Multisensory interactions regulate feeding behavior in Drosophila

Abstract

The integration of two or more distinct sensory cues can help animals make more informed decisions about potential food sources, but little is known about how feeding-related multimodal sensory integration happens at the cellular and molecular levels. Here, we show that multimodal sensory integration contributes to a stereotyped feeding behavior in the model organism Drosophila melanogaster. Simultaneous olfactory and mechanosensory inputs significantly influence a taste-evoked feeding behavior called the proboscis extension reflex (PER). Olfactory and mechanical information are mediated by antennal Or35a neurons and leg hair plate mechanosensory neurons, respectively. We show that the controlled delivery of three different sensory cues can produce a supra-additive PER via the concurrent stimulation of olfactory, taste, and mechanosensory inputs. We suggest that the fruit fly is a versatile model system to study multisensory integration related to feeding, which also likely exists in vertebrates.

Odors drive feeding through gustatory receptor neurons inDrosophila

“…Once PER brings the labella into contact with the food, GRNs act as a multisensory integrator to make a decision on food intake (Figure 4C). Because inputs from olfactory and gustatory organs interact centrally as well (Oh et al, 2021; Shiraiwa, 2008) (Figure 2A), this indicates that unified chemosensory experience is built through layered integration in different parts of the body.…”

“…PER is an initial step of feeding evoked by the presentation of sugar to the proboscis or legs housing gustatory receptor neurons (GRNs). Previous studies reported that odors increase the rate of PER (Oh et al, 2021;Reisenman and Scott, 2019;Shiraiwa, 2008), exemplifying olfactory enhancement of feeding in Drosophila. However, aside from the involvement of olfactory receptor neurons (Oh et al, 2021;Shiraiwa, 2008), biological mechanisms underlying this multisensory enhancement remain elusive.…”

Neural Circuits Underlying Behavioral Flexibility: Insights From Drosophila

“…For instance, although feeding responses are primarily determined by the taste of a food source, they can be strongly modulated by its smell, texture, and temperature. Flies show a feeding response when their legs contact sugar and the presence of yeast odor enhances this response by acting through OR35a-expressing OSNs (Oh et al, 2021 ). Robust feeding responses also require mechanosensory input from the leg, which provides information related to the viscosity of the food.…”

“…Robust feeding responses also require mechanosensory input from the leg, which provides information related to the viscosity of the food. Both smell and touch work synergistically to enhance feeding responses elicited by sugar, enabling flexible feeding behavior based on multiple sensory properties of the food (Oh et al, 2021 ).…”

Modulation of taste sensitivity by the olfactory system inDrosophila

“…Nevertheless, our observation that short-term optogenetic activation of ORNs is sufficient to inhibit PER suggests that olfactory input can acutely suppress sweet taste. However, it is also important to note that not all olfactory activity exerts net suppression on taste sensitivity, as specific odors can either enhance or suppress PER and feeding [38][39][40][41] . Thus, complex connections likely exist between olfactory and gustatory circuits that go beyond the scope of what was revealed through our broad manipulations of ORN activity.…”