Targeted expression of tetanus toxin reveals sets of neurons involved in larval locomotion in <i>Drosophila</i>

Suster, Maximiliano L.; Martin, Jean‐René; Sung, Carl; Robinow, Steven

doi:10.1002/neu.10202

Cited by 53 publications

(44 citation statements)

References 52 publications

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“…These observations suggest that csp peristalsis is disrupted at the level of CNS integration. Recently, through targeted expression of TeTx, numerous central neurons that contribute to the larval locomotor CPG were identified, and their characterization is underway (18). Together, these data support the idea that many levels of integration at the PNS, NMJ, and CNS are necessary to produce rhythmic patterns of movement via the CPG circuit.…”

mentioning

confidence: 68%

Dynamic analysis of larval locomotion in Drosophila chordotonal organ mutants

Caldwell

Miller

Wing

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

139

144

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Rhythmic movements, such as peristaltic contraction, are initiated by output from central pattern generator (CPG) networks in the CNS. These oscillatory networks elicit locomotion in the absence of external sensory or descending inputs, but CPG circuits produce more directed and behaviorally relevant movement via peripheral nervous system (PNS) input. Drosophila melanogaster larval locomotion results from patterned muscle contractions moving stereotypically along the body segments, but without PNS feedback, contraction of body segments is uncoordinated. We have dissected the role of a subset of mechanosensory neurons in the larval PNS, the chordotonal organs (chos), in providing sensory feedback to the locomotor CPG circuit with DIAS (Dynamic Image Analysis System) software. We analyzed mutants carrying cho mutations including atonal, a cho proneural gene, beethoven, a cho cilia class mutant, smetana and touch-insensitive larva B, two axonemal mutants, and 5D10, a weak cho mutant. All cho mutants have defects in gross path morphology compared to controls. These mutants exhibit increased frequency and duration of turning (decision-making) and reduced duration of linear locomotion. Furthermore, cho mutants affect locomotor parameters, including reduced average speed, direction change, and persistence. DIAS analysis of peristaltic waves indicates that mutants exhibit reduced average speed, positive flow and negative flow, and increased stride period. Thus, cho sensilla are major proprioceptive components that underlie touch sensitivity, locomotion, and peristaltic contraction by providing sensory feedback to the locomotor CPG circuit in larvae.R hythmic movements, such as peristaltic contraction, are initiated by output from central pattern generators (CPGs) in the CNS. These oscillatory networks elicit locomotion in the absence of external sensory or descending inputs, but without feedback from the peripheral nervous system (PNS), contraction of body segments is uncoordinated (1-5). The Drosophila peristaltic CPGs form and become active during late embryogenesis and persist throughout larval stages (5-9). Coordinated peristalsis in Drosophila embryos, therefore, relies on output from the preformed CPG circuits as well as sensory feedback from the PNS. Here, we use DIAS (Dynamic Image Analysis System) software (10, 11) to demonstrate that chordotonal organs (chos), type I sense organs of the larval PNS (12, 13), constitute a major feedback mechanism that provides peripheral input to the CPG for normal locomotion.Suster and Bate (5) demonstrated that blocking neurotransmitter release in the entire embryonic PNS with tetanus toxin (TeTx) prevented normal peristalsis during late embryogenesis (14, 15). Interestingly, the peristaltic defects seen in TeTx embryos phenocopied those exhibited in senseless (sens) null mutants (5, 16). DIAS motility software was used to dissect the dysfunctional locomotor parameters of first-instar TeTx and sens larvae and the role of sensory input from the PNS in driving CPGs (5). Wang et ...

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mentioning

confidence: 68%

Dynamic analysis of larval locomotion in Drosophila chordotonal organ mutants

Caldwell

Miller

Wing

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

139

144

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“…For example, bursting activity could be pharmacologically evoked from a semi-intact preparation in which the brain lobes were severed from the ventral ganglia (Cattaert and Birman, 2001). In addition, subsets of neurons in the Drosophila brain were shown to contribute to initiation or modulation of locomotion (Suster et al, 2003).…”

Section: Cpg Localizationmentioning

confidence: 99%

Coordination and Modulation of Locomotion Pattern Generators inDrosophilaLarvae: Effects of Altered Biogenic Amine Levels by the Tyramine β Hydroxlyase Mutation

2006

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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 T␤h 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 T␤h nM18 mutants. These centrally generated patterned activities were eliminated in the distal stumps of both wild-type and T␤h 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 T␤h nM18 larvae. Significantly, rhythmic patterns of bursts and waves could be evoked in T␤h 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.

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“…To facilitate cell-autonomous expression of these constructs in the Tv cells, the above stocks were crossed with a fly stock containing both the GAL4 driver (Brand and Perrimon, 1993) under control of the FMRF-amide promoter and a UAS-GFP insert (Lee and Luo, 1999) that targets CD8::GFP to the membrane. The ywUASmCD8::GFP; FG10 stock made use of a FMRF-amide promoter construct created by S. Robinow, University of Hawaii (Schubiger et al, 2003;Suster et al, 2003). Progeny expressed both membrane-bound GFP and either EcR dominant negative construct or IR-EcR (core) cell autonomously in the Tv neurosecretory cells.…”

Section: W650amentioning

confidence: 99%