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Rescheduling Behavioral Subunits of a Fixed Action Pattern by Genetic Manipulation of Peptidergic Signaling.

Kim DH, Han MR, Lee G, Lee SS, Kim YJ, Adams ME - PLoS Genet. (2015)

Bottom Line: Activation of CCAP or CAMB neurons through temperature-sensitive TRPM8 gating is sufficient to trigger ecdysis behavior.Our findings demonstrate that kinin and CAMB neurons are direct targets of ETH and play critical roles in scheduling successive behavioral steps in the ecdysis FAP.Moreover, temporal organization of the FAP is likely a function of ETH receptor density in target neurons.

View Article: PubMed Central - PubMed

Affiliation: Department of Entomology, University of California, Riverside, Riverside, California, United States of America.

ABSTRACT
The ecdysis behavioral sequence in insects is a classic fixed action pattern (FAP) initiated by hormonal signaling. Ecdysis triggering hormones (ETHs) release the FAP through direct actions on the CNS. Here we present evidence implicating two groups of central ETH receptor (ETHR) neurons in scheduling the first two steps of the FAP: kinin (aka drosokinin, leucokinin) neurons regulate pre-ecdysis behavior and CAMB neurons (CCAP, AstCC, MIP, and Bursicon) initiate the switch to ecdysis behavior. Ablation of kinin neurons or altering levels of ETH receptor (ETHR) expression in these neurons modifies timing and intensity of pre-ecdysis behavior. Cell ablation or ETHR knockdown in CAMB neurons delays the switch to ecdysis, whereas overexpression of ETHR or expression of pertussis toxin in these neurons accelerates timing of the switch. Calcium dynamics in kinin neurons are temporally aligned with pre-ecdysis behavior, whereas activity of CAMB neurons coincides with the switch from pre-ecdysis to ecdysis behavior. Activation of CCAP or CAMB neurons through temperature-sensitive TRPM8 gating is sufficient to trigger ecdysis behavior. Our findings demonstrate that kinin and CAMB neurons are direct targets of ETH and play critical roles in scheduling successive behavioral steps in the ecdysis FAP. Moreover, temporal organization of the FAP is likely a function of ETH receptor density in target neurons.

No MeSH data available.


Related in: MedlinePlus

A model depicting functional roles of kinin and CAMB neurons in scheduling of the ecdysis FAP.ETH release from Inka cells activates ETHR neurons (ETHR-A and ETHR-B). ETHR-B neurons are more sensitive to ETH and become active immediately following ETH release. These neurons release signal(s) that engage Gαo signaling in CAMB neurons. ETH activates kinin neurons directly governing pre-ecdysis and CAMB neurons via ETHR-A and Gαq signaling. Initially, pre-ecdysis is induced, whereas CAMB neurons remain silent due to relatively low sensitivity to ETH and Gαo-mediated inhibitory input. Upon reaching adequate ETH levels in the hemolymph, ETH-mediated Gαq signaling overrides Gαo signaling in CAMB neurons, leading to co-release of CCAP, AstCC, MIP, and bursicon. This results in pre-ecdysis inhibition and the switch to ecdysis behavior and post-ecdysis behavior. Additional excitatory inputs from non-CAMB CCAP neurons contribute to vigorous ecdysis swings, resulting in head eversion. The dashed arrow represents hypothetical input to CAMB neurons from as yet unidentified ETHR-B neurons.
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pgen.1005513.g007: A model depicting functional roles of kinin and CAMB neurons in scheduling of the ecdysis FAP.ETH release from Inka cells activates ETHR neurons (ETHR-A and ETHR-B). ETHR-B neurons are more sensitive to ETH and become active immediately following ETH release. These neurons release signal(s) that engage Gαo signaling in CAMB neurons. ETH activates kinin neurons directly governing pre-ecdysis and CAMB neurons via ETHR-A and Gαq signaling. Initially, pre-ecdysis is induced, whereas CAMB neurons remain silent due to relatively low sensitivity to ETH and Gαo-mediated inhibitory input. Upon reaching adequate ETH levels in the hemolymph, ETH-mediated Gαq signaling overrides Gαo signaling in CAMB neurons, leading to co-release of CCAP, AstCC, MIP, and bursicon. This results in pre-ecdysis inhibition and the switch to ecdysis behavior and post-ecdysis behavior. Additional excitatory inputs from non-CAMB CCAP neurons contribute to vigorous ecdysis swings, resulting in head eversion. The dashed arrow represents hypothetical input to CAMB neurons from as yet unidentified ETHR-B neurons.

Mentions: We propose a mechanistic model to explain neural mechanisms underlying the Drosophila pupal ecdysis FAP (Fig 7). Principle players in orchestration of pre-ecdysis and ecdysis behaviors are the kinin and CAMB ETHR ensembles, respectively. As ETH levels rise in the hemolymph, ETHR-B neurons are activated due to their high sensitivity (EC50 ~ 1 nM). These neurons release inhibitory signals acting through Gαi/o to inhibit CAMB neurons. As ETH levels rise further, kinin neurons receive direct excitatory input from ETH signaling via ETHR-A and Gαq to mobilize calcium from intracellular stores, leading to electrical activity in these neurons. ETH acts simultaneously on CAMB neurons, but inhibition from ETHR-B neurons descending from anterior ganglia prevents them from becoming active. As inhibition wanes, CAMB neurons become active, initiating the switch to ecdysis behavior.


