Neuromodulation of olfactory sensitivity in the peripheral olfactory organs of the American cockroach, Periplaneta americana

• Published in: PloS one Vol. 8; no. 11; p. e81361
• Main Authors: Jung, Je Won, Kim, Jin-Hee, Pfeiffer, Rita, Ahn, Young-Joon, Page, Terry L, Kwon, Hyung Wook
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 14.11.2013; Public Library of Science (PLoS)
• Subjects: Agricultural biotechnology; Agriculture; Ambystoma mexicanum; Amines; Animals; Antennae; Apis mellifera; Biogenic amines; Blattaria; Brain; Cloning; Cockroaches; Drosophila; Drosophila melanogaster; Genomes; Hybridization; Insects; Life sciences; Nerves; Neuromodulation; Neurons; Neuropeptides; Octopamine; Octopamine - metabolism; Octopamine receptors; Odorant receptors; Olfactory organs; Olfactory pathways; Olfactory receptor neurons; Olfactory Receptor Neurons - metabolism; Olfactory system; Olfactory thresholds; Organs; Peptides; Periplaneta - genetics; Periplaneta - metabolism; Periplaneta americana; Physiology; Receptors; Receptors, Tachykinin - metabolism; Regulators; Sensitivity; Signaling; Structure-function relationships; Tachykinin; Tachykinin receptors; Tachykinins - metabolism; Tribolium castaneum; South Korea; United States > US; Madeira; Tennessee; Nashville Tennessee
• DOI: 10.1371/journal.pone.0081361
• ISSN: 1932-6203

Olfactory sensitivity exhibits daily fluctuations. Several studies have suggested that the olfactory system in insects is modulated by both biogenic amines and neuropeptides. However, molecular and neural mechanisms underlying olfactory modulation in the periphery remain unclear since neuronal circuits regulating olfactory sensitivity have not been identified. Here, we investigated the structure and function of these signaling pathways in the peripheral olfactory system of the American cockroach, Periplaneta americana, utilizing in situ hybridization, qRT-PCR, and electrophysiological approaches. We showed that tachykinin was co-localized with the octopamine receptor in antennal neurons located near the antennal nerves. In addition, the tachykinin receptor was found to be expressed in most of the olfactory receptor neurons in antennae. Functionally, the effects of direct injection of tachykinin peptides, dsRNAs of tachykinin, tachykinin receptors, and octopamine receptors provided further support for the view that both octopamine and tachykinin modulate olfactory sensitivity. Taken together, these findings demonstrated that octopamine and tachykinin in antennal neurons are olfactory regulators in the periphery. We propose here the hypothesis that octopamine released from neurons in the brain regulates the release of tachykinin from the octopamine receptor neurons in antennae, which in turn modulates the olfactory sensitivity of olfactory receptor neurons, which house tachykinin receptors.