation

Spatial orientation is a fundamental cognitive function required for survival. To navigate, an animal must know its location and its heading. The neurons thought to underlie the sense of direction are known as head-direction cells, which respond maximally when an animal is facing in a particular direction. Collectively, these cells form a cognitive map, analogous to a compass, that specifies heading direction relative to the surrounding world. How do neural circuits evaluate and combine multimodal cues to robustly and accurately build a cognitive map? This proposal applies an integrated experimental and theoretical approach to a well-characterized navigation center, the Drosophila central complex and, in particular, the ellipsoid body, which is known to use multimodal sensory information to provide the fly with its sense of orientation in the world. One of the most important cues that flies and other insects use for this purpose is the sky. In addition to the location of the sun, insects use the polarization pattern and chromatic gradient of sunlight scattered by the atmosphere, which persist even when the sun is clouded over. Lightpolarization has a preeminent role in controlling the fly's compass system, but polarization, by itself, suffers from a 180° ambiguity as a directional signal. We hypothesize that the compass system resolves this ambiguity by combining polarization and sky-color information, and that these together are the primary drivers of the heading direction system in a natural setting. Our preliminary data supports this hypothesis by showing that a visual ring neuron, presynaptic to directional-selective compass neurons, integrates polarization and color information. The proposed work will unravel fundamental mechanisms of sensory integration for goal-directed behavior by 1) Determining how chromatic information is relayed to the Drosophila compass system, 2) Uncovering how ch romatic signals are combined with polarization signals to create an unambiguous sky map, and 3) Exploring the dominant role played by sky compass signals and how they interact with other directional cues to determine heading direction. RELEVANCE (See instructions): The completion of the proposed aims will explain how neural circuits construct a cognitive map by optimally weighing multi-sensory streams to achieve a robust yet flexible representation of direction in the world. The achieved understanding will be mechanistic, at the level of specific neurons and synapses. Our focus on multisensory integration will have broad implications for many cognitive functions, such as learning and memory, which require integrating multimodal cues.