Encoding of Wind Direction by Central Neurons in Drosophila
Mechanosensation is perhaps one of the most mysterious senses. We use mechanosensation to care for young, to avoid harm, and to explore the world around us. It plays a crucial role in the lives of many organisms. However, how the nervous system integrates sensory information at the periphery to create a coherent percept remains mostly unclear.
In a recent study, we sought to understand how mechanosensory information at the periphery is translated into a higher-order signal that an animal can use to direct behavior (Suver et al. 2019).
To analyze the function of specific central mechanosensory circuits and their presynaptic inputs originating at the periphery, we took advantage of the powerful tools available in the fruit fly Drosophila melanogaster. By doing so, we elucidated novel central circuits in a model where powerful genetic tools enabled targeted circuit analysis and manipulation in both electrophysiological and behavioral paradigms.
In insects, wind information provides a crucial signal indicating where odors originate. Because odors are carried by wind, measuring wind direction enables them to navigate towards hosts, mates, prey, and food. We know from many previous studies that insects, including fruit flies, rely on wind-induced movements of the antennae to measure wind direction.
To assess how fruit flies use this information to guide behavior, we first used miniature wind tunnels in which we track the movements of single freely-walking flies in the presence of pseudo-laminar wind and odor stimuli. Using these behavioral arenas, we measured how input from the two antennae is used to navigate toward attractive odors.
These experiments revealed that both antennae are necessary for robust olfactory navigation behavior, suggesting that integration between these sensory structures is crucial and likely happens somewhere in the central brain.
We next wanted to understand how mechanosensory signals from the antennae are represented along the sensory pathway leading to central brain regions. By designing an apparatus that precisely delivers directional wind stimuli and measuring antennal deflections, we found that movements of one antennae encode an ambiguous wind direction signal. However, by combining motions across the two antennae, a linear readout of wind direction could be generated, supporting conclusions from the behavioral experiments that both antennae are important for measuring wind direction.
To trace how movements of these sensors are combined in the central brain, we performed an electrophysiological screen to identify novel mechanosensory pathways encoding wind direction. Using intracellular recordings from genetically identified neurons, we found that mechanosensory neurons encode tonic deflections of the antennae. These neurons also share a similar ambiguity in wind direction encoding as single antenna movements.
We then discovered a completely novel set of third-order mechanosensory neurons that combine information from the two antennae to create a remarkably linear representation of wind direction. Using additional techniques including two-photon lesions, pharmacology, precise physical manipulations of the sensors, and cutting-edge genetic tracing techniques, we developed a model of how this information is processed at several levels in the central brain by distinct classes of mechanosensory neurons.
Overall, this study established how information from two sensors is decoded by neurons in the central brain to create a high-level representation of external signals.
—Marie Suver, PhD
Read the paper “Encoding of Wind Direction by Central Neurons in Drosophila” in Neuron, published April 1, 2019.