Odor-identity dependent motor programs underlie behavioral responses to odors

Abstract

All animals use olfactory information to perform tasks essential to their survival. Odors typically activate multiple olfactory receptor neuron (ORN) classes and are therefore represented by the patterns of active ORNs. How the patterns of active ORN classes are decoded to drive behavior is under intense investigation. In this study, using Drosophila as a model system, we investigate the logic by which odors modulate locomotion. We designed a novel behavioral arena in which we could examine a fly’s locomotion under precisely controlled stimulus condition. In this arena, in response to similarly attractive odors, flies modulate their locomotion differently implying that odors have a more diverse effect on locomotion than was anticipated. Three features underlie odor-guided locomotion: First, in response to odors, flies modulate a surprisingly large number of motor parameters. Second, similarly attractive odors elicit changes in different motor programs. Third, different ORN classes modulate different subset of motor parameters.DOI: http://dx.doi.org/10.7554/eLife.11092.001

WalkingDrosophilanavigate complex plumes using stochastic decisions biased by the timing of odor encounters

“…As expected, flies were more likely to be oriented upwind when the odor was on ( Figure 2C), as previously reported [14,18,[20][21][22][23]49]. However, unlike for flies walking into a spatially homogeneous odor block [20,39,40], changes in average angular speed were minor, with a less than 10% change between blocks ( Figure 2D). Walking speeds were similarly unmodulated, again in contrast to walking flies in homogenous odor blocks ( Figure 2E) [20].…”

“…It is surprising that despite the rich locomotive repertoire of walking Drosophila, a large part of their olfactory navigational strategy can be reduced to four actionsleft turn, right turn, walk and stop. Still, we expect that differences in wind conditions and in odor identity and valence might modulate finer motor control in navigation [39]. A recent, systematic study of the locomotive structure of walking Drosophila in various odor environments without horizontal wind has found that behaviors fall into a limited number of states comprising a hierarchical hidden Markov model [57].…”

“…Upwind bias results not from modulating turn magnitude or frequency but rather turn direction: the randomly-occurring saccades are more likely to be oriented upwind when the frequency of odor encountersbut not their duration or concentrationis high, suggesting an important role for precise odor timing detection [35][36][37][38]. Prior studies have shown that flies increase walking speed at the onset of a uniform odor blocks [20,39,40]. In our spatiotemporal plume, flies spend only a fraction of time (~15%) experiencing detectable odor concentrations, and we expectedly do not find an appreciable increase in walking speed.…”

Behavior Reveals Selective Summation and Max Pooling among Olfactory Processing Channels

“…The low dimensionality of olfactory behavior in our data is likely a consequence of the simple experimental paradigm we have used. In other contexts, olfactory behavior may have a higher dimensionality (Jung et al, 2015). …”

Dynamics of memory-guided choice behavior in <i>Drosophila</i>

“…For example, flies modulate their locomotor activity in response to many stimuli, such as odors with different biological significance. 40) Another recent study reported that locomotor activity influences sugar preference behavior. 41) Advances in these studies are based on emerging computational image analysis techniques, which enable the measurement of multiple behavioral parameters of individual flies.…”