In an environment cluttered with competing information, animals are faced with the challenge of detecting stimuli critical for their survival and reproductive success. Neural mechanisms such as center-surround, orientation selectivity and color opponency promote feature extraction in the early visual system. Less is understood, however, about how perceptual saliency is achieved in the olfactory system. We hypothesize that gain control by synaptic modulation is an important mechanism to prune irrelevant olfactory information and accentuate neural response to behaviorally relevant cues in the environment. Olfactory systems exhibit similar design principles across many species in the animal kingdom, including insects and mammals. Insect odorant receptor neurons (ORNs) relay odor information to glomeruli in the antennal lobe (AL), a structure that resembles the vertebrate olfactory bulb. Excitatory and inhibitory local interneurons (LNs) in the antennal lobe play an important role in controlling antennal lobe output. Axons of second order projection neurons (PNs) innervate two higher brain centers - the mushroom body (MB) and the lateral horn (LH). The anatomical simplicity and the power of genetics make Drosophila a particularly amenable system to study the neural circuit for feature extraction in the olfactory system. Experiments in Aims 1 are designed to probe the modulatory mechanism of dopamine in a context-dependent olfactory behavior.
In Aims 2 and 3, we will test the hypothesis that serotonin, a neuromodulator associated with arousal and wakefulness, promotes contrast enhancement and functions to enhance feature in a noisy odor environment. Behavioral experiments are aimed to test the role of serotonin in this context (Specific Aim 2). Physiological experiments are designed to better understand the antennal lobe circuitry mediating serotonin's effects on odor representation (Specific Aim 3). Neuromodulators play key roles in flexibly altering synaptic processing in local circuits in response to both internal and external cues. The proposed projects address the role of serotonin and dopamine in a fundamental problem in olfactory processing: how does olfactory context influence the saliency of certain olfactory features? Understanding basic principles about how neuromodulators exert their actions on simple olfactory circuits will provide insight into understanding how different therapeutic agents targeting serotonin or dopamine signaling shape information processing in neural systems.

Public Health Relevance

The proposed projects address the role of serotonin and dopamine in a fundamental problem in sensory processing: how does olfactory context influence the saliency of certain olfactory features? Understanding basic principles about how neuromodulators exert their actions on simple olfactory circuits will provide insight into understanding how different therapeutic agents targeting serotonin or dopamine signaling shape information processing in neural systems.

Agency
National Institute of Health (NIH)
Institute
National Institute on Deafness and Other Communication Disorders (NIDCD)
Type
Research Project (R01)
Project #
2R01DC009597-06
Application #
8506624
Study Section
Molecular Neurogenetics Study Section (MNG)
Program Officer
Sullivan, Susan L
Project Start
2008-06-20
Project End
2018-05-31
Budget Start
2013-06-01
Budget End
2014-05-31
Support Year
6
Fiscal Year
2013
Total Cost
$320,212
Indirect Cost
$107,712
Name
University of California San Diego
Department
Biology
Type
Schools of Arts and Sciences
DUNS #
804355790
City
La Jolla
State
CA
Country
United States
Zip Code
92093
Su, Chih-Ying; Wang, Jing W (2014) Modulation of neural circuits: how stimulus context shapes innate behavior in Drosophila. Curr Opin Neurobiol 29:9-16
Wang, Jing W (2012) Presynaptic modulation of early olfactory processing in Drosophila. Dev Neurobiol 72:87-99
Masuyama, Kaoru; Zhang, Yi; Rao, Yi et al. (2012) Mapping neural circuits with activity-dependent nuclear import of a transcription factor. J Neurogenet 26:89-102
Hoover, Erich E; Field, Jeffrey J; Winters, David G et al. (2012) Eliminating the scattering ambiguity in multifocal, multimodal, multiphoton imaging systems. J Biophotonics 5:425-36
Root, Cory M; Ko, Kang I; Jafari, Amir et al. (2011) Presynaptic facilitation by neuropeptide signaling mediates odor-driven food search. Cell 145:133-44
Kim, Susy M; Wang, Jing W (2009) Lateral inhibition and concentration-invariant odor perception. J Biol 8:4
Ignell, Rickard; Root, Cory M; Birse, Ryan T et al. (2009) Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila. Proc Natl Acad Sci U S A 106:13070-5
Dacks, Andrew M; Green, David S; Root, Cory M et al. (2009) Serotonin modulates olfactory processing in the antennal lobe of Drosophila. J Neurogenet 23:366-77
Dacks, Andrew; Green, David; Root, Cory et al. (2009) Serotonin Modulates Olfactory Processing in the Antennal Lobe of Drosophila. J Neurogenet :1-13
Semmelhack, Julia L; Wang, Jing W (2009) Select Drosophila glomeruli mediate innate olfactory attraction and aversion. Nature 459:218-23

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