Dynamic analysis of larval locomotion in Drosophila chordotonal organ mutants

Abstract

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 ...

The Extracellular Matrix Protein Artichoke Is Required for Integrity of Ciliated Mechanosensory and Chemosensory Organs inDrosophilaEmbryos

“…The severity of the defect was similar in all atk alleles, including Uhg8 EY07139 . The fact that Uhg8 EY07139 homozygous larvae-which no longer show detectable atk expression in ch organs but keep a detectable expression in es organs-also show locomotive defects confirms previous works that propose that ch organs, in contrast to es organs, are major contributors to locomotive sensory feedback (Caldwell et al 2003;Cheng et al 2010).…”

“…Although muscle contractions that direct larval locomotion are controlled by the central nervous system, feedback from ch organs is required to coordinate the larval movement (Caldwell et al 2003;Cheng et al 2010). To test whether atk mutants display impaired locomotion, we assayed the crawling behavior of third instar larvae.…”

Mechanotransduction and auditory transduction in Drosophila

“…Chordotonal organs, thus, essentially stretch receptors, but like bristles, may transduce different stimuli depending on their location and attachment. In the larva, groups of up to five scolopidia attached to the body wall in each segment sense touch [54] and provide proprioceptive feedback on larval locomotion [12]. Adult chordotonal organs typically bridge the joint between two limb segments, so that flexion of the joint stretches the sense organ and stimulates the neurons.…”

Expression of the rubber‐like protein, resilin, in developing and functional insect cuticle determined using a Drosophila anti‐rec 1 resilin antibody

“…The lateral patches happen to overlie the lateral penta-scolopidial organs (lch5), stretch receptors in the embryo that are slung between a proximal and distal attachment point where the cablelike ligament cell and attachment cell make contact with the hypodermis (Hartenstein, 2005). Functional chordotonal organs are essential for normal peristaltic locomotion by larvae (Caldwell et al, 2003;Hughes and Thomas, 2007). One possibility is that resilin elasticises the cuticle between the upper and lower attachment points of the chordotonal organs.…”