Most primary olfactory neurons have individually neutral effects on behavior

Abstract

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.

Sensorimotor transformation underlying odor-modulated locomotion in walking Drosophila

“…Even in our current study, if we define attraction as fraction time spent in the stimulated region, attraction downstream of single ORN classes is small (Figure 1-S1) as the fly spends more time in the vicinity of the stimulated region rather than within the region itself. This resultthat activation of single ORN class would result in either no attraction or mild attractionis consistent with most work on attraction (Tumkaya et al, 2022).…”

“…As already mentioned, much of the work in flies is aimed at understanding whether a given ORN class is attractive or repulsive (Semmelhack and Wang, 2009; Tumkaya et al, 2022) or the valence of a given ORN class. What are the implications of parallel sensorimotor loops on the valence of a ORN class?…”

“…Relating activation of different ORN classes to the movement of freely locomoting animals has predominantly been addressed only in Drosophila because of the genetic tools and the relative ease with which experiments can be performed on many flies. Much of this work has focused on the question of valence or what makes an odor attractive or repulsive (Badel et al, 2016; Bell and Wilson, 2016; Knaden et al, 2012; Tumkaya et al, 2021). To probe the mechanism of attraction – i.e., what are the changes in locomotion underlying attraction to odor in flies - we created a ring arena whose center had a fixed odor concentration, and the periphery did not have any odor (Jung et al, 2015).…”

Wind Gates Olfaction Driven Search States in Free Flight

“…Motivated by prior optogenetic activation experiments with walking flies 32,43,44,79,80 , we chose to express the red-light sensitive ion channel, CsChrimson in olfactory receptor neurons that express the co-receptor Orco using the Gal4-UAS binary expression system. Although Orco+ neurons mediate a broad range of olfactory responses that are linked to odors with a range of valences 81,82 , the behaviors we observed by activating Orco+ neurons (detailed in results) are remarkably consistent with published free flight responses of Drosophila tracking ethanol and vinegar plumes in flight (Figure 1 and S2) 8 .…”

Drosophila olfaction: past, present and future

“…Many odour-evoked behaviours have been causally linked to specific olfactory pathways, typically through analysis of olfactory receptor mutants or animals in which specific OSN populations are ablated or artificially activated. The availability of driver lines for nearly all OSN populations has enabled systematic screening for behaviours evoked upon activation of individual pathways [179,231,232]. However, robust responses are rarely observed, indicating that meaningful perception of olfactory stimuli in the brain might require combinatorial activation of multiple sensory pathways with appropriate intensity and temporal precision.…”