Dynamic Characterization ofDrosophilaAntennal Olfactory Neurons Indicates Multiple Opponent Signaling Pathways in Odor Discrimination

Abstract

Opponent signaling refers to processes in which antagonistic signals are produced by different, but closely related, stimuli. It allows enhanced discrimination and more accurate behavioral responses. We explored opponent signaling in the Drosophila melanogaster olfactory system by measuring frequency response functions between odorant concentrations and primary olfactory neuron responses. Random fluctuations in concentration of two aliphatic and two aromatic fruit odorants were used to modulate action potentials from basiconic antennal sensilla. We separated action potentials by two-dimensional cluster analysis using amplitude and cross-correlation with a median action-potential template. Frequency response functions were fitted with either bandpass or second-order low-pass functions and then divided into two polarity groups, excitatory and inhibitory, by fitting the frequency response functions. Cluster analysis gave two, three, or four action potential clusters for each sensillum recording. Sensilla were then grouped by the patterns of response polarities of the individual neurons into four sensillum types, one with four neurons and three with two neurons. All four odorant compounds produced a mixture of excitatory, inhibitory, and null responses in different neurons. Statistical analysis of frequency response parameters for individual odorants gave only weak correlation between dynamics and some neuron types, even when comparing the dynamics of excitatory and inhibitory responses to the same odorant. However, response dynamics were significantly different between aliphatic and aromatic compounds, and between the two aliphatic compounds. Each odorant caused opposing excitatory and inhibitory signals to be sent to the antennal lobe along at least two pairs of axonal pathways.

Ultrastructure and distribution of antennal sensilla of the chilli thrips Scirtothrips dorsalis hood (Thysanoptera: Thripidae)

“…An electrophysiological investigation by De Bruyne, Foster, & Carlson () showed that that one of these neurons responds to CO 2 , whereas the other three respond to other olfactory stimuli, such as methyl salicylate, ethyl butyrate, and 2,3‐butanedione. Electrophysiological evidence for the single‐walled MP sensilla of many insect species, including moths, honey bees, mosquitoes, and flies, revealed that different ORNs respond to different odors and have different response properties, such as signaling modes and response dynamics (Bogner, ; French, Torkkeli & Schuckel, ; Hallem, Dahanukar & Carlson, ; Leal, ; Stange & Stowe, ). Research on odor molecule binding proteins and chemosensory proteins on the SB of F. occidentalis also revealed their olfactory functions (Zhang & Lei, ).…”

Weaker Ligands Can Dominate an Odor Blend due to Syntopic Interactions

“…Nevertheless, this does not exclude that under other conditions, either for different odors or other receptor cells, additional mechanisms of mixture interactions may occur. Such mechanisms could include multiple binding sites on 1 receptor, multiple second-messenger cascades, multiple receptors on 1 cell (e.g., the receptor cell studied here also expresses receptor dOr22b in addition to dOr22a although no active role for dOr22b has been shown yet), or interactions between neurons within 1 sensillum (e.g., ephaptic effects; Boekhoff et al 1994; Cromarty and Derby 1997; Dobritsa et al 2003; Vermeulen and Rospars 2004; French et al 2011; Su et al 2012). Some receptor cells show inhibitory responses to some odorants (antagonistic ligands), in which cases mixture interactions need to be analyzed and modeled differently (Boekhoff et al 1994; Kang and Caprio 1997; de Bruyne et al 1999, 2001; Duchamp-Viret et al 2003; Schuckel et al 2009; Turner and Ray 2009).…”

Complementary Function and Integrated Wiring of the Evolutionarily DistinctDrosophilaOlfactory Subsystems

“…4)]. Such an "opponent signaling" strategy may also enhance odor discrimination (French et al, 2011).…”