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Acoustics

In a fly's ear

Organisms often identify the source of a sound by comparing the noises that arrive at the two ears. Using some interesting tricks, a minute fly has mastered this feat as accurately as humans.

The auditory systems of animals from insects to mammals are adept at detecting and identifying sounds — and, crucially, at locating their source. Although it is certainly helpful for a female tree frog to be informed of a male's presence in the vegetation from the sound of its call, it is arguably more useful to be able to locate the source of the call with precision, so that (in this case) mating can occur. Similarly, when the small parasitoid fly Ormia ochracea hears the song of the field cricket (Gryllus species), it must be able to locate the exact source of the song: female flies deposit larvae on or near the calling crickets, which ultimately serve as a food source for the developing fly larvae. Writing on page 686 of this issue1, Mason and colleagues reveal the degree of precision with which Ormia can locate crickets from their songs. They also describe a neuronal mechanism that could underlie this remarkable behaviour.

In general, the position of a sound source in three-dimensional space is computed by the auditory system from two physical cues: the difference in the time it takes for the sound to reach each of the ears (interaural time difference), and the difference in the intensity of the sound that reaches the ears (interaural intensity difference). These cues vary according to where the sound source is located relative to the midline axis. The midline axis runs equidistant between your ears, from behind to in front of your head. The interaural time difference is zero for a sound source located on the midline, but increases with the angular displacement of the sound source from the midline. (For a sound source that is located directly to the right or left of your head, the angular displacement is 90°.)

Sound localization becomes especially challenging for small animals such as Ormia, for which the distance between the ears is only 0.5 mm. In practice, this means that the maximum interaural time difference for Ormia (that is, when the sound is located at 90° to the midline) is only about 1.5 μs, and the interaural intensity difference is vanishingly small. Even so, these flies can pinpoint sounds exceptionally well. Mason et al.1 report that Ormia is capable of locating a loudspeaker broadcasting cricket songs to within 2° of the midline. This means that Ormia can detect a change in interaural time difference of a mere 50 ns. How does it achieve this?

The tympana (eardrums) of Ormia, located behind the fly's head, are connected internally by a cuticle-based bridge that functions as a flexible lever2,3. This unusual structure means that the membranes of the tympana can vibrate in response to sound in two distinct ways, with different resonant frequencies3. Over the operating range of 5–20 kHz, the actual motion of the tympana is the result of a linear combination of these two resonant modes. There are two consequences of this arrangement2,3. First, the maximum difference in the amplitude of vibration of the two eardrums increases to 10 dB. Second, the maximum time delay between the mechanical displacements of the two eardrums increases to about 55 μs. So, minute interaural time differences are converted by Ormia's unique tympanal structures into respectable interaural amplitude differences and increased interaural mechanical time differences. These differences can be processed more easily by sensory receptor neurons.

Mason et al.1 have now measured the differences in the time it takes for individual sensory receptor neurons to fire (a time known as the latency) in response to sounds at various angles from the midline. They also measured the 'summed response latency differences' for the whole auditory nerve — the collection of sensory receptor neurons — in response to stimuli from the left and right sides of the animal. Neuronal response latencies are known to shorten in direct proportion to the intensity of a stimulus4, so the neuronal latency differences for sounds impinging on the fly from 90° to the midline are six times higher (about 300 μs) than the mechanical time differences1. In other words, the interaural difference increases still further with this next step in sound detection (Fig. 1).

Figure 1: The parasitoid fly Ormia can locate cricket songs with pinpoint accuracy.
figure1

RON HOY, CORNELL UNIV.

It can do so by amplifying the difference between the sounds that reach each ear. a, The head of Ormia. b, Amplification of sound differences. The interaural time difference refers to the maximal difference between the amount of time it takes sounds to reach each ear. The mechanical time difference is the maximal difference between the times at which the two eardrum membranes respond to the sound. The neural time difference is the maximal difference between the response latencies of the left and right auditory nerves. At each stage the left–right differences are exaggerated, enabling the central nervous system of the fly to localize cricket songs with stunning accuracy, as shown by Mason et al.1.

Nevertheless, Mason et al. find that interaural neuronal latency differences are only about 3.5 μs per degree of angular displacement. So, when the source of the sound (the loudspeaker) is moved through an angle of 2°, the corresponding latency differences are remarkably small, about 7 μs. Adding insult to injury, the variability in the timing of firing by receptor neurons following repetitive stimuli is ten times greater than this, of the order 70 μs. Mason et al. suggest that, for Ormia to detect a latency (signal) of 7 μs in jitter (noise) of 70 μs, the fly must use a mechanism of temporal hyperacuity, much like that first described for the weakly electric fish Eigenmannia virescens5,6. Temporal hyperacuity is the result of convergence of many receptor neurons onto a central cell. Each input neuron, when it fires, generates a subthreshold action potential in the central cell. That cell will fire an action potential only when it receives most of its inputs together. This arrangement is relatively resistant to 'outlier' subthreshold potentials that occur much earlier or later than the mean. So the temporal variability in the firing of action potentials by the central cell will be reduced.

Despite their inherent noise, sensory systems often have specialized mechanisms for reliably detecting extremely small signals. One such mechanism, stochastic resonance, takes advantage of random, broad-spectrum noise in the sensory receptors to increase the system's sensitivity to weak signals. Not surprisingly, stochastic resonance has been described in several sensory systems, including mechanoreceptors7,8,9, photoreceptors10, electroreceptors11, auditory hair cells12 and auditory nerve fibres13. Work on Eigenmannia5,6 and now Ormia1,2,3 has addressed the problem of the temporal variability that is introduced by sensory receptors. It seems that temporal hyperacuity is one mechanism that may help to overcome such variability, and so might be seen as complementary to stochastic resonance. It is only because its central nervous system reduces temporal variability that Ormia is able to localize sound sources to within 2°. Ineluctably, further studies of this remarkable insect ear will lead to the development of biologically based, miniaturized directional 'ormiaphones' for potential use in hearing aids and other listening devices.

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Correspondence to Peter M. Narins.

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