Journal Article

Stereotyped responses of Drosophila peptidergic neuronal ensemble depend on downstream neuromodulators

Diegelmann, Sören, Ewer, John, Mena, Wilson, Wegener, Christian

2016

Overview

Neuropeptides play a key role in the regulation of behaviors and physiological responses including alertness, social recognition, and hunger, yet, their mechanism of action is poorly understood. Here, we focus on the endocrine control ecdysis behavior, which is used by arthropods to shed their cuticle at the end of every molt. Ecdysis is triggered by ETH (Ecdysis triggering hormone), and we show that the response of peptidergic neurons that produce CCAP (crustacean cardioactive peptide), which are key targets of ETH and control the onset of ecdysis behavior, depends fundamentally on the actions of neuropeptides produced by other direct targets of ETH and released in a broad paracrine manner within the CNS; by autocrine influences from the CCAP neurons themselves; and by inhibitory actions mediated by GABA. Our findings provide insights into how this critical insect behavior is controlled and general principles for understanding how neuropeptides organize neuronal activity and behaviors. Most behaviors occur only under specific circumstances: we eat when we are hungry, for example. But how does the nervous system decide when to start or stop a particular behavior? Molecules called neuropeptides are thought to play a key role in these decisions. Neuropeptides are produced by organs throughout the body and also by the nervous system itself. When neuropeptides act on neurons responsible for a particular behavior – such as feeding – they can inform those neurons about conditions elsewhere in the body and the brain. This enables the nervous system to decide whether to start or stop the behavior. Yet, how the signals from the different neuropeptides are integrated is poorly understood. As immature insects grow, they regularly molt then shed their outer skeleton – or cuticle – in a process called ecdysis. This requires a series of behaviors to occur in a particular order. The old cuticle is first loosened and shed, and then the new cuticle expands and hardens. A number of neuropeptides control ecdysis: for example, a key neuropeptide called ecdysis-triggering hormone (ETH) triggers the process. However, it was not clear how each of the other neuropeptides that are released at this time contributes to the behaviors involved in ecdysis. By studying ecdysis in developing fruit flies, Mena et al. now show that the various ecdysial neuropeptides work together to produce the precise behaviors that are observed. For instance, the effect that ETH has on the nervous system depends on whether another neuropeptide called eclosion hormone is also present. ETH can therefore cause different behavioral outcomes depending on the actions of the other neuropeptides. Further work is needed in order to work out exactly how the nervous system integrates information from different neuropeptides. Do certain neurons respond to specific neuropeptide combinations? It also remains to be seen how different insects are able to use the same neuropeptides to control ecdysis despite their different body shapes.

• Publisher: eLife Science Publications, Ltd,eLife Sciences Publications Ltd,eLife Sciences Publications, Ltd
• Subject: Animals / Autocrine signalling / Behavior / Behavior, Animal - drug effects / Central nervous system / Crustacean cardioactive peptide / Developmental Biology and Stem Cells / Drosophila / Drosophila - physiology / ecdysis / ecdysis triggering hormone / eclosion hormone / Hunger / Insects / molt / Molting / Nervous system / Neural circuitry / neurohormone / Neuromodulation / Neurons - drug effects / Neurons - physiology / Neuropeptides / Neuroscience / Neurosciences / Neurotransmitter Agents - metabolism / Paracrine signalling / Peptides / Physiological aspects / Physiology / Sensors / Social interactions / Software / γ-Aminobutyric acid