Hearing in Drosophila

The dissection of the Drosophila auditory system has revealed multiple parallels between fly and vertebrate hearing. Recent studies have analyzed the operation of auditory sensory cells and the processing of sound in the fly's brain. Neuronal responses to sound have been characterized, and novel classes of auditory neurons have been defined; transient receptor potential (TRP) channels were implicated in auditory transduction, and genetic and environmental causes of auditory dysfunctions have been identified. This review discusses the implications of these recent advances on our understanding of how hearing happens in the fly

Power gain exhibited by motile mechanosensory neurons in Drosophila ears

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

A mechanosensory pathway to the Drosophila circadian clock

Circadian clocks attune the physiology of virtually all living organisms to the diurnal cycles of their environments. In metazoan animals, multiple sensory input pathways have been linked to clock synchronization with the environmental cycle (entrainment). Extrinsic entrainment cues include light and temperature. We show that (12-hour:12-hour) cycles of vibration and silence (VS) are sufficient to synchronize the daily locomotor activity of wild-type Drosophila melanogaster. Behavioral synchronization to VS cycles required a functional clock and functional chordotonal organs and was accompanied by phase-shifts of the daily oscillations of PERIOD protein concentrations in brain clock neurons. The feedback from mechanosensory-and particularly, proprioceptive-organs may help an animal to keep its circadian clock in sync with its own, stimulus-induced activities

Assessing the acoustic behaviour of Anopheles gambiae (s.l.) dsxF mutants: implications for vector control

BACKGROUND: Release of gene-drive mutants to suppress Anopheles mosquito reproduction is a promising method of malaria control. However, many scientific, regulatory and ethical questions remain before transgenic mosquitoes can be utilised in the field. At a behavioural level, gene-drive carrying mutants should be at least as sexually attractive as the wildtype populations they compete against, with a key element of Anopheles copulation being acoustic courtship. We analysed sound emissions and acoustic preference in a doublesex mutant previously used to collapse Anopheles gambiae (s.l.) cages. METHODS: Anopheles rely on flight tones produced by the beating of their wings for acoustic mating communication. We assessed the impact of disrupting a female-specific isoform of the doublesex gene (dsxF) on the wing beat frequency (WBF; measured as flight tone) of males (XY) and females (XX) in homozygous dsxF- mutants (dsxF-/-), heterozygous dsxF- carriers (dsxF+/-) and G3 dsxF+ controls (dsxF+/+). To exclude non-genetic influences, we controlled for temperature and wing length. We used a phonotaxis assay to test the acoustic preferences of mutant and control mosquitoes. RESULTS: A previous study showed an altered phenotype only for dsxF-/- females, who appear intersex, suggesting that the female-specific dsxF allele is haplosufficient. We identified significant, dose-dependent increases in the WBF of both dsxF-/- and dsxF+/- females compared to dsxF+/+ females. All female WBFs remained significantly lower than male equivalents, though. Males showed stronger phonotactic responses to the WBFs of control dsxF+/+ females than to those of dsxF+/- and dsxF-/- females. We found no evidence of phonotaxis in any female genotype. No male genotypes displayed any deviations from controls. CONCLUSIONS: A prerequisite for anopheline copulation is the phonotactic attraction of males towards female flight tones within mating swarms. Reductions in mutant acoustic attractiveness diminish their mating efficiency and thus the efficacy of population control efforts. Caged population assessments may not successfully reproduce natural mating scenarios. We propose to amend existing testing protocols to better reflect competition between mutants and target populations. Our findings confirm that dsxF disruption has no effect on males; for some phenotypic traits, such as female WBFs, the effects of dsxF appear dose-dependent rather than haplosufficient

Turnover and activity-dependent transcriptional control of NompC in the Drosophila ear.

Across their lives, biological sensors maintain near-constant functional outputs despite countless exogenous and endogenous perturbations. This sensory homeostasis is the product of multiple dynamic equilibria, the breakdown of which contributes to age-related decline. The mechanisms of homeostatic maintenance, however, are still poorly understood. The ears of vertebrates and insects are characterized by exquisite sensitivities but also by marked functional vulnerabilities. Being under the permanent load of thermal and acoustic noise, auditory transducer channels exemplify the homeostatic challenge. We show that (1) NompC-dependent mechanotransducers in the ear of the fruit fly Drosophila melanogaster undergo continual replacement with estimated turnover times of 9.1 hr; (2) a de novo synthesis of NompC can restore transducer function in the adult ears of congenitally hearing-impaired flies; (3) key components of the auditory transduction chain, including NompC, are under activity-dependent transcriptional control, likely forming a transducer-operated mechanosensory gain control system that extends beyond hearing organs

Temperature Entrainment of Drosophila's Circadian Clock Involves the Gene nocte and Signaling from Peripheral Sensory Tissues to the Brain

