Morphological basis for a tonotopic design of an insect ear

    loading  Checking for direct PDF access through Ovid


For reproduction and survival, it is essential to detect and differentiate between species‐specific sound signals and those of predators or competing species. All of these signals differ in their temporal and spectral composition. Thus, efficient hearing organs should be capable of analyzing the relevant components. The hearing organ of flies for example, the Johnston's organ, which is located within the antennae (Child, 1894; Eggers, 1924) detects particle velocity leading to a high resolution of the temporal pattern of a sound stimulus (for review see Albert & Göpfert, 2015). Another mechanism to perceive temporal patterns is achieved by the tympanal membranes of notodontid moths (for review see Nakano, Takanashi, & Surlykke, 2015). The moths' organs often possess only a single receptor cell that is tuned to bat echolocation calls (Surlykke, 1984; Fullard, 1984) with the tuning based on the mechanical resonance of the tympanal membrane. In contrast to this single‐frequency tuning, dedicated spectral analysis of a signal can only be achieved by multiple sensory cells tuned to different frequencies, which could be produced by anatomical gradients along the extension of a hearing organ (Dallos, 1992; Patuzzi, 1996; Vater & Kössl, 2011). Cells at different locations along the anatomical gradient respond to different frequencies, which creates a tonotopic frequency representation. Such anatomical gradients together with a tonotopic representation of mechanical resonance frequencies were found and analytically explored in vertebrate ears (e.g., Lighthill, 1981; von Békésy, 1960), as well as in tympanal membranes of locusts and cicadas (Malkin, McDonagh, Mhatre, Scott, & Robert, 2013; Stephen & Bennet‐Clark, 1982; Sueur, Windmill, & Robert, 2006; Windmill, Göpfert, & Robert, 2005). As it is the case in vertebrates (mammals: for review see Pickles, 2015), the tonotopy created in the hearing organ of insects is preserved along the auditory pathway (for review see Stumpner & von Helversen, 2001). However, the frequency resolution often decreases along the auditory pathway in insects (Hennig, Franz, & Stumpner, 2004; Rheinlaender, 1975). Therefore, tonotopy helps to categorize neuronal frequency content (Römer, 1987; Römer & Lewald, 1992; Schildberger, Wohlers, Schmitz, Kleindienst, & Huber, 1986), for example, in predator and conspecific signals, or to sharpen frequency tuning (Boyan, 1981; Römer, 1987; Schildberger, 1984; Schul, 1997; Stumpner, 1997). This indicates the importance of tonotopic tuning that provides elementary cues for neuronal frequency analysis.
In this study, we investigated an insect hearing organ that uses traveling waves for spectral analysis of sound stimuli. These waves are inherent to the physical structure of the organ, which possesses an anatomical gradient with longitudinal coupling (Palghat Udayashankar, Kössl, & Nowotny, 2012). In mammals, the airborne acoustic signal is delivered to the inner ear via the eardrum and ossicles. The acoustic energy impinging on the cochlea via the stapes launches a fluid‐pressure and tissue wave along the longitudinal axis of the cochlea (Olson, 1999; von Békésy, 1960). The anatomical gradient of increasing mass and decreasing stiffness along the hearing organ causes a decrease in wave speed and an increase in the wave's amplitude. The wave's pressure becomes focused around the cochlear partition resulting in a bundling of energy at a characteristic frequency‐specific place on the basilar membrane. Beyond this place, mechanical damping is sufficient to dissipate energy and extinguish the traveling wave. In contrast to this complex chain of mechanical coupling in mammals, in locusts and cicadas the tympanal membrane is attached directly to the receptor cells. In the bushcricket hearing organ that is the subject of our work, the mechanical coupling of environmental sound is between these simple and complex extremes in locusts and mammals, respectively.
    loading  Loading Related Articles