Animals use olfactory receptors to navigate mates, food, and danger. However, for complex olfactory systems, it is unknown what proportion of primary olfactory sensory neurons can individually drive avoidance or attraction. Similarly, the rules that govern behavioral responses to receptor combinations are unclear. We used optogenetic analysis in Drosophila to map the behavior elicited by olfactory-receptor neuron (ORN) classes: just one-fifth of ORN-types drove either avoidance or attraction. Although wind and hunger are closely linked to olfaction, neither had much effect on single-class responses. Several pooling rules have been invoked to explain how ORN types combine their behavioral influences; we activated two-way combinations and compared patterns of single- and double-ORN responses: these comparisons were inconsistent with simple pooling. We infer that the majority of primary olfactory sensory neurons have neutral behavioral effects individually, but participate in broad, odor-elicited ensembles with potent behavioral effects arising from complex interactions.

Animals use olfactory receptors to navigate mates, food, and danger. However, for complex olfactory systems, it is unknown what proportion of primary olfactory sensory neurons can individually drive avoidance or attraction. Similarly, the rules that govern behavioral responses to receptor combinations are unclear. We used optogenetic analysis in Drosophila to map the behavior elicited by olfactory-receptor neuron (ORN) classes: just one-fifth of ORN-types drove either avoidance or attraction. Although wind and hunger are closely linked to olfaction, neither had much effect on single-class responses. Several pooling rules have been invoked to explain how ORN types combine their behavioral influences; we activated two-way combinations and compared patterns of single- and double-ORN responses: these comparisons were inconsistent with simple pooling. We conclude that the majority of primary olfactory sensory neurons have neutral behavioral effects individually, but participate in broad, odor-elicited ensembles with potent behavioral effects arising from complex interactions.

Optogenetics has become an important tool for the study of behavior, enabling neuroscientists to infer causations by examining behavior after activating genetically circumscribed neurons with light. Light-induced neural activity is affected by illumination parameters used in experiments, such as intensity, duration, and frequency. Here, we hypothesized that the intensity of light and the presence of oscillations in illumination would alter optogenetically induced olfactory behaviours. To test this, we activated olfactory receptor neurons (ORNs) in Drosophila by using either static or pulsed light stimuli across a range of light intensities. The various regimes elicited distinct behavioral valence responses (attraction, aversion, indifference) from several ORN types. Our results demonstrate the importance of both frequency and intensity for interpreting optogenetic behavioral experiments accurately;successfully generalizing optogenetic results requires the use of more than a single illumination regime.

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