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The Journal of Neuroscience, February 1, 2006, 26(5):1486-1498; doi:10.1523/JNEUROSCI.4749-05.2006

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Behavioral/Systems/Cognitive
Coordination and Modulation of Locomotion Pattern Generators in Drosophila Larvae: Effects of Altered Biogenic Amine Levels by the Tyramine Hydroxlyase Mutation

Lyle E. Fox, David R. Soll, and Chun-Fang Wu

Department of Biological Sciences, University of Iowa, Iowa City, Iowa 52242

Correspondence should be addressed to Dr. Lyle E. Fox, Department of Biological Sciences, University of Iowa, 231 Biology Building, Iowa City, IA 52242. Email: lyle-fox{at}uiowa.edu

Forward locomotion of Drosophila melanogaster larvae is composed of rhythmic waves of contractions that are thought to be produced by segmentally organized central pattern generators. We present a systematic description of spike activity patterns during locomotive contraction waves in semi-intact wild-type and mutant larval preparations. We have shown previously that Th^nM18 mutants, with altered levels of octopamine and tyramine, have a locomotion deficit. By recording en passant from the segmental nerves, we investigated the coordination of the neuronal activity driving contraction waves of the abdominal body-wall muscles. Rhythmic bursts of activity that occurred concurrently with locomotive waves were frequently observed in wild-type larvae but were rarely seen in Th^nM18 mutants. These centrally generated patterned activities were eliminated in the distal stumps of both wild-type and Th^nM18 larvae after severing the segmental nerve from the CNS. Patterned activities persisted in the proximal stumps deprived of sensory feedback from the periphery. Simultaneous recordings demonstrated a delay in the bursting activity between different segments, with greater delay for segments that were farther apart. In contrast, bilateral recordings within a single segment revealed a well synchronized activity pattern in nerves innervating each hemisegment in both wild-type and Th^nM18 larvae. Significantly, rhythmic patterns of bursts and waves could be evoked in Th^nM18 mutants by head or tail stimulation despite their highly irregular spontaneous activities. These observations suggest a role of the biogenic amines in the initiation and modulation of motor pattern generation. The technique presented here can be readily extended to examine the locomotion motor program of other mutants.

Key words: fictive locomotion; biogenic amines; motor pattern; locomotion control; octopamine; tyramine; segmental coordination

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Received Nov. 5, 2005; revised Dec. 14, 2005; accepted Dec. 14, 2005.

Correspondence should be addressed to Dr. Lyle E. Fox, Department of Biological Sciences, University of Iowa, 231 Biology Building, Iowa City, IA 52242. Email: lyle-fox{at}uiowa.edu

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