Circadian clocks are synchronized by the natural day/night and temperature cycles. Our previous work demonstrated that synchronization by temperature is a tissue autonomous process, similar to synchronization by light. We show here that this is indeed the case, with the important exception of the brain. Using luciferase imaging we demonstrate that brain clock neurons depend on signals from peripheral tissues in order to be synchronized by temperature. Reducing the function of the gene nocte in chordotonal organs changes their structure and function and dramatically interferes with temperature synchronization of behavioral activity. Other mutants known to affect the function of these sensory organs also interfere with temperature synchronization, demonstrating the importance of nocte in this process and identifying the chordotonal organs as relevant sensory structures. Our work reveals surprising and important mechanistic differences between light- and temperature-synchronization and advances our understanding of how clock resetting is accomplished in nature

How Many Clocks, How Many Times? On the Sensory Basis and Computational Challenges of Circadian Systems

A vital task for every organism is not only to decide what to do but also when to do it. For this reason, “circadian clocks” have evolved in virtually all forms of life. Conceptually, circadian clocks can be divided into two functional domains; an autonomous oscillator creates a ∼24 h self-sustained rhythm and sensory machinery interprets external information to alter the phase of the autonomous oscillation. It is through this simple design that variations in external stimuli (for example, daylight) can alter our sense of time. However, the clock’s simplicity ends with its basic concept. In metazoan animals, multiple external and internal stimuli, from light to temperature and even metabolism have been shown to affect clock time. This raises the fundamental question of cue integration: how are the many, and potentially conflicting, sources of information combined to sense a single time of day? Moreover, individual stimuli, are often detected through various sensory pathways. Some sensory cells, such as insect chordotonal neurons, provide the clock with both temperature and mechanical information. Adding confusion to complexity, there seems to be not only one central clock in the animal’s brain but numerous additional clocks in the body’s periphery. It is currently not clear how (or if) these “peripheral clocks” are synchronized to their central counterparts or if both clocks “tick” independently from one another. In this review article, we would like to leave the comfort zones of conceptual simplicity and assume a more holistic perspective of circadian clock function. Focusing on recent results from Drosophila melanogaster we will discuss some of the sensory, and computational, challenges organisms face when keeping track of time

Transducer-Based Force Generation Explains Active Process in Drosophila Hearing

BACKGROUND: Like vertebrate hair cells, Drosophila auditory neurons are endowed with an active, force-generating process that boosts the macroscopic performance of the ear. The underlying force generator may be the molecular apparatus for auditory transduction, which, in the fly as in vertebrates, seems to consist of force-gated channels that occur in series with adaptation motors and gating springs. This molecular arrangement explains the active properties of the sensory hair bundles of inner-ear hair cells, but whether it suffices to explain the active macroscopic performance of auditory systems is unclear.Results: To relate transducer dynamics and auditory-system behavior, we have devised a simple model of the Drosophila hearing organ that consists only of transduction modules and a harmonic oscillator that represents the sound receiver. In vivo measurements show that this model explains the ear's active performance, quantitatively capturing displacement responses of the fly's antennal sound receiver to force steps, this receiver's free fluctuations, its response to sinusoidal stimuli, nonlinearity, and activity and cycle-by-cycle amplification, and properties of electrical compound responses in the afferent nerve.Conclusions: Our findings show that the interplay between transduction channels and adaptation motors accounts for the entire macroscopic phenomenology of the active process in the Drosophila auditory system, extending transducer-based amplification from hair cells to fly ears and demonstrating that forces generated by transduction modules can suffice to explain active processes in ears

Light Dominates Peripheral Circadian Oscillations in Drosophila melanogaster During Sensory Conflict

In Drosophila, as in other animals, the circadian clock is a singular entity in name and concept only. In reality, clock functions emerge from multiple processes and anatomical substrates. One distinction has conventionally been made between a central clock (in the brain) and peripheral clocks (e.g., in the gut and the eyes). Both types of clock generate robust circadian oscillations, which do not require external input. Furthermore, the phases of these oscillations remain exquisitely sensitive to specific environmental cues, such as the daily changes of light and temperature. When these cues conflict with one another, the central clock displays complex forms of sensory integration; how peripheral clocks respond to conflicting input is unclear. We therefore explored the effects of light and temperature misalignments on peripheral clocks. We show that under conflict, peripheral clocks preferentially synchronize to the light stimulus. This photic dominance requires the presence of the circadian photoreceptor, Cryptochrome

Hitting the right note at the right time: Circadian control of audibility in Anopheles mosquito mating swarms is mediated by flight tones

Mating swarms of malaria mosquitoes form every day at sunset throughout the tropical world. They typically last less than 30 minutes. Activity must thus be highly synchronized between the sexes. Moreover, males must identify the few sporadically entering females by detecting the females’ faint flight tones. We show that the Anopheles circadian clock not only ensures a tight synchrony of male and female activity but also helps sharpen the males’ acoustic detection system: By raising their flight tones to 1.5 times the female flight tone, males enhance the audibility of females, specifically at swarm time. Previously reported “harmonic convergence” events are only a random by-product of the mosquitoes’ flight tone variance and not a signature of acoustic interaction between males and females. The flight tones of individual mosquitoes occupy narrow, partly non-overlapping frequency ranges, suggesting that the audibility of individual females varies across males