Contrast enhancement mediated by lateral inhibition within the nervous system enhances detection of salient features of visual and auditory stimuli, such as spatial and temporal edges. However, it remains unclear how mechanisms for temporal contrast enhancement in the olfactory system can enhance detection of odor plume edges during navigation. To address this question we delivered to Drosophila melanogaster flies pulses of high odor intensity that induce sustained peripheral responses in olfactory sensory neurons (OSNs). We use optical electrophysiology to directly measure electrical responses in presynaptic terminals and demonstrate that sustained peripheral responses are temporally sharpened by the combined activity of two types of inhibitory GABA receptors to generate contrast-enhanced voltage responses in central OSN axon terminals. Furthermore, we show how these GABA receptors modulate the time-course of innate behavioral responses after odor pulse termination demonstrating an important role for temporal contrast enhancement in odor-guided navigation.
Significance Statement: Contrast enhancement of visual, auditory and olfactory information shapes the spatial and temporal perception of our environment. The cellular mechanisms that mediate temporal contrast enhancement of olfactory information and their impact on behavior are not fully understood. We therefore use optical electrophysiology to investigate how presynaptic GABA receptors in olfactory sensory neurons of Drosophila melanogaster shape olfactory information and how this affects odor-driven behavioral kinetics. We find that the combined activity of two types of inhibitory GABA receptors mediates temporal contrast enhancement and modulate behavioral kinetics after an odor pulse demonstrating the importance of this mechanism for odor-guided navigation.
Authors report no conflict of interest.
Work in the laboratory of M.N.N. was supported in part by the National Institute of Neurological Disorders and Stroke, National Institutes of Health (NIH) (R01NS055035, R01NS056443, R01NS091070), National Institute of General Medical Sciences, NIH (R01GM098931), and the Kavli Institute for Neuroscience. L.Y.M was supported by a Gruber Science Fellowship and NIGMS, NIH (T32GM007223).