Odor attraction in walking Drosophila melanogaster is commonly used to relate neural function to behavior, but the algorithms underlying attraction are unclear. Here, we develop a high-throughput assay to measure olfactory behavior in response to well-controlled sensory stimuli. We show that odor evokes two behaviors: an upwind run during odor (ON response), and a local search at odor offset (OFF response). Wind orientation requires antennal mechanoreceptors, but search is driven solely by odor. Using dynamic odor stimuli, we measure the dependence of these two behaviors on odor intensity and history. Based on these data, we develop a navigation model that recapitulates the behavior of flies in our apparatus, and generates realistic trajectories when run in a turbulent boundary layer plume. The ability to parse olfactory navigation into quantifiable elementary sensori-motor transformations provides a foundation for dissecting neural circuits that govern olfactory behavior.

Neurons in putative decision-making structures can reflect both sensory and decision signals, making their causal role in decisions unclear. Here, we tested whether rat posterior parietal cortex (PPC) is causal for processing visual sensory signals or instead for accumulating evidence for decision alternatives. We disrupted PPC activity optogenetically during decision making and compared effects on decisions guided by auditory versus visual evidence. Deficits were largely restricted to visual decisions. To further test for visual dominance in PPC, we evaluated electrophysiological responses after individual sensory events and observed much larger response modulation after visual stimuli than auditory stimuli. Finally, we measured trial-to-trial spike count variability during stimulus presentation and decision formation. Variability decreased sharply, suggesting that the network is stabilized by inputs, unlike what would be expected if sensory signals were locally accumulated. Our findings suggest that PPC plays a causal role in processing visual signals that are accumulated elsewhere. Defining the neural circuits that support decision making bridges a gap between our understanding of simple sensorimotor reflexes and our understanding of truly complex behavior. However, identifying brain areas that play a causal role in decision making has proved challenging. We tested the causal role of a candidate component of decision circuits, the rat posterior parietal cortex (PPC). Our interpretation of the data benefited from our use of animals trained to make decisions guided by either visual or auditory evidence. Our results suggest that PPC plays a causal role specifically in visual decision making and may support sensory aspects of the decision, such as interpreting the visual signals so that evidence for a decision can be accumulated elsewhere.

Odor attraction in walking Drosophila melanogaster is commonly used to relate neural function to behavior, but the algorithms underlying attraction are unclear. Here we develop a high-throughput assay to measure olfactory behavior in response to well-controlled sensory stimuli. We show that odor evokes two behaviors: an upwind run during odor (ON response), and a local search at odor offset (OFF response). Wind orientation requires antennal mechanoreceptors, but search is driven solely by odor. Using dynamic odor stimuli, we measure the dependence of these two behaviors on odor intensity and history. Based on these data, we develop a navigation model that recapitulates the behavior of flies in our apparatus, and generates realistic trajectories when run in a turbulent boundary layer plume. The ability to parse olfactory navigation into quantifiable elementary sensori-motor transformations provides a foundation for dissecting neural circuits that govern olfactory behavior.

Olfactory inputs are organized in an array of functional units (glomeruli), each relaying information from sensory neurons expressing a given odorant receptor to a small population of output neurons, mitral/tufted (MT) cells. MT cells respond heterogeneously to odorants, and how the responses encode stimulus features is unknown. We recorded in awake mice responses from “sister” MT cells that receive input from a functionally characterized, genetically identified glomerulus, corresponding to a specific receptor (M72). Despite receiving similar inputs, sister MT cells exhibit temporally diverse, concentration-dependent, excitatory and inhibitory responses to most M72 ligands. In contrast, the strongest known ligand for M72 elicits temporally stereotyped, early excitatory responses in sister MT cells, consistent across a range of concentrations. Our data suggest that information about ligand affinity is encoded in the collective stereotypy or diversity of activity among sister MT cells within a glomerular functional unit in a concentration-tolerant manner.

To navigate towards odor in a turbulent environment, animals integrate odor value cues with wind direction cues. The central neural circuits subserving this behavior are unknown. Here we used optogenetic activation to identify neurons in the lateral horn (LH), mushroom body (MB), and fan-shaped body (FB), that drive upwind orientation in walkingDrosophila. Using calcium imaging, we show that MB/LH neurons encode odor independent of wind direction, and that odor and wind are integrated within hΔC local neurons of the FB to drive re-orientation. Based on connectome data, we model an FB circuit that allows odor to switch behavioral orientation to wind. Our work identifies central neural circuits that integrate value and direction signals to generate an essential goal-directed behavior.