Synchrony through twice-frequency forcing for sensitive and selective auditory processing

Abstract

Male mosquitoes detect flying females using antennal hearing organs sensitive to nanoscale mechanical displacements and that harbor motile mechanosensory neurons. The mechanisms supporting neuronal motility, and their function in peripheral sensory processing, remain, however, puzzling. The mechanical and neural responses reveal a transition that unmasks the onset of synchronization between sensory neurons. This synchronization constitutes an unconventional, mechanically driven, process of communication between sensory neurons. Enhancing auditory sensitivity and selectivity, synchronization between mechanosensors in the mosquito arises from entrainment to twice-frequency forcing and is formally analogous to injection-locking in high-power laser technology. This discovery opens up the enticing possibility that other sensory systems, even nonsensory cell ensembles, coordinate their actions through mechanical signaling.bioacoustics ͉ entrainment ͉ mosquito audition ͉ nonlinear hearing H earing organs convert acoustic energy into mechanical energy that, in turn, is transduced into action potentials from mechanically sensitive neurons. One particular challenge associated with this process is the extremely low energy content of sound waves. Physically, the sound energy imparted to the ear is weak, even compared with that conveyed by photons onto the retina of visual animals. In effect, energy thresholds for hearing can be close to thermal noise (Ϸ4 zJ), or one-hundredth of the energy of 1 single green photon (1, 2). Hearing has long been suggested, first by Gold (3), to operate in analogy to a regenerative amplifier, whereby the mechanically sensitive cells add their own mechanical energy to the oscillation they sense in the first place. Known as the cochlear amplifier in mammals and humans, this process assists sound-induced vibrations to nonlinearly amplify weak sounds and enhance frequency selectivity (4). Hearing organs usually comprise a large collection of mechanosensory cells (neurons in insects, epithelial hair cells in vertebrates) that can be viewed as an ensemble of mechanically coupled sensors. In mosquitoes and flies, auditory neurons have an unconventional dual sensory and motor function (5, 6) that is used to generate power, actively enhancing the mechanical response of the antenna to sound (5, 6).More generally, coupled nonlinear oscillators undergo a variety of synchronization phenomena (7,8), examples of which include fireflies flashing in unison (9) and chemical waves in the Belousov-Zhabotinsky (BZ) chemical reaction (10,11). Of particular importance is the class of synchronization called frequency entrainment (12), where coupled oscillators lock to the rhythm of an external stimulus. For example the suprachiasmatic nucleus of mammals, which controls circadian rhythms, is entrained to the day-night cycle by photoreceptors in the eye (7, 13). Further examples, borrowed from technology, include van der Pol's early investigations into entrainment of triode generators (14), and the synchronization of m...

Exceptional high-frequency hearing and matched vocalizations in Australian pygopod geckos

“…An indirect influence would be compatible with the substantially higher thresholds of responses to frequencies above 8kHz. A similar suggestion was recently made for the responses of auditory receptor cells in Johnson's organ of the antennae of mosquitoes, for which a response forcing was envisaged, with some receptors responding to twice the best frequency of the hearing organ but amplifying the response of other receptors to lower frequencies (Jackson et al, 2009). It is an intriguing possibility worth pursuing that in Delma, a vertebrate ear has also realized the same twice-frequency forcing mechanism.…”

Neural responses to one- and two-tone stimuli in the hearing organ of the dengue vector mosquito

“…It is also curious that while mosquito sensory neurons are paired in scolopidial transduction units, mammalian hair cells come in two types, outer ones that add energy to the system and inner ones that convey information centrally. Active amplification is known in mosquitoes but its cellular basis has not yet been identified (Göpfert and Robert, 2001;Jackson et al, 2009). Periodic oscillations observed in Johnston's organ are often at twice the stimulus frequency.…”

“…It has long been known that the primary afferents therein are sensitive to pure tones near the fundamental frequency of the wing beats, with gross-evoked field potentials oscillating at twice the stimulus frequency (e.g. Tischner, 1953;Wishart et al, 1962;Belton, 1974;Göpfert and Robert, 2000;Jackson et al, 2009). Oscillations are not observed at stimulus frequencies corresponding to the higher harmonics of the flight tone, however, and so cannot underlie matching behavior in Ae.…”

No evidence for DPOAEs in the mechanical motion of the locust tympanum

“…Sound is received by antennal structures on the head with a chordotonal organ, the Johnston's organ, at the base. The non-linearity is produced by mechanical amplification of the oscillations of the antennae, generated through the mechanosensory cells within the Johnston's organ (Göpfert and Robert, 2001;Jackson and Robert, 2006;Albert et al, 2007;Nadrowski et al, 2008;Jackson et al, 2009). As Müller's organ is composed of scolopidia, in common with Johnston's organ in Diptera, it would not be surprising if Muller's organ was capable of active amplification.…”

“…antennal displacements of mosquitoes and fruit flies have both been shown to amplify received sound through mechanical and active non-linearities (Göpfert and Robert, 2001;Jackson and Robert, 2006;Jackson et al, 2009). Sound is received by antennal structures on the head with a chordotonal organ, the Johnston's organ, at the base.…”