Peripheral multidendritic sensory neurons are necessary for rhythmic locomotion behavior in Drosophila larvae

University of California, San Francisco, San Francisco, California, United States
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 04/2007; 104(12):5199-204. DOI: 10.1073/pnas.0700895104
Source: PubMed


From breathing to walking, rhythmic movements encompass physiological processes important across the entire animal kingdom. It is thought by many that the generation of rhythmic behavior is operated by a central pattern generator (CPG) and does not require peripheral sensory input. Sensory feedback is, however, required to modify or coordinate the motor activity in response to the circumstances of actual movement. In contrast to this notion, we report here that sensory input is necessary for the generation of Drosophila larval locomotion, a form of rhythmic behavior. Blockage of all peripheral sensory inputs resulted in cessation of larval crawling. By conditionally silencing various subsets of larval peripheral sensory neurons, we identified the multiple dendritic (MD) neurons as the neurons essential for the generation of rhythmic peristaltic locomotion. By recording the locomotive motor activities, we further demonstrate that removal of MD neuron input disrupted rhythmic motor firing pattern in a way that prolonged the stereotyped segmental motor firing duration and prevented the propagation of posterior to anterior segmental motor firing. These findings reveal that MD sensory neuron input is a necessary component in the neural circuitry that generates larval locomotion.

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    • "To test whether Ppk1 and Ppk26 regulate locomotor behavior via their activity in class IV da neurons in a cell-autonomous manner, we examined locomotor behavior in larvae expressing either Ppk26-RNAi or Ppk1-RNAi in class IV da neurons using the ppk1-Gal4 driver (Grueber et al., 2007). Crawling behavior in Drosophila larvae consists of sequential contractions of circumferential and longitudinal muscles in each segment, which propagate from posterior to anterior segments (Fox et al., 2006; Hughes and Thomas, 2007; Song et al., 2007; Ainsley et al., 2003; Vogelstein et al., 2014). Knockdown of either Ppk1 or Ppk26 resulted in a decrease in turning frequency (Figure 5A), such that locomotion was predominately composed of directional crawling. "
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    • "Detailed genotypes of the animals and clones are described and summarized in Supplementary Table S1. To visualize dendrites and /or express transgenes, we used the following Gal4 drivers: Gr28b.c5152 and Gal45-4053. To express fluorescent proteins, we used UAS-mCD8:GFP (#5137 of the Bloomington Stock Center) or UAS-Venus-pm445455. "
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    • "Multiple dendritic neurons are further classified, based on the complexity of their dendritic arbors, into bipolar dendritic (bd) neurons and four classes of dendritic arborization (da) neurons (I–IV) [10]. Among these, bd and class-I da neurons, which have relatively simple dendritic arbors, appear to be particularly important for normal larval locomotion (hereafter, we refer to these neurons as md neurons for simplicity) [8], [11], [12]. When function of the md neurons is temporally inhibited, the speed of locomotion is greatly reduced. "
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