The Role of the Tympanal Membranes in the Tuning of Auditory Receptors in Tettigoniidae (Orthoptera: Ensifera)

One of the fundamental problems in auditory research is the origin of the frequency selectivity of auditory receptors. Horridge (1960) demonstrated that the auditory interneurones in locusts were tuned to different sound frequencies, thus suggesting that the auditory receptors were frequency selective. Michelsen (1968, 1971) established that the auditory organ of locusts contained four groups of receptors with different characteristic sound frequencies and proposed that the frequency selectivity of the individual groups was dependent on the resonant properties of the tympanum. Investigation using the more sensitive of the two auditory receptors in the moth Prodenia eridania extended this proposal by suggesting that the tuning of this receptor depended on both resonant properties of the auditory organ (scoloparium) and filtering properties of the acoustic system (Adams, 1972), the most important factor in the latter being the tympanal membranes. In crickets and bushcrickets, however, the tympanal membranes vibrate in a simple mode for a wide band of sound frequencies (Paton, Capranica, Dragsten & Webb, 1977; Michelsen & Larsen, 1978), thus making it unlikely that the motion of the tympanum is responsible for the frequency selectivity (Zhantiev & Korsunovskaya, 1978; Esch, Huber & Wohlers, 1980) of the individual auditory receptors. Similarly, Ball & Hill (1978) demonstrated that auditory intemeurones of larval instar crickets are tuned even though they have no tympanal membranes. A recent study of the tonotopic organization of the auditory organ in bushcrickets (Oldfield, 1982) revealed that the auditory receptors remained tuned after the removal of one tympanum. This result, like those obtained from crickets, suggests that the resonant properties of the tympanal membranes are not responsible for the tuning of the individual auditory receptors. Conclusive evidence on this proposal, however, requires the removal of both tympanal membranes, thus eliminating the possibility that the remaining tympanum in the study by Oldfield (1982) determined the tuning of the auditory receptors.

Physiological recordings were obtained from 16 auditory receptors in preparations of the bushcricket Mygalopsis marki (Bailey) from which the tympanal membranes had been removed and more than 18 receptors in individuals with intact auditory systems. Each insect was waxed to a Perspex stage and the prothoracic legs, with a small portion of leg cuticle covering the auditory organ removed, were supported in a depression filled with insect Ringer (Fielden, 1960, buffered with 20mmoll⁻¹ HEPES and containing 3 g l⁻¹ glucose). This procedure did not alter the characteristic frequency or roll-offs in sensitivity of auditory intemeurones (Oldfield, 1984) and therefore did not affect the tuning of the auditory receptors. Physiological responses of individual auditory receptors to an 80-ms tone pulse with 10-ms rise and decay time were recorded by inserting glass microelectrodes filled with 5% aqueous Lucifer Yellow CH into the cell body of individual receptors. Following the determination of the frequency-threshold characteristic -defined as the sound pressure required to produce an average of three action potentials/stimulus for five consecutive stimulus presentations — Lucifer Yellow was injected into the receptor by passing negative current pulses through the recording electrode. Subsequent examination of the organ with fluorescent microscopy provided an unambiguous identification of the receptor from which recordings were obtained (Fig. 1).

In both intact preparations, and those in which the tympanal membranes were removed, each auditory receptor was tuned to a single sound frequency and had rolloffs in sensitivity of approximately 30–40 dB octave⁻¹ (Fig. 2A,B). The most sensitive receptors in both types of preparation were tuned to sound frequencies between 14 and 20 kHz (Fig. 2A,B). The tuning of specific receptors was not altered by removing the tympanal membranes. Fig. 3 shows the frequency-threshold characteristics of receptors 6 and 11 in the crista acustica of M. marki. In preparations with and without tympanal membranes these receptors were tuned to 7 and 20 kHz respectively. For receptor 6, the minimum threshold of 42 dB at 7 kHz, in the preparation without tympana, was 10 dB less than the average minimum threshold for receptor 6 in five intact preparations. For receptor 11, the threshold of 15 dB at 20 kHz, in the preparation without tympana, was only 1 dB greater than the average sensitivity for receptor 11 in five intact preparations.

These findings demonstrate that the presence of the tympanal membranes in M. marki does not contribute to the frequency selectivity of individual auditory receptors. In addition, the findings suggest that the sensitivity of individual receptors may not be determined by the motion of the tympana. This conclusion contrasts with the observations in crickets of Ball & Hill (1978) and Kliendienst, Wohlers & Larsen (1983). The auditory system of bushcrickets is significantly different from that of crickets. Most importantly, the sound pressure within the prothoracic leg trachea of bushcrickets is 15–25 dB greater than that surrounding the leg for sound frequencies above the cut-off frequency of the trachea (Hill & Oldfield, 1981). Unlike that in crickets, the response of the receptors in bushcrickets is dominated by the sound pressure in the prothoracic trachea. The tympanal membranes may, therefore, merely act as a device to release the pressure, in the haemolymph surrounding the receptors, created by the motion of the tracheal surface. As such, the tympanal membranes of bushcrickets may be analogues to the round window of the mammalian cochlea.