Computations underlying Drosophila photo-taxis, odor-taxis, and multi-sensory integration

Abstract

To better understand how organisms make decisions on the basis of temporally varying multi-sensory input, we identified computations made by Drosophila larvae responding to visual and optogenetically induced fictive olfactory stimuli. We modeled the larva's navigational decision to initiate turns as the output of a Linear-Nonlinear-Poisson cascade. We used reverse-correlation to fit parameters to this model; the parameterized model predicted larvae's responses to novel stimulus patterns. For multi-modal inputs, we found that larvae linearly combine olfactory and visual signals upstream of the decision to turn. We verified this prediction by measuring larvae's responses to coordinated changes in odor and light. We studied other navigational decisions and found that larvae integrated odor and light according to the same rule in all cases. These results suggest that photo-taxis and odor-taxis are mediated by a shared computational pathway.DOI: http://dx.doi.org/10.7554/eLife.06229.001

The use of computational modeling to link sensory processing with behavior in Drosophila

“…A number of studies using Drosophila have examined the impact of visual, chemosensory, or thermal cues on navigational decisions (Gomez-Marin et al 2011;Clark et al 2011;Censi et al 2013;Klein et al 2014;Gepner et al 2015;Schulze et al 2015). In these studies, the detailed recording of fly movement parameters with a quantitative, model-supported analysis of the behavior revealed the navigational strategies with which Drosophila negotiates its environment to find food and avoid noxious chemical, heat, or light stimuli.…”

The use of computational modeling to link sensory processing with behavior in Drosophila

“…Drosophila larval behaviors can easily be classified into three relatively stereotyped motor programs during chemotaxis: phases of straight locomotion (termed "runs"), intense side-to-side movement of the head ("head casting"), and fast reorientation events ("turns"). Models that explain the relation between chemosensory cues and navigation behaviors usually use the rate or probability of performing one of these behaviors as a function of the stimulus (Gomez-Marin et al 2011;Gepner et al 2015;Schulze et al 2015;Hernandez-Nunez et al 2015). Based on an accurate description of the larva's sensory experience as well as of its complete body posture during navigation, the authors determined the features of the odor concentration gradient that triggered turning and head casting using STA-like analyses.…”

“…Several studies of Drosophila have employed decoding models to investigate the relationship between chemosensory codes and behavior (Parnas et al 2013;Gepner et al 2015;Hernandez-Nunez et al 2015;Badel et al 2016;Bell and Wilson 2016). For example, (Hernandez-Nunez et al 2015) asked how the activity of gustatory receptor neurons (GRN) affects chemotaxis behavior.…”

“…(Gepner et al 2015) studied how visual and chemosensory cues are integrated during larval orientation behavior. Visual stimuli were provided using blue light and chemosensory neurons were activated optogenetically (via csChrimson, (Klapoetke et al 2014)) using red light, which is outside the sensitivity range of the photoreceptors.…”

Illuminating odors: when optogenetics brings to light unexpected olfactory abilities

“…For instance, this approach was implemented to study navigational decisions in Drosophila larvae (Gepner et al 2015). The larvae are known to avoid light to increase their survival in the dark but are attracted by some odorant cues such as ethyl acetate (EtAc).…”