The sense of smell is caused by odorants activating olfactory sensory neurons in the nose. A pivotal question in the field is how these neuronal activities give rise to odor perceptions. Since the neuronal architecture of the olfactory system i remarkably similar between insects and mammals, studying how the fly brain processes olfactory information could shed light on principles underlying olfaction in other organisms. We previously demonstrated that the olfactory cortex (lateral horn) is divided into two broad domains, one representing food odors and one representing pheromones. Therefore, this olfactory region, which to the naked eye looks homogenous, might be organized into olfactory processing centers that reflect biologically relevant information. These studies were based on simple classifications of odorants as being food or pheromone, but did not take into account the valence of the odorant - that is if it is behaviorally attractive or repulsive. Preliminary data frm our recent work suggests that aversive odors might represent a new processing center in the olfactory cortex. Using a combination of genetics, behavioral analyses, axon tracing, and brain imaging studies, we will test the hypothesis that (1) the olfactory cortex is organized into domains based on three important aspects of a fly's life: food, pheromones, and avoidance. Results from this work will allow us to link repulsive behaviors to their underlying neuronal components and thus model how newly identified and known aversive signals might be represented in the higher olfactory cortex. To understand how attractive signals such as attractive food odors and attractive pheromones are represented in the olfactory cortex, as well as how the olfactory system utilizes them to communicate relevant information regarding an animal's environment, we investigate a novel pheromone signaling system that we have identified. Our preliminary data suggests that this signaling system in Drosophila represents a behavioral link between food and pheromone signaling. Using a combination of genetics, molecular biology, GC-MS, calcium imaging, and electrophysiological recordings, we will test the hypothesis that (2) Drosophila secrete an attractive pheromone when stimulated by attractive food odors to tag sites for positive social behaviors such as egg laying or courtship. Results from the characterization of this new pheromone signaling mechanism will enrich our understanding of how olfactory communications are used to guide behavioral responses to a changing environment. The proposed studies are significant because we will gain insights into how aversive and attractive olfactory information is represented in higher processing centers of an olfactory system that could serve as a model for how olfactory perceptions are encoded in the brains of other animals.

Public Health Relevance

Millions of people die every year from insect born diseases such as dengue fever and malaria. In addition, billions of dollars worth of agricultural production is lost annually as a direct result of insect pests. Since insects rely heavily on their sense of smell for finding hosts, food sites, and for social interactions, the insect olfactory system represents a good target for pest control.

Agency
National Institute of Health (NIH)
Institute
National Institute on Deafness and Other Communication Disorders (NIDCD)
Type
Research Project (R01)
Project #
4R01DC013079-04
Application #
9011523
Study Section
Somatosensory and Chemosensory Systems Study Section (SCS)
Program Officer
Sullivan, Susan L
Project Start
2013-03-25
Project End
2018-02-28
Budget Start
2016-03-01
Budget End
2017-02-28
Support Year
4
Fiscal Year
2016
Total Cost
Indirect Cost
Name
Johns Hopkins University
Department
Neurosciences
Type
Schools of Medicine
DUNS #
001910777
City
Baltimore
State
MD
Country
United States
Zip Code
21205
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Riabinina, Olena; Task, Darya; Marr, Elizabeth et al. (2016) Organization of olfactory centres in the malaria mosquito Anopheles gambiae. Nat Commun 7:13010
Lin, Chun-Chieh; Riabinina, Olena; Potter, Christopher J (2016) Olfactory Behaviors Assayed by Computer Tracking Of Drosophila in a Four-quadrant Olfactometer. J Vis Exp :
Riabinina, Olena; Potter, Christopher J (2016) The Q-System: A Versatile Expression System for Drosophila. Methods Mol Biol 1478:53-78
Lin, Chun-Chieh; Potter, Christopher J (2016) Editing Transgenic DNA Components by Inducible Gene Replacement in Drosophila melanogaster. Genetics 203:1613-28
Lin, Chun-Chieh; Potter, Christopher J (2016) Non-Mendelian Dominant Maternal Effects Caused by CRISPR/Cas9 Transgenic Components in Drosophila melanogaster. G3 (Bethesda) 6:3685-3691
Diao, Fengqiu; Ironfield, Holly; Luan, Haojiang et al. (2015) Plug-and-play genetic access to drosophila cell types using exchangeable exon cassettes. Cell Rep 10:1410-21
Riabinina, Olena; Luginbuhl, David; Marr, Elizabeth et al. (2015) Improved and expanded Q-system reagents for genetic manipulations. Nat Methods 12:219-22, 5 p following 222
Gao, Xiaojing J; Riabinina, Olena; Li, Jiefu et al. (2015) A transcriptional reporter of intracellular Ca(2+) in Drosophila. Nat Neurosci 18:917-25

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