Date of Award
Doctor of Philosophy (PhD)
Sensory systems receive and process external stimuli to allow an organism to perceive and react to the environment. How is sensory information subsequently represented, transformed, and interpreted in the neural system? In this dissertation, I have investigated this fundamental question using the fruit fly (Drosophila melanogaster) olfactory system.Chemical cues are transduced into neural signals in the insect antenna by the olfactory receptor neurons (ORNs). The ORNs send their axons to the antennal lobe (AL), with each ORN type innervating a specific neuropil (glomerulus), where they synapse onto excitatory and inhibitory projection neurons (ePNs and iPNs). The ePNs project their axons to the 3rd order stages, the calyx (CL) and lateral horn (LH). On the other hand, the iPNs only innervate the LH. In this dissertation, I first examined how well the peripheral neural activities evoked by an odorant could predict the final behavioral output. As the stimulus intensity increases, a fly’s preference for some odorants switch from attraction to aversion. Behavior assay suggested this phenomenon may help the fly evade harmful environment. Our results indicate that at the level of ORNs, increases in stimulus intensity could result in oscillatory extracellular field potentials that arise entirely due to abrupt changes in cell excitability. Notably, combining the activity of a few ORNs was sufficient to predict intensity-dependent preference changes with odor intensity. How is the sensory input organized in the downstream neural circuit, the insect antennal lobe? Odor-evoked signals from sensory neurons (ORNs) triggered neural responses that were patterned over space and time in cholinergic ePNs and GABAergic iPNs within the antennal lobe. The dendritic-axonal (I/O) response mapping was complex and diverse, and the axonal organization was region-specific (mushroom body vs. lateral horn). In the lateral horn, feed-forward excitatory and inhibitory axonal projections matched ‘odor tuning’ in a stereotyped, dorsal-lateral locus, but mismatched in most other locations. In the temporal dimension, ORN, ePN, and iPN odor-evoked responses had similar encoding features, such as information refinement over time and divergent ON and OFF responses. Notably, analogous spatial and temporal coding principles were observed in all flies, and the latter emerged from idiosyncratic neural processing approaches. In sum, these results provide key insights necessary for understanding how sensory information is organized along spatial and temporal dimensions.
Barani B. Raman
Bruce B. Carlson, Dennis D. Barbour, Timothy T. Holy, Yehuda Y. Ben-Shahar,