Disruption of a Behavioral Sequence by Targeted Death of Peptidergic Neurons in Drosophila

McNabb, Susan L.; Baker, James D.; Agapite, Julie; Steller, Hermann; Riddiford, Lynn M.; Truman, James W.

doi:10.1016/s0896-6273(00)80963-0

Cited by 197 publications

(189 citation statements)

References 46 publications

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“…These findings help to explain several observations that flies lacking VM cells can perform ecdysis (27,28). Furthermore, ETH induces ecdysis behavior in the debrained CNS of M. sexta or isolated abdomens of B. mori (7,11).…”

Section: Vm Neurons (Eh)supporting

confidence: 68%

Central peptidergic ensembles associated with organization of an innate behavior

Kim

Žitňan

Cho³

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

168

158

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At the end of each developmental stage, insects perform the ecdysis sequence, an innate behavior necessary for shedding the old cuticle. Ecdysis triggering hormones (ETHs) initiate these behaviors through direct actions on the CNS. Here, we identify the ETH receptor (ETHR) gene in the moth Manduca sexta, which encodes two subtypes of GPCR (ETHR-A and ETHR-B). Expression of ETHRs in the CNS coincides precisely with acquisition of CNS sensitivity to ETHs and behavioral competence. ETHR-A occurs in diverse networks of neurons, producing both excitatory and inhibitory neuropeptides, which appear to be downstream signals for behavior regulation. These peptides include allatostatins, crustacean cardioactive peptide (CCAP), calcitonin-like diuretic hormone, CRF-like diuretic hormones (DHs) 41 and 30, eclosion hormone, kinins, myoinhibitory peptides (MIPs), neuropeptide F, and short neuropeptide F. In particular, cells L 3,4 in abdominal ganglia coexpress kinins, DH41, and DH30, which together elicit the fictive preecdysis rhythm. Neurons IN704 in abdominal ganglia coexpress CCAP and MIPs, whose joint actions initiate the ecdysis motor program. ETHR-A also is expressed in brain ventromedial cells, whose release of EH increases excitability in CCAP͞MIP neurons. These findings provide insights into how innate, centrally patterned behaviors can be orchestrated via recruitment of peptide cotransmitter neurons.ecdysis sequence ͉ ecdysis triggering hormone ͉ G protein-coupled receptors ͉ neuropeptide ͉ steroid I nnate behaviors are highly stereotypic and fully functional in the absence of prior experience. Examples include nurturing, nest building, courtship, and escape behaviors as well as certain developmental behaviors such as the ecdysis sequence, necessary for the shedding of old cuticle at the end of each developmental stage in insects. Because the ecdysis sequence is hormonally controlled, it provides unique opportunities to define mechanisms by which chemical messengers assemble and regulate the performance of behaviors (for review, see ref. 1).The ecdysis sequence is initiated through direct actions of bloodborne pre-ecdysis triggering hormone (PETH) and ecdysis triggering hormone (ETH) on the CNS (2, 3). These peptides are released from endocrine Inka cells, which are present throughout the Insecta (4-6). In larval Manduca sexta, the sequence consists of three behavioral phases (3). In the first phase, PETH activates preecdysis I behavior; subsequently, ETH activates preecdysis II and ecdysis behaviors. These behaviors can be elicited by ETH from the isolated CNS in vitro and, hence, are centrally patterned (3, 7).The ecdysis behavioral sequence is repeatedly acquired and lost throughout the life history of insects (3,8). The signaling pathways triggered by PETH and ETH are assembled at the end of each developmental stage through steroid-induced gene expression, which is critical for synthesis of PETH and ETH in Inka cells and sensitivity of the CNS to these peptides. Once ecdysis is performed, CNS sensitivity to ET...

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Section: Vm Neurons (Eh)supporting

confidence: 68%

Central peptidergic ensembles associated with organization of an innate behavior

Kim

Žitňan

Cho³

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

168

158

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“…In Drosophila, CCAP release occurs after EH release at larval ecdysis (A. C. Clark, M. del Campo, and J. Ewer, unpublished data), suggesting that the same relationship may exist in the fly. Importantly, EH KO and CCAP KO animals both show an altered response to the light-on signal (McNabb et al, 1997) (this paper), and recent evidence suggests that light can cause a premature release of EH (S. McNabb and J. W. Truman, personal communication). Thus, it is possible that certain CCAP neurons mediate the light-on response that is channeled through the EH neurons.…”