Rescheduling Behavioral Subunits of a Fixed Action Pattern by Genetic Manipulation of Peptidergic Signaling.

Kim DH, Han MR, Lee G, Lee SS, Kim YJ, Adams ME - PLoS Genet. (2015)

A model depicting functional roles of kinin and CAMB neurons in scheduling of the ecdysis FAP.ETH release from Inka cells activates ETHR neurons (ETHR-A and ETHR-B). ETHR-B neurons are more sensitive to ETH and become active immediately following ETH release. These neurons release signal(s) that engage Gαo signaling in CAMB neurons. ETH activates kinin neurons directly governing pre-ecdysis and CAMB neurons via ETHR-A and Gαq signaling. Initially, pre-ecdysis is induced, whereas CAMB neurons remain silent due to relatively low sensitivity to ETH and Gαo-mediated inhibitory input. Upon reaching adequate ETH levels in the hemolymph, ETH-mediated Gαq signaling overrides Gαo signaling in CAMB neurons, leading to co-release of CCAP, AstCC, MIP, and bursicon. This results in pre-ecdysis inhibition and the switch to ecdysis behavior and post-ecdysis behavior. Additional excitatory inputs from non-CAMB CCAP neurons contribute to vigorous ecdysis swings, resulting in head eversion. The dashed arrow represents hypothetical input to CAMB neurons from as yet unidentified ETHR-B neurons.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4581697&req=5

pgen.1005513.g007: A model depicting functional roles of kinin and CAMB neurons in scheduling of the ecdysis FAP.ETH release from Inka cells activates ETHR neurons (ETHR-A and ETHR-B). ETHR-B neurons are more sensitive to ETH and become active immediately following ETH release. These neurons release signal(s) that engage Gαo signaling in CAMB neurons. ETH activates kinin neurons directly governing pre-ecdysis and CAMB neurons via ETHR-A and Gαq signaling. Initially, pre-ecdysis is induced, whereas CAMB neurons remain silent due to relatively low sensitivity to ETH and Gαo-mediated inhibitory input. Upon reaching adequate ETH levels in the hemolymph, ETH-mediated Gαq signaling overrides Gαo signaling in CAMB neurons, leading to co-release of CCAP, AstCC, MIP, and bursicon. This results in pre-ecdysis inhibition and the switch to ecdysis behavior and post-ecdysis behavior. Additional excitatory inputs from non-CAMB CCAP neurons contribute to vigorous ecdysis swings, resulting in head eversion. The dashed arrow represents hypothetical input to CAMB neurons from as yet unidentified ETHR-B neurons.
Mentions: We propose a mechanistic model to explain neural mechanisms underlying the Drosophila pupal ecdysis FAP (Fig 7). Principle players in orchestration of pre-ecdysis and ecdysis behaviors are the kinin and CAMB ETHR ensembles, respectively. As ETH levels rise in the hemolymph, ETHR-B neurons are activated due to their high sensitivity (EC50 ~ 1 nM). These neurons release inhibitory signals acting through Gαi/o to inhibit CAMB neurons. As ETH levels rise further, kinin neurons receive direct excitatory input from ETH signaling via ETHR-A and Gαq to mobilize calcium from intracellular stores, leading to electrical activity in these neurons. ETH acts simultaneously on CAMB neurons, but inhibition from ETHR-B neurons descending from anterior ganglia prevents them from becoming active. As inhibition wanes, CAMB neurons become active, initiating the switch to ecdysis behavior.

Bottom Line: Activation of CCAP or CAMB neurons through temperature-sensitive TRPM8 gating is sufficient to trigger ecdysis behavior.Our findings demonstrate that kinin and CAMB neurons are direct targets of ETH and play critical roles in scheduling successive behavioral steps in the ecdysis FAP.Moreover, temporal organization of the FAP is likely a function of ETH receptor density in target neurons.

View Article: PubMed Central - PubMed

Affiliation: Department of Entomology, University of California, Riverside, Riverside, California, United States of America.

ABSTRACT
The ecdysis behavioral sequence in insects is a classic fixed action pattern (FAP) initiated by hormonal signaling. Ecdysis triggering hormones (ETHs) release the FAP through direct actions on the CNS. Here we present evidence implicating two groups of central ETH receptor (ETHR) neurons in scheduling the first two steps of the FAP: kinin (aka drosokinin, leucokinin) neurons regulate pre-ecdysis behavior and CAMB neurons (CCAP, AstCC, MIP, and Bursicon) initiate the switch to ecdysis behavior. Ablation of kinin neurons or altering levels of ETH receptor (ETHR) expression in these neurons modifies timing and intensity of pre-ecdysis behavior. Cell ablation or ETHR knockdown in CAMB neurons delays the switch to ecdysis, whereas overexpression of ETHR or expression of pertussis toxin in these neurons accelerates timing of the switch. Calcium dynamics in kinin neurons are temporally aligned with pre-ecdysis behavior, whereas activity of CAMB neurons coincides with the switch from pre-ecdysis to ecdysis behavior. Activation of CCAP or CAMB neurons through temperature-sensitive TRPM8 gating is sufficient to trigger ecdysis behavior. Our findings demonstrate that kinin and CAMB neurons are direct targets of ETH and play critical roles in scheduling successive behavioral steps in the ecdysis FAP. Moreover, temporal organization of the FAP is likely a function of ETH receptor density in target neurons.

No MeSH data available.


Related in: MedlinePlus