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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

Activation of CCAP and CAMB neurons initiates ecdysis behavior.(A) Held at a constant 24°C, the natural ecdysis FAP observed in puparium-free control (w1118) and two test groups (CCAP-Gal4>UAS-TRPM8, Pburs-Gal4>UAS-TRPM8) shows normal scheduling of behavioral steps. (B) Induction of ecdysis behavior within minutes upon reducing temperature from 24°C to 18°C in CCAP (CCAP>TRPM8) and CAMB (Pburs>TRPM8) flies. Upon returning to 24°C, the natural ecdysis FAP ensues with occasional bouts of ecdysis behavior (red strips in the pre-ecdysis bar) occurring during pre-ecdysis. Head eversion is delayed and highly variable in CAMB-activated flies, whereas it occurs within a few minutes of ecdysis behavior onset in CCAP-activated flies. (C) Ecdysis swing frequency during natural behavior or temperature-induced behavior. At 18°C, CAMB flies show ecdysis contraction frequency significantly low than control, whereas CCAP-induced behavior is similar to the natural ecdysis swing frequency. Overall, ecdysis swing frequency is decreased significantly at 18°C relative to 24°C.
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pgen.1005513.g006: Activation of CCAP and CAMB neurons initiates ecdysis behavior.(A) Held at a constant 24°C, the natural ecdysis FAP observed in puparium-free control (w1118) and two test groups (CCAP-Gal4>UAS-TRPM8, Pburs-Gal4>UAS-TRPM8) shows normal scheduling of behavioral steps. (B) Induction of ecdysis behavior within minutes upon reducing temperature from 24°C to 18°C in CCAP (CCAP>TRPM8) and CAMB (Pburs>TRPM8) flies. Upon returning to 24°C, the natural ecdysis FAP ensues with occasional bouts of ecdysis behavior (red strips in the pre-ecdysis bar) occurring during pre-ecdysis. Head eversion is delayed and highly variable in CAMB-activated flies, whereas it occurs within a few minutes of ecdysis behavior onset in CCAP-activated flies. (C) Ecdysis swing frequency during natural behavior or temperature-induced behavior. At 18°C, CAMB flies show ecdysis contraction frequency significantly low than control, whereas CCAP-induced behavior is similar to the natural ecdysis swing frequency. Overall, ecdysis swing frequency is decreased significantly at 18°C relative to 24°C.

Mentions: Control flies show no differences in scheduling of the pupal ecdysis behavioral sequence when temperature is lowered from 24°C to 18°C. However flies expressing TRPM8 in either the entire CCAP ensemble (CCAP>TRPM8) or in the CAMB neuron subset (CAMB>TRPM8) initiated ecdysis behavior upon lowering ambient temperature to 18°C (Fig 6B). No pre-ecdysis behavior was observed in either case. In CCAP>TRPM8 flies, we observed robust ecdysis swinging frequency (1.4 ± 0.1 swings/min), with head eversion occurring within ~6 min (5.8 ± 2.9) of behavior initiation, compared to corresponding events in control flies (1.4 ± 0.03 swings/min; head eversion at 2.8 ± 1.8 min) at the same temperature (18°C; Fig 4B and 4C and S2 Movie). After a 10 min observation period at 18°C, the temperature was returned to 24°C. Ecdysis contractions continue for 1–3 min, whereupon the natural ecdysis FAP invariably ensues in its entirety, starting with pre-ecdysis contractions (Fig 6B). Intermittent ecdysis contractions occur for several minutes following initiation of pre-ecdysis behavior. The second bout of ecdysis behavior was somewhat abbreviated (2.9 ± 1.6 min) compared to controls (4.4 ± 0.6 min).


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)

Activation of CCAP and CAMB neurons initiates ecdysis behavior.(A) Held at a constant 24°C, the natural ecdysis FAP observed in puparium-free control (w1118) and two test groups (CCAP-Gal4>UAS-TRPM8, Pburs-Gal4>UAS-TRPM8) shows normal scheduling of behavioral steps. (B) Induction of ecdysis behavior within minutes upon reducing temperature from 24°C to 18°C in CCAP (CCAP>TRPM8) and CAMB (Pburs>TRPM8) flies. Upon returning to 24°C, the natural ecdysis FAP ensues with occasional bouts of ecdysis behavior (red strips in the pre-ecdysis bar) occurring during pre-ecdysis. Head eversion is delayed and highly variable in CAMB-activated flies, whereas it occurs within a few minutes of ecdysis behavior onset in CCAP-activated flies. (C) Ecdysis swing frequency during natural behavior or temperature-induced behavior. At 18°C, CAMB flies show ecdysis contraction frequency significantly low than control, whereas CCAP-induced behavior is similar to the natural ecdysis swing frequency. Overall, ecdysis swing frequency is decreased significantly at 18°C relative to 24°C.
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pgen.1005513.g006: Activation of CCAP and CAMB neurons initiates ecdysis behavior.(A) Held at a constant 24°C, the natural ecdysis FAP observed in puparium-free control (w1118) and two test groups (CCAP-Gal4>UAS-TRPM8, Pburs-Gal4>UAS-TRPM8) shows normal scheduling of behavioral steps. (B) Induction of ecdysis behavior within minutes upon reducing temperature from 24°C to 18°C in CCAP (CCAP>TRPM8) and CAMB (Pburs>TRPM8) flies. Upon returning to 24°C, the natural ecdysis FAP ensues with occasional bouts of ecdysis behavior (red strips in the pre-ecdysis bar) occurring during pre-ecdysis. Head eversion is delayed and highly variable in CAMB-activated flies, whereas it occurs within a few minutes of ecdysis behavior onset in CCAP-activated flies. (C) Ecdysis swing frequency during natural behavior or temperature-induced behavior. At 18°C, CAMB flies show ecdysis contraction frequency significantly low than control, whereas CCAP-induced behavior is similar to the natural ecdysis swing frequency. Overall, ecdysis swing frequency is decreased significantly at 18°C relative to 24°C.
Mentions: Control flies show no differences in scheduling of the pupal ecdysis behavioral sequence when temperature is lowered from 24°C to 18°C. However flies expressing TRPM8 in either the entire CCAP ensemble (CCAP>TRPM8) or in the CAMB neuron subset (CAMB>TRPM8) initiated ecdysis behavior upon lowering ambient temperature to 18°C (Fig 6B). No pre-ecdysis behavior was observed in either case. In CCAP>TRPM8 flies, we observed robust ecdysis swinging frequency (1.4 ± 0.1 swings/min), with head eversion occurring within ~6 min (5.8 ± 2.9) of behavior initiation, compared to corresponding events in control flies (1.4 ± 0.03 swings/min; head eversion at 2.8 ± 1.8 min) at the same temperature (18°C; Fig 4B and 4C and S2 Movie). After a 10 min observation period at 18°C, the temperature was returned to 24°C. Ecdysis contractions continue for 1–3 min, whereupon the natural ecdysis FAP invariably ensues in its entirety, starting with pre-ecdysis contractions (Fig 6B). Intermittent ecdysis contractions occur for several minutes following initiation of pre-ecdysis behavior. The second bout of ecdysis behavior was somewhat abbreviated (2.9 ± 1.6 min) compared to controls (4.4 ± 0.6 min).

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