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

Department of Physiology, Howard Hughes Medical Institute, University of California, San Francisco, CA 94143, USA.
Proceedings of the National Academy of Sciences (Impact Factor: 9.81). 04/2007; 104(12):5199-204. DOI: 10.1073/pnas.0700895104
Source: PubMed

ABSTRACT 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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    • "All chemicals were obtained from Sigma (St. Louis, Missouri). Previous electrophysiological studies of Drosophila larvae have used a dissection method which involves cutting up the dorsal midline (Barclay, Atwood & Robertson, 2002; Cattaert & Birman, 2001; Cooper & Neckameyer, 1999; Fox, Soll & Wu, 2006; Song et al., 2007; Ueda & Wu, 2006). However, since reliable access to intact dorsal-most body wall muscles 1 and 2 (Hoang & Chiba, 2001) was required for experiments, a new dissection method was developed in which these muscles did not risk damage from cutting down the midline or pinning. "
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    ABSTRACT: Rhythmic motor behaviors are generated by networks of neurons. The sequence and timing of muscle contractions depends on both synaptic connections between neurons and the neurons' intrinsic properties. In particular, motor neuron ion currents may contribute significantly to motor output. Large conductance Ca(2+)-dependent K(+) (BK) currents play a role in action potential repolarization, interspike interval, repetitive and burst firing, burst termination and interburst interval in neurons. Mutations in slowpoke (slo) genes encoding BK channels result in motor disturbances. This study examined the effects of manipulating slo channel expression on rhythmic motor activity using Drosophila larva as a model system. Dual intracellular recordings from adjacent body wall muscles were made during spontaneous crawling-related activity in larvae expressing a slo mutation or a slo RNA interference construct. The incidence and duration of rhythmic activity in slo mutants were similar to wild-type control animals, while the timing of the motor pattern was altered. slo mutants showed decreased burst durations, cycle durations, and quiescence intervals, and increased duty cycles, relative to wild-type. Expressing slo RNAi in identified motor neurons phenocopied many of the effects observed in the mutant, including decreases in quiescence interval and cycle duration. Overall, these results show that altering slo expression in the whole larva, and specifically in motor neurons, changes the frequency of crawling activity. These results suggest an important role for motor neuron intrinsic properties in shaping the timing of motor output.
    PeerJ 03/2013; 1:e57. DOI:10.7717/peerj.57 · 2.10 Impact Factor
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    • "In contrast, multidendritic neurons have a variable number of fine dendritic processes that lie beneath the epidermis and do not innervate a specific structure. Different subclasses of these neurons provide information about touch and body position as well as function as nociceptors (Hughes and Thomas, 2007; Song et al., 2007; Zhong et al., 2010). In the adult, external sensory and chordotonal neurons innervate more elaborate structures formed by the cuticle including bristles and antennae. "
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    ABSTRACT: Every moment of every day, our skin and its embedded sensory neurons are bombarded with mechanical cues that we experience as pleasant or painful. Knowing the difference between innocuous and noxious mechanical stimuli is critical for survival and relies on the function of mechanoreceptor neurons that vary in their size, shape, and sensitivity. Their function is poorly understood at the molecular level. This review emphasizes the importance of integrating analysis at the molecular and cellular levels and focuses on the discovery of ion channel proteins coexpressed in the mechanoreceptors of worms, flies, and mice.
    Neuron 05/2012; 74(4):609-19. DOI:10.1016/j.neuron.2012.04.023 · 15.98 Impact Factor
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    • "But does each class of Md neurons respond to different sensory inputs such as touch and temperature? Class I neurons, together with bipolar dendrite neurons, function in a proprioceptive sensory feedback circuit for rhythmic locomotion (Hughes and Thomas, 2007; Song et al., 2007), whereas class IV Md neurons are involved in avoidance behavior from a very bright light (Xiang et al., 2010). Are there also designated nociceptive neurons among the various classes of Md neurons? "
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    ABSTRACT: The word "nociception" is derived from the Latin "nocere," which means "to harm." Nociception refers to the sensory perception of noxious stimuli that have the potential to cause tissue damage. Since the perception of such potentially harmful stimuli often results in behavioral escape responses, nociception provides a protective mechanism that allows an organism to avoid incipient (or further) damage to the tissue. It appears to be universal in metazoans as a variety of escape responses can be observed in both mammalian and non-mammalian vertebrates, as well as diverse invertebrates such as leeches, nematodes, and fruit flies (Sneddon [2004] Brain Research Review 46:123-130; Tobin and Bargmann [2004] Journal of Neurobiology 61:161-174; Smith and Lewin [2009] Journal of Comparative Physiology 195:1089-1106). Several types of stimuli can trigger nociceptive sensory transduction, including noxious heat, noxious chemicals, and harsh mechanical stimulation. Such high-threshold stimuli induce the firing of action potentials in peripheral nociceptors, the sensory neurons specialized for their detection (Basbaum et al. [2009] Cell 139:267-284). In vertebrates, these action potentials can either be relayed directly to a spinal motor neuron to provoke escape behavior (the so-called monosynaptic reflex) or can travel via spinal cord interneurons to higher-order processing centers in the brain. This review will cover the establishment of Drosophila as a system to study various aspects of nociceptive sensory perception. We will cover development of the neurons responsible for detecting noxious stimuli in larvae, the assays used to assess the function(s) of these neurons, and the genes that have been found to be required for both thermal and mechanical nociception. Along the way, we will highlight some of the genetic tools that make the fly such a powerful system for studies of nociception. Finally, we will cover recent studies that introduce new assays employing adult Drosophila to study both chemical and thermal nociception and provide an overview of important unanswered questions in the field.
    Developmental Dynamics 01/2012; 241(1):16-26. DOI:10.1002/dvdy.22737 · 2.67 Impact Factor
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