Section: Role Of Ccap In the Circadian Timing Of Adult Eclosionmentioning

confidence: 56%

“…EH is also believed to act upstream of CCAP (reviewed by Ewer and Reynolds, 2002). However, the exact role of EH in the control of ecdysis is currently unclear, as EH KO animals are usually able to ecdyse, although their behavior is somewhat disorganized (McNabb et al, 1997). An examination of the ecdysis of animals lacking both EH and CCAP neurons compared with that of CCAP KO and EH KO animals will reveal the extent to which EH can compensate for the lack of CCAP, and vice versa.…”

Section: Discussionmentioning

confidence: 99%

“…A similar approach has been successfully used to study the function of other Drosophila neuropeptides and hormones (e.g. McNabb et al, 1997;Renn et al, 1999;Rulifson et al, 2002).…”

Section: Targeted Ablation Of Ccap Neuronsmentioning

confidence: 99%

“…For instance, adult ecdysis still occurs in Drosophila lacking EH neurons (McNabb et al, 1997). Likewise, although the genetic deletion of the gene encoding ETH causes most animals to die at the first larval ecdysis, many of these animals still display ecdysis-like behavior at the end of this molt (Park et al, 2002a).…”

Section: Introductionmentioning

confidence: 99%

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Targeted ablation of CCAP neuropeptide-containing neurons ofDrosophilacauses specific defects in execution and circadian timing of ecdysis behavior

et al. 2003

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Insect growth and metamorphosis is punctuated by molts, during which a new cuticle is produced. Every molt culminates in ecdysis, the shedding of the remains of the old cuticle. Both the timing of ecdysis relative to the molt and the actual execution of this vital insect behavior are under peptidergic neuronal control. Based on studies in the moth, Manduca sexta, it has been postulated that the neuropeptide Crustacean cardioactive peptide (CCAP)plays a key role in the initiation of the ecdysis motor program. We have used Drosophila bearing targeted ablations of CCAP neurons (CCAP KO animals) to investigate the role of CCAP in the execution and circadian regulation of ecdysis. CCAP KO animals showed specific defects at ecdysis, yet the severity and nature of the defects varied at different developmental stages. The majority of CCAP KO animals died at the pupal stage from the failure of pupal ecdysis, whereas larval ecdysis and adult eclosion behaviors showed only subtle defects. Interestingly, the most severe failure seen at eclosion appeared to be in a function required for abdominal inflation, which could be cardioactive in nature. Although CCAP KO populations exhibited circadian eclosion rhythms, the daily distribution of eclosion events (i.e.,gating) was abnormal. Effects on the execution of ecdysis and its circadian regulation indicate that CCAP is a key regulator of the behavior. Nevertheless, an unexpected finding of this work is that the primary functions of CCAP as well as its importance in the control of ecdysis behaviors may change during the postembryonic development of Drosophila.

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Genetic analysis of theDrosophila ellipsoid body neuropil: Organization and development of the central complex

et al. 1999

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The central complex is an important center for higher-order brain function in insects. It is an intricate neuropil composed of four substructures. Each substructure contains repeated neuronal elements which are connected by processes such that topography is maintained. Although the neuronal architecture has been described in several insects and the behavioral role investigated in various experiments, the exact function of this neuropil has proven elusive. To describe the architecture of the central complex, we study 15 enhancer-trap lines that label various ellipsoid body neuron types. We find evidence for restriction of gene expression that is correlated with specific neuronal types: such correlations suggest functional classifications as well. We show that some enhancer-trap patterns reveal a single ellipsoid body neuron type, while others label multiple types. We describe the development of the ellipsoid body neuropil in wild-type animals and propose developmental mechanisms based on animals displaying structural mutations of this neuropil. The experiments performed here demonstrate the degree of resolution possible from the analysis of enhancer-trap lines and form a useful library of tools for future structure/function studies of the ellipsoid body.

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Disruption of a Behavioral Sequence by Targeted Death of Peptidergic Neurons in Drosophila

Cited by 197 publications

References 46 publications

Central peptidergic ensembles associated with organization of an innate behavior

Central peptidergic ensembles associated with organization of an innate behavior

Targeted ablation of CCAP neuropeptide-containing neurons ofDrosophilacauses specific defects in execution and circadian timing of ecdysis behavior

Genetic analysis of theDrosophila ellipsoid body neuropil: Organization and development of the central complex

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