Neuromodulation of olfactory sensitivity in the peripheral olfactory organs of the American cockroach, Periplaneta americana
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 circu...
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Published in | PloS one Vol. 8; no. 11; p. e81361 |
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Main Authors | , , , , , |
Format | Journal Article |
Language | English |
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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. |
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AbstractList | 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. 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. |
Audience | Academic |
Author | Kwon, Hyung Wook Page, Terry L Kim, Jin-Hee Ahn, Young-Joon Pfeiffer, Rita Jung, Je Won |
AuthorAffiliation | University of Houston, United States of America 1 WCU Biomodulation Major, Department of Agricultural Biotechnology, College of Agriculture & Life Sciences, Seoul, Republic of Korea 2 Department of Biological Sciences, Vanderbilt University, Nashville, Tennessee, United States of America |
AuthorAffiliation_xml | – name: 2 Department of Biological Sciences, Vanderbilt University, Nashville, Tennessee, United States of America – name: 1 WCU Biomodulation Major, Department of Agricultural Biotechnology, College of Agriculture & Life Sciences, Seoul, Republic of Korea – name: University of Houston, United States of America |
Author_xml | – sequence: 1 givenname: Je Won surname: Jung fullname: Jung, Je Won organization: WCU Biomodulation Major, Department of Agricultural Biotechnology, College of Agriculture & Life Sciences, Seoul, Republic of Korea – sequence: 2 givenname: Jin-Hee surname: Kim fullname: Kim, Jin-Hee – sequence: 3 givenname: Rita surname: Pfeiffer fullname: Pfeiffer, Rita – sequence: 4 givenname: Young-Joon surname: Ahn fullname: Ahn, Young-Joon – sequence: 5 givenname: Terry L surname: Page fullname: Page, Terry L – sequence: 6 givenname: Hyung Wook surname: Kwon fullname: Kwon, Hyung Wook |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Competing Interests: The authors have declared that no competing interests exist. Conceived and designed the experiments: JJ YA TLP HWK. Performed the experiments: JJ JK RP. Analyzed the data: JJ YA TLP HWK. Wrote the manuscript: JJ TLP HWK. |
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Snippet | Olfactory sensitivity exhibits daily fluctuations. Several studies have suggested that the olfactory system in insects is modulated by both biogenic amines and... |
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SubjectTerms | 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 |
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Title | Neuromodulation of olfactory sensitivity in the peripheral olfactory organs of the American cockroach, Periplaneta americana |
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