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The Journal of Neuroscience, November 14, 2007, 27(46):12611-12622; doi:10.1523/JNEUROSCI.2179-07.2007

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Development/Plasticity/Repair
Temperature-Dependent Developmental Plasticity of Drosophila Neurons: Cell-Autonomous Roles of Membrane Excitability, Ca²⁺ Influx, and cAMP Signaling

I-Feng Peng,^1 * Brett A. Berke,^2 * Yue Zhu,¹ Wei-Hua Lee,¹ Wenjia Chen,¹ and Chun-Fang Wu^1,2

¹Department of Biological Sciences and ²Interdisciplinary Program in Neuroscience, University of Iowa, Iowa City, Iowa 52242

Correspondence should be addressed to Dr. Chun-Fang Wu, Professor, Department of Biological Sciences, University of Iowa, Iowa City, IA 52242. Email: chun-fang-wu{at}uiowa.edu

Environmental temperature is an important factor exerting pervasive influence on neuronal morphology and synaptic physiology. In the Drosophila brain, axonal arborization of mushroom body Kenyon cells was enhanced when flies were raised at high temperature (30°C rather than 22°C) for several days. Isolated embryonic neurons in culture that lacked cell–cell contacts also displayed a robust temperature-induced neurite outgrowth. This cell-autonomous effect was reflected by significantly increased high-order branching and enlarged growth cones. The temperature-induced morphological alterations were blocked by the Na⁺ channel blocker tetrodotoxin and a Ca²⁺ channel mutation but could be mimicked by raising cultures at room temperature with suppressed K⁺ channel activity. Physiological analyses revealed increased inward Ca²⁺ currents and decreased outward K⁺ currents, in conjunction with a distal shift in the site of action potential initiation and increased prevalence of TTX-sensitive spontaneous Ca²⁺ transients. Importantly, the overgrowth caused by both temperature and hyperexcitability K⁺ channel mutations were sensitive to genetic perturbations of cAMP metabolism. Thus, temperature acts in a cell-autonomous manner to regulate neuronal excitability and spontaneous activity. Presumably, activity-dependent Ca²⁺ accumulation triggers the cAMP cascade to confer the activity-dependent plasticity of neuronal excitability and growth.

Key words: mushroom body; Kenyon cells; growth cones; nerve terminal arborization; K⁺ channels; Ca²⁺ channels; action potential; Ca²⁺ transients/dynamics; spontaneous activity

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Received May 11, 2007; revised Sept. 6, 2007; accepted Sept. 27, 2007.

Correspondence should be addressed to Dr. Chun-Fang Wu, Professor, Department of Biological Sciences, University of Iowa, Iowa City, IA 52242. Email: chun-fang-wu{at}uiowa.edu

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