ALBERT

Notes: Summary 1. Phonotaxis by female cricketsTeleogryllus commodus to synthetic signals is dependent on carrier frequency. Signals with carrier frequencies of 2.0 kHz and 16.0 kHz elicit phonotactic responses from relatively few individuals, although presented more than 20 dB above the threshold of cervical auditory interneurons. 2. The frequency of the natural song covers 3.5–4.0 kHz. The further from this is the frequency of the synthetic signal, the greater is the difference between the corresponding auditory threshold of cervical interneurons and the intensity of presentation of the signal at which a significant number of female crickets respond phonotactically. 3. Two categories of auditory interneuron with differing pitch sensitivities have been recorded in the cervical connectives. Activity in the two types of interneuron results from vibration of only the large tympanum of the auditory organ.

Notes: Summary The ears of crickets (Teleogryllus commodus and an undescribed species) are sharply tuned to the frequency of the species' communication signal. The auditory tympanum is vibrated by sound simultaneously acting on its external surface and on its internal surface after entering the prothoracic tracheal system. The sensitivity and frequency of the hearing optimum of the ear ipsilateral to incident sound, however, does not depend on the interaction of the external and internal sound pressures at the tympanum. The tuned response of the ear does not depend on acoustic properties of the prothoracic leg trachea, but on unknown mechanisms at the ear itself. When considered in isolation from the rest of the auditory system, the cricket ear has no directional sensitivity to sound, in the range 2.0 kHz to 15.0 kHz, propagated in the plane perpendicular to the tibia. Directional sensitivity of the intact auditory system is achieved by a diminution of the response of the ear contralateral to the source. This is the result of sound transmission along the trachea from the ipsilateral ear to the contralateral tympanum, where destructive interference with the external sound pressure occurs. The directional sensitivity occurs in a narrow frequency band which includes the species' song frequency and it may depend in part on tuned transmission of sound in the trachea. The nature of the binaural response in crickets locomoting in a sound field is discussed in terms of the mechanism of directional hearing. The possible generality of this principle of directionality to other families of insects is considered.

Notes: Summary 1. InTeleogryllus commodus andT. oceanicus, vibration of the tibia of the prothoracic leg at audio-frequencies stimulates auditory receptors in the tympanal organ, despite immobilization of the large tympanum by vaseline. 2. Responses of characteristic auditory interneurons in the adult cervical connective are similar whether stimulation is by sound or by vibration of the tibia (Figs. 3–5). 3. Interneurons in second-last (A-2) and last (A-1) immature instars are stimulated by sound and by vibration of the tibia and we conclude that these interneurons are the same as those recorded in adults (Figs. 6, 7). Peripheral receptors and some interneurons in the immature auditory system are, therefore, physiologically competent. 4. At the imaginai moult, auditory threshold at the optimum frequency decreases dramatically (Fig. 8 A). This increase in sensitivity to sound is attributed mainly to the appearance of the auditory tympanum in the adult. There is a much smaller increase in sensitivity to vibration of the tibia at audio frequencies between last instar nymphs and adults (Fig. 8 B). 5. From the A-2 to adult stages ofT. commodus, auditory receptors stimulated by sound show a peak sensitivity at 3.8 to 4.0 kHz (Fig. 8 A). Such tuning must be independent of vibration characteristics of the tympanum and of acoustic resonance characteristics depending on the dimensions of the leg trachea.

Notes: Summary Investigation of the physiological and biophysical properties of the auditory system of the New Zealand weta,Hemideina crassidens has revealed the following: 1. The frequency/threshold curve for the massed response of primary auditory fibres in the tympanal nerve has a peak of sensitivity at 2.0–2.5 kHz. Absolute threshold is 20–35 dB SPL in individual preparations and the roll-off is about 15 dB/octave below the optimum and about 27 dB/octave above the optimum frequency (Fig. 1). 2. Occlusion of either the anterior or posterior tympanum causes a small loss of sensitivity (〈8dB) only for frequencies above the hearing optimum. Occlusion of both auditory tympana reduces the sensitivity of the ear by 20–25 dB from 0.63 kHz to 5.0 kHz and by 7–15 dB up to 10 kHz (Fig. 2). 3. Blocking the leg tracheae in the femur causes no change in the sensitivity of the ear to sounds of 0.63–10 kHz (Fig. 3). Shielding the tympanic membranes from external sound, with the tracheal system intact, reduces the sensitivity of the ear by about 40 dB at the optimum frequency and by more than 10 dB for other frequencies in the range 0.63–10 kHz (Fig. 4). 4. Reducing the volume of the tibial air space behind the tympana by approximately 60% increases auditory thresholds for frequencies at and below the hearing optimum, whereas thresholds for higher frequencies are unchanged (Fig. 5). 5. For sound frequencies from 0.63 kHz to 8.0 kHz, the intact auditory system inH. crassidens has no directional sensitivity (Fig. 6). 6. Stridulatory sounds produced byH. crassidens are broad-band, having a peak in the power spectrum near 2.0 kHz and a roll-off of about 15 dB/octave towards higher frequencies (Fig. 7). 7. The weta auditory system functions as a one-input pressure receiver; its characteristics are compared with the auditory systems of Gryllidae and Tettigoniidae.

Notes: Summary 1. An ascending, auditory unit has been extracellularly recorded from the cervical connective in specimens of two tettigoniid species. Spike potentials arising from unilateral afferent input were monitored in response to airborne sounds in the frequency range 6.3–40 kHz and incident from different directions. Recordings were also obtained of the massed auditory response in the tympanal nerve in a third species. 2. Frequency sensitivities of auditory organs were measured at threshold and suprathreshold levels. Optimum frequencies generally corresponded with energy peaks in relevant song spectra (Figs. 3, 4). Intensity characteristics of the ascending unit were obtained near the corresponding frequency optimum (Fig. 5). Directional sensitivities of the auditory organs near the frequency optima were measured at 15 ° intervals around the preparation at threshold and suprathreshold levels of stimulation (Fig. 6). Threshold sensitivities to ipsilateral and contralateral stimulation were compared over the range 6.3–40 kHz. 3. Directional sensitivity of the ascending unit generally increased with increasing sound frequency. Maximum differences of from 8–25 dB were observed between sensitivities to ipsilateral and contralateral sound presentation in the frequency range 6.3–40 kHz (Fig. 8). Similar results were obtained for the massed primary response. 4. The frequency sensitivity and the directional sensitivity of the auditory organs, for sound frequencies higher than 8–10 kHz (depending on species) and at threshold and suprathreshold levels, were found to be independent of pressure-gradient effects at the auditory tympana (Figs. 7, 8). 5. The gross morphology of the prothoracic spiracle and associated trachea to the level of the tympanic membranes has been examined in each species. In the thorax, the trachea abruptly reduces in cross sectional area by about a factor of five. From the coxa to the distal femur the trachea undergoes a further three to four-fold reduction in cross section (Fig. 2). 6. Physiological experiments and direct measurements using miniature probe microphones indicate that, in the frequency range 8–40 kHz (depending on species) the acoustic gain of the trachea leading from the prothoracic spiracle to the auditory tympana is 10–30 dB (Figs. 9, 10). The shape of the hearing threshold curve, however, only partially matches the gain curve of the trachea. 7. Near the frequency optimum of the auditory organ, the sound pressure measured by a probe microphone in the thoracic tracheal vesicle adjacent to the prothoracic spiracle changes by 10–16 dB as a function of the direction of the incident sound (Fig. 12 A). 8. Simultaneous measurements using two probe microphones show that relative sound pressure in the thoracic tracheal vesicle changes by 10–16 dB, whereas that in the trachea distal in the femur may change by 8–24 dB for different directions of sound (Fig. 12C). Directional sensitivities measured neurophysiologically are, therefore, fully explained by the relative sound pressure level in the fore-leg trachea leading to the auditory tympana. 9. Dissimilarities sometimes observed between the directivity patterns of the sound pressures measured in the thoracic vesicle and in the femoral trachea possibly are due to the effects of sound entering the trachea along the length of the leg. 10. These results are discussed in relation to the properties of acoustic horns and to other recent studies of auditory function in tettigoniids.

Notes: Summary 1. From intracellular recordings from auditory receptors in locusts, confirmed by dye injection (Fig. 1), five distinct types of sustained or transient membrane potentials are identified that are associated with sensory function. 2. Receptor cell membranes are at resting potentials of 50–65 mV, inside negative, relative to a presumed potassium ion equilibrium potential of about -70 mV (Fig. 2). 3. Spontaneous and stimulus-evoked, discrete subthreshold depolarizations of up to about 5 mV are recorded (as described in the preceding paper) (Figs. 3, 9, 12). 4. Stimulus-evoked receptor potentials of up to about 20 mV and graded with stimulus intensity, result from the superposition of discrete depolarizations (as indicated in the preceding paper). In some of the cells recorded, there is pronounced adaptation in the receptor potential (Figs. 3, 4). 5. Regenerative (transient), depolarizing potentials of consistent, small amplitude (from 10 mV to 30 mV in any particular cell) occur spontaneously and/or in response to acoustic stimuli. Based on the inferred site of the generation of this class of spike, they are termed apical spikes (Figs. 5, 6, 7, 8). 6. The generation of apical spikes is membrane voltage-dependent. Their occurrence is reduced by hyperpolarization of the cell and increased by depolarization (Figs. 5, 6). 7. The apical spike potentials seem to be restricted to a region of the cell membrane. The conduction of the apical spike potential along the dendrite appears to be electrotonic. 8. Regenerative (transient) depolarizations of consistent, large amplitude (from 50 mV to 65 mV in any cell) occur spontaneously and/or in response to acoustic stimuli. Based on the inferred site of the generation of this class of spike, they are termed basal spikes (Fig. 9). 9. The generation of basal spikes is also membrane voltage-dependent. They are suppressed by hyperpolarization and are initiated by depolarization of the cell. Basal spike frequency is directly proportional to membrane depolarization (Figs. 2, 3). 10. Apical spikes appear normally to initiate basal spikes, with one to one correspondence. On occasions, the basal spike fails, evidently due to insufficient depolarization of the membrane by the apical spike (Figs. 7, 8). 11. Basal spikes appear to depend on conventional sodium ion (inward) and potassium ion (outward) currents via voltage-dependent conductance channels. The spiking mechanism is disabled by excessive depolarization of the cell. Spike potentials are abolished by extracellular application of the sodium conductance blocker, tetrodotoxin (TTX) (Fig. 4). Intracellular application of the potassium conductance blockers, tetraethylammonium ion (TEA) or caesium ion rapidly abolishes the hyperpolarizing undershoot on the action potentials (Fig. 10). 12. Within 1–2 min of injection of either TEA or caesium ion into receptor cells, all voltage-dependent and stimulus-dependent conductance mechanisms are disabled and the cell becomes unexcitable. In one case, this effect was reversed by about one hour after drug injection. 13. Intracellular recordings from some unidentified, unexcitable cells in M/:uller's organ reveal small amplitude (1–4 mV), transient and sustained potentials. The sustained potentials are negative going and adapting. The transient potentials are biphasic with the negative phase leading. In most cases, the relative amplitude of each phase of the transient potentials systematically varies with the amplitude of the sustained potential (Fig. 11). 14. By analogy with recordings from identified attachment cells in the crista acustica of tettigoniids and with transepithelial recordings from insect epidermal sensilla, the recordings of sensory events from unexcitable cells in Müller's organ are attributed to penetrations of attachment cells. 15. Based on these initial intracellular recordings from receptor cells, a proposal for the functional organization of the locust auditory sensillum is presented.

Notes: Summary 1. Single unit recording from the oesophageal connectives was used to characterise the physiological responses to monaural stimulation of ascending auditory interneurons in the tettigoniidCaedicia simplex. 2. In terms of characteristic patterns of spike discharge, ascending auditory interneurons have been classified as tonic, phasic-tonic or phasic (Fig. 1). 3. According to suprathreshold, isoresponse criteria, tonic interneurons either are broadlytuned between 10–16 kHz or are more narrowlytuned to a single sound frequency below 10 kHz (Fig. 2A). All tonic interneurons recorded have a roll-off in sensitivity of 20–40 dB/octave above and below their frequencies of maximum sensitivity. This corresponds with the roll-offs applicable to primary afferent fibres. 4. Most phasic-tonic interneurons display uniform sensitivity to one of three different frequency bands (about 3 kHz in width) in the range 10-18 kHz (Fig. 2B). These three classes of phasictonic interneuron have roll-off in sensitivity of more than 50 dB/octave for sound frequencies below their range of maximum sensitivity. 5. In contrast, a distinct class of phasic-tonic interneuron is sharply-tuned to 16 kHz, the species' call frequency (Fig. 3 A). The roll-off in sensitivity of this class of interneuron 40–50 dB/octave for frequencies above and greater than 50 dB/octave for frequencies below 16 kHz. For frequencies below 16 kHz, this roll-off in sensitivity exceeds that of primary afferent fibres by a factor of two (Fig. 3B). 6. Phasic interneurons each are tuned to a single sound frequency in the range 10–16 kHz and have roll-off's in sensitivity of 40–50 dB/octave above and 20–30 dB/octave below their frequency of maximum sensitivity (Fig. 2C). 7. For tonic interneurons, a positive, approximately linear relationship exists between sound intensity and spike response that is similar for different sound frequencies (Fig. 4 A). 8. Phasic-tonic interneurons have a complex intensity-response characteristic that is dependent on sound frequency (Fig. 4B). For frequencies within or above the range of maximum sensitivity, the response increases at a rate of 6 spikes/20 dB, saturates at 10–12 spikes/stimulus and may then decline to as little as 2–3 spikes/stimulus at the higher sound intensities. For frequencies below the band of highest sensitivity the gradient, maximum response and dynamic range of the intensity characteristic progressively decrease. 9. Phasic interneurons produce a maximum of 2–4 spikes/stimulus and, as with tonic interneurons, the intensity characteristic is independent of sound frequency (Fig. 4C). 10. Two-tone experiments demonstrate that phasic-tonic interneurons are inhibited by a sensory response to sound frequencies below their band of highest sensitivity (Fig. 5) and that the onset of this inhibition is delayed by 20 ms, relative to that of excitation (Fig. 6). Similar two-tone experiments conducted on primary afferent fibres demonstrate that no such inhibition occurs at the periphery (Fig. 7). 11. Based on idealized frequency and intensity characteristics of primary afferent fibres (Fig. 8) derived from empirical data (Oldfield 1982, 1983) and on the characteristics of monaurally-stimulated ascending interneurons, a simple model of integration is developed, in which the response of each class of ascending interneuron is attributed to the sum of the inferred excitatory and inhibitory inputs provided by an array of separately-tuned primary afferent fibres. The model accurately predicts the responses of ascending auditory interneurons inC. simplex for the monaural case (Fig. 9).

Notes: Summary Cystosoma saundersii is a cicada in which the male is specialised for the production of low frequency (800 Hz) sound. The basic anatomical and physiological features of its auditory system are examined in males and females. 1. Paired auditory (chordotonal) organs are located in auditory capsules on the second abdominal segment (Figs. 6, 9 A). Each auditory organ is suspended between a distal attachment horn and a proximal apodeme (Figs 5B, 7A, B) connected to a complex tympanum (Figs. 4, 10). Male and female tympana are approximately equal in area. Male tympana are loaded (Figs. 5A, 7C) with masses of amorphous material. 2. Both tympana are coupled into a single abdominal air chamber which, in males, almost fills the enlarged abdomen, but in females occupies a restricted volue within the abdomen (Fig. 8). 3. Male and female auditory organs are both sharply tuned to the frequency of the species' song at 800 Hz (Figs. 11, 12). 4. Each female auditory organ exhibits a directional sensitivity which is limited to frequencies near 800 Hz but males lack directional hearing (Figs. 13, 14). 5. The enlarged male abdomen acts as an omnidirectional receiver of sound at frequencies near 800 Hz, which results in an augmented sound pressure at the inside surfaces of the tympana (Figs. 15, 16). However, male and female absolute sensitivities at the hearing optima are similar (Figs. 11, 12) which indicates reduced sensitivity of the male tympana. 6. We conclude that the auditory system ofC. saundersii is finely adapted to the requirements of intraspecific acoustic communication with low frequency sound.

Notes: Summary 1. Physiological characteristics of single, primary auditory units have been examined in a member of the Orthopteran family Stenopelmatidae. 2. Individual units are tuned more sharply than the whole auditory organ. Units have peaks of sensitivity within the bandwidth described by the summed threshold curve of the auditory organ. 3. Some units display one or two additional peaks of sensitivity at higher frequencies, which may not be harmonically related to the major peak. 4. Units respond to tones with a tonic discharge in which an initial, partial adaptation may occur. Stimulus intensity is coded in terms of spike rate and latency and units display typical, sigmoidal input-output curves. High intensity suppression of the response is sometimes observed. 5. Repetition rates of brief sound pulses that units can follow are limited by mechanical and/or physiological aspects of the sensory process. Minimum latency of response is of the order of 13 ms.

Notes: Summary 1. Intracellular recordings from locust auditory receptors reveal discrete, subthreshold depolarizations of the cell membrane, with variable amplitude up to about 5 mV, that are the first electrical sign of mechanosensory transduction (Fig. 1). 2. Hyperpolarization of the receptor cell membrane causes an increase in the amplitude of the discrete depolarizations without suppressing their occurrence (Fig. 2). 3. In the absence of acoustic stimuli, the subthreshold potentials appear to occur spontaneously at random. The mean frequency of the recorded potentials varies widely between cells (Figs. 1, 2, 3). 4. The potentials also occur in response to sound stimuli. The probability of a response following a brief tone increases from near zero to 1.0 with increasing intensity of the tone (Fig. 4). The number of potentials occurring during an extended tone initially increases as the stimulus intensity is increased (Fig. 5) and typically, the discrete potentials superimpose to form a graded receptor potential (Fig. 6), as occurs in visual receptor cells. 5. In both a train of discrete potentials and a sustained depolarization, the amplitude may progressively decline from its initial peak, indicative of adaptation. 6. Receptor potentials produced by weak stimulation are characteristically noisy. Amplitude and frequency analyses of the membrane voltage noise recorded during sound stimulation suggests that the noise results from the superposition of discrete depolarizations, consistent with direct observations. 7. The first electrical sign of transduction in locust auditory receptors is a quantal membrane voltage response. By analogy with vision, it is suggested that discrete mechano-chemical events may lead to activation of ionic conductance channels in receptor cell membranes, possibly via an intermediate biochemical process.