nompA Encodes a PNS-Specific, ZP Domain Protein Required to Connect Mechanosensory Dendrites to Sensory Structures

161

126

In Drosophila melanogaster, hearing is supported by mechanosensory neurons transducing sound-induced vibrations of the antenna. It is shown here that these neurons additionally generate motions that mechanically drive the antenna and tune it to relevant sounds. Motion generation in the Drosophila auditory system is betrayed by the auditory mechanics; the antenna of the fly nonlinearly alters its tuning as stimulus intensity declines and oscillates spontaneously in the absence of sound. The susceptibility of auditory motion generation to mechanosensory mutations shows that motion is generated by mechanosensory neurons. Motion generation depends on molecular components of the mechanosensory transduction machinery (NompA, NompC, Btv, and TilB), apparently involving mechanical activity of ciliated dendrites and microtubule-dependent motors. Hence, in analogy to vertebrate hair cells, the mechanosensory neurons of the fly serve dual, transducing, and actuating roles, documenting a striking functional parallel between the vertebrate cochlea and the ears of Drosophila.

Section: Resultsmentioning

confidence: 80%

Section: Resultsmentioning

confidence: 99%

See 1 more Smart Citation

Motion generation by Drosophila mechanosensory neurons

Göpfert

Robert

2003

161

126

“…Similarly, differences in centroid piling during a single wave of peristaltic contraction can discriminate between the axonemal class and btv; the peaks͞plateaus in btv and troughs in axonemal class mutants are aberrant, suggesting that differences in defects in the ultrastructure of a cho will produce different, but predictable, peristaltic defects. This is particularly interesting when considering the number of touch sensitivity and locomotor mutants that have been identified as molecular components of the cho (19,20,25,(31)(32)(33)(34)(35)(36) and whose defects in larval locomotion are likely to be similar to those presented in this article. A more thorough understanding of the role of these genes in mechanosensation and their effects on feedback to the CPG will be possible through identification and characterization of their gene products.…”

Section: Discussionmentioning

confidence: 76%

Dynamic analysis of larval locomotion in Drosophila chordotonal organ mutants

Caldwell

Miller

Wing

et al. 2003

136

138

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 ...

“…7), we examined the fluctuations of the receiver in live mutants with defective mechanosensory neurons. In tilB 2 , btv 5P1 , and nompA 2 mutants, the mechanosensory neurons that mediate hearing reportedly display distinct, mutant-specific anatomical defects, including aberrations of dendritic cilia (tilB 2 , btv 5P1 ) (24) and the disconnection of the neurons from the antennal receiver (nompA 2 ) (25). In line with these structural defects, the receivers of the mutants displayed mutant-specific natural frequencies and fluctuation powers (Fig.…”

Section: Validating the Prediction: Receiver Fluctuations In Live Mecmentioning

confidence: 73%

Power gain exhibited by motile mechanosensory neurons in Drosophila ears

Göpfert

Humphris²,

Albert³

et al. 2004

116

134

In insects and vertebrates alike, hearing is assisted by the motility of mechanosensory cells. Much like pushing a swing augments its swing, this cellular motility is thought to actively augment vibrations inside the ear, thus amplifying the ear's mechanical input. Power gain is the hallmark of such active amplification, yet whether and how much energy motile mechanosensory cells contribute within intact auditory systems has remained uncertain. Here, we assess the mechanical energy provided by motile mechanosensory neurons in the antennal hearing organs of Drosophila melanogaster by analyzing the fluctuations of the sound receiver to which these neurons connect. By using dead WT flies and live mutants (tilB 2 , btv 5P1 , and nompA 2 ) with defective neurons as a background, we show that the intact, motile neurons do exhibit power gain. In WT flies, the neurons lift the receiver's mean total energy by 19 zJ, which corresponds to 4.6 times the energy of the receiver's Brownian motion. Larger energy contributions (200 zJ) associate with self-sustained oscillations, suggesting that the neurons adjust their energy expenditure to optimize the receiver's sensitivity to sound. We conclude that motile mechanosensory cells provide active amplification; in Drosophila, mechanical energy contributed by these cells boosts the vibrations that enter the ear.cochlear amplifier ͉ hearing ͉ auditory mechanics ͉ cell mobility ͉ hair cell T he cochlear amplifier is the dominant unifying concept in cochlear mechanics (1). The concept assumes that the cochlea is endowed with a biological energy source that amplifies the ear's input by pumping mechanical energy into the vibrations inside the ear (1-6). The validity of the concept is supported by the mechanics of the cochlea and its mechanosensory cells. Hair cells, the cochlear mechanosensory cells, provide a source of mechanical energy. In addition to transducing mechanical vibrations into electrical responses, some hair cells are equipped with molecular motors that convert metabolic or electrical energy into mechanical energy, resulting in active movements of the cells (1, 3-7). These cellular movements, in turn, exert positive feedback on the cochlear mechanics. By nonlinearly undamping the cochlear resonances as the stimulus intensity declines, this feedback selectively improves the ear's sensitivity to small vibrations induced by faint sound (1, 3-6). Notably, this hair cell-based feedback occasionally becomes unstable, leading to self-sustained feedback oscillations within the cochlear duct. Such self-sustained feedback oscillations may account for the ear's ability to generate spontaneous otoacoustic emissions, i.e., to spontaneously emit sound (8, 9).Collectively, the hair cells' motility, the cochlea's nonlinearity, and the ear's spontaneous otoacoustic emissions document the presence of hair cell-based mechanical feedback inside the cochlear duct. Yet, whether this feedback brings about power gain by expending biological energy, as assumed by the concept of the cochlear ampli...