Summary Animals use olfactory receptors to navigate danger, mates, and food. However, for complex olfactory systems, it is unknown what proportion of olfactory-receptor neurons (ORNs) can individually drive avoidance or attraction. Similarly it is unclear what rules govern behavioral responses to ORN-activity combinations. We used optogenetic analysis in Drosophila to map the behavior elicited by nearly all ORN classes; just one-fifth of ORNs drove either avoidance or attraction. Although wind and hunger are closely linked to olfaction, neither context had much effect on single-ORN-class behavior. Various models have been used to explain the way multiple ORNs combine their behavioral influences, including several simple pooling rules. To assess these, 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 ORN types have neutral behavioral effects individually, but participate in broad, odor-elicited ensembles with potent behavioral effects arising from complex interactions.