Olfactory and neuromodulatory signals reverse visual object avoidance to approach in Drosophila

Abstract

Innate behavioral reactions to sensory stimuli may be subject to modulation by contextual conditions including signals from other modalities. Whereas sensory processing by individual modalities has been well-studied, the cell circuit mechanisms by which signals from different sensory systems are integrated to control behavior remains poorly understood. Here, we provide a new behavioral model to study the mechanisms of multisensory integration. This behavior, which we termed odor-induced visual valence reversal, occurs when the innate avoidance response to a small moving object by flying Drosophila melanogaster is reversed by the presence of an appetitive odor. Instead of steering away from the small object representing an approaching threat, flies begin to steer towards the object in the presence of odor. Odor-induced visual valence reversal occurs rapidly without associative learning and occurs for attractive odors including apple cider vinegar and ethanol, but not for innately aversive benzaldehyde. Optogenetic activation of octopaminergic neurons robustly induces visual valence reversal in the absence of odor, as does optogenetic activation of directional columnar motion detecting neurons that express octopamine receptors. Optogenetic activation of octopamine neurons drives calcium responses in the motion detectors. Taken together, our results implicate a multisensory processing cascade in which appetitive odor activates octopaminergic neuromodulation of visual pathways, which leads to increased visual saliency and the switch from avoidance to approach toward a small visual object.

Visual-Olfactory Integration in the Human Disease Vector Mosquito Aedes aegypti

“…This modulation is consistent with, yet more subtle than, their free flight behaviour. It is worth noting that the difference between free flight [3] and tethered behaviour is also less pronounced in Drosophila [36]. Although the behavioural modulation we observed was subtle, quantifying the modulation allowed us to design a tethered preparation in which we could use calcium imaging to observe the neural basis for the behavioural modulation.…”

Serotonergic modulation of visual neurons in Drosophila melanogaster

“…Additional studies have shown that aminergic neurotransmitters can modulate visual information processing in flies and other insects [ 26 , 41 – 46 ]. Octopamine, the invertebrate equivalent of noradrenaline, is present in processes innervating the medulla, lobula and lobula plate in Drosophila , where it regulates state-dependent modulation of visual interneurons [ 42 , 46 ] including the saliency of objects during flight [ 43 ]. Serotonergic neurons also innervate the optic ganglia [ 47 – 52 ] and previous studies indicate that serotonin impacts cellular activity and visual behaviors in insects [ 44 , 45 , 53 – 56 ].…”

Drosophila Neuroscience: Should I Land or Should I Jump?

“…In order to maximize uptake of nutrients the gut expands its absorptive area by forming finger-like protrusions (villi) connected to small invaginations into the connective tissue (crypts) ( Figure 1A). In this way, the human gut generates a surface area covering more than 30 m 2 [1]. This, however, creates fragile structures that are exposed to mechanical, chemical and biological stress and are prone to rapidly disintegrate, causing substantial threats such as systemic infections or inflammatory bowel diseases.…”

“…An approaching predator, for example, can elicit a similar rapidly expanding looming pattern on the observer's retina as an approaching conspecific. In insects, it has been shown that the decision to avoid or approach an ambiguous object can depend on context-sensitive inputs such as food odor [1], which can be confounded by visual circuits that only function properly during locomotion [2]. Thus, reactions to a single sensory stimulus are unlikely to be hard-wired.…”