Neuromodulation of Olfactory Sensitivity in the Peripheral Olfactory Organs of the American Cockroach, Periplaneta americana

Abstract

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.

Leucokinin mimetic elicits aversive behavior in mosquito Aedes aegypti (L.) and inhibits the sugar taste neuron

“…This finding suggests that kinin analogs interact with G protein-coupled receptors expressed within gustatory sensilla similar to the way that peripheral olfactory neurons are modulated by tachykinin (16,17) and neuropeptide F (18)(19)(20). These peptides bind to GPCRs in olfactory receptor neurons (ORNs) or in circuits that modulate chemosensory signal-dependent feeding behaviors and food search (21).…”

Peptidomics of Neuropeptidergic Tissues of the Tsetse FlyGlossina morsitans morsitans

“…Besides their myotropic activity, they also regulate aggression [114,115], act as modulators of olfactory perception and locomotion [116,117], and inhibit insulin signaling in the brain [118]. Tachykinins are expressed in the CNS and endocrine cells of the midgut [114,119,120].…”

Transcriptomics supports local sensory regulation in the antenna of the kissing bugRhodnius prolixus

“…The presence of neurosecretory cells in insect antennae has only been previuosly described for mosquitoes 34 , but no other study has reported neuropeptide synthesis in these organs. The existence of similar cells could be the basis for the detection of a broad set of neuropeptide transcripts in the antennae of kissing-bugs (a total of 36 neuropeptides seems to be expressed) and other insects 23,35,36 . The expression of neuropeptide processing enzyme genes in the antennae was also detected.…”

“…In fact, variations in gene expression depending on nutritional status or development have been described for olfactory correceptors in the antennae of R. prolixus 10 . Nevertheless, information about elements regulating sensory gene transcription and the abundance of the corresponding proteins in insect peripheral organs is very limited [22][23][24][25] . Physiological mechanisms modulating peripheral responses to sensory stimuli involve signaling controlled by biogenic amines, hormones, and neuropeptides, as well as their target Gprotein coupled receptors (GPCRs) and nuclear receptors, overall controlling the functional status of sensory processes 16 .…”