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The Journal of Neuroscience, March 18, 2009, 29(11):3343-3353; doi:10.1523/JNEUROSCI.4241-08.2009

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Behavioral/Systems/Cognitive
Characterization of the Decision Network for Wing Expansion in Drosophila Using Targeted Expression of the TRPM8 Channel

Nathan C. Peabody, Jascha B. Pohl, Fengqiu Diao, Andrew P. Vreede, David J. Sandstrom, Howard Wang, Paul K. Zelensky, and Benjamin H. White

Laboratory of Molecular Biology, National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland 20892

Correspondence should be addressed to Benjamin H. White, National Institute of Mental Health, National Institutes of Health, 9000 Rockville Pike, Bethesda, MD 20892. Email: benjaminwhite{at}mail.nih.gov

After emergence, adult flies and other insects select a suitable perch and expand their wings. Wing expansion is governed by the hormone bursicon and can be delayed under adverse environmental conditions. How environmental factors delay bursicon release and alter perch selection and expansion behaviors has not been investigated in detail. Here we provide evidence that in Drosophila the motor programs underlying perch selection and wing expansion have different environmental dependencies. Using physical manipulations, we demonstrate that the decision to perch is based primarily on environmental valuations and is incrementally delayed under conditions of increasing perturbation and confinement. In contrast, the all-or-none motor patterns underlying wing expansion are relatively invariant in length regardless of environmental conditions. Using a novel technique for targeted activation of neurons, we show that the highly stereotyped wing expansion motor patterns can be initiated by stimulation of N_CCAP, a small network of central neurons that regulates the release of bursicon. Activation of this network using the cold-sensitive rat TRPM8 channel is sufficient to trigger all essential behavioral and somatic processes required for wing expansion. The delay of wing expansion under adverse circumstances thus couples an environmentally sensitive decision network to a command-like network that initiates a fixed action pattern. Because N_CCAP mediates environmentally insensitive ecdysis-related behaviors in Drosophila development before adult emergence, the study of wing expansion promises insights not only into how networks mediate behavioral choices, but also into how decision networks develop.

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Received Sept. 5, 2008; revised Jan. 9, 2009; accepted Feb. 3, 2009.

Correspondence should be addressed to Benjamin H. White, National Institute of Mental Health, National Institutes of Health, 9000 Rockville Pike, Bethesda, MD 20892. Email: benjaminwhite{at}mail.nih.gov

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