Hans Ulrich Kleindienst

Auditory behavior of the cricket. III: Tracking of male calling song by surgically and developmentally one-eared females, and the curious role of the anterior tympanum

Summary1.Many one-eared female crickets (Gryllus campestris andGryllus bimaculatus), whether the loss is due to surgery or to developmental accident, can maintain characteristic, stable courses with respect to the direction of male calling song, when tested on the Kramer spherical tread-mill. The error angles are usually less than 90°, so that Regens (1924) remark about the success of such females in finding singing males is supported.2.Some females with developmental unilateral hearing deficit, confirmed both histologically and by sparing of tracking after removal of the suspect leg, track nearly as accurately as normal animals with two ears.3.Experiments in which tympana were immobilized with wax, whether tracking behavior or interneuron responses were monitored, show that the anterior tympanum — considered for some time to be irrelevant to hearing — mediates appreciable sound input to the auditory receptors, at least when the posterior tympana are blocked.4.The above results resolve two current paradoxes regarding comparison of tympanum immobilization in behavior with the mechanics of receptor excitation:First, because even unambiguously one-eared animals can maintain stable sound-oriented courses, such tracking performance with waxed tympana does not argue that total tympanal immobilization spares some auditory function of that ear (cf. Schmitz et al. 1983). The argument assumes that tracking would not be expected if one ear were silenced; the assumption is evidently false.Second, it has been unclear why waxing of both posterior tympana raises tracking threshold only ca. 20 dB (Schmitz 1983) whereas the tympanalmechanics studies of Kleindienst et al. (1983) have suggested a much greater deficit. Our finding that one must wax the anterior tympana as well, in order to produce deficit greater than ca. 20 dB, clarifies the situation. That is, in the biophysical experiments both tympana of the leg were immobilized by the procedures used (pressure matching and water immersion), whereas in most current behavioral tympanum-waxing experiments (but not in those of Bailey and Thomson 1977) the anterior tympana have been ignored.5.A novel behavioral effect was observed with all four tympana blocked. Thresholds for orientation were ca. 90–100 dB, but in every case the animals tended to walk away from the loudspeaker.6.The search for an explanation of one-eared tracking leads us to analogies with the recovery from imbalance following such surgery as hemilabyrinthectomy in vertebrates. A ‘phantom tympanum’, on the side with deficit, could in principle participate in corrective tracking, by the usual notions of bilateral comparison.

The mechanics of stridulation of the cricketGryllus campestris

SummaryDetails in the stridulatory movement ofGryllus campestris were investigated using an improved high resolution miniature angle measurement system. The following results were obtained: During the closing (sound producing) stroke, the speed of the plectrum always has the same value (within measuring accuracy) at a given position. Plectrum speed is directly proportional to tooth spacing, which is known to vary along the file. The only exception to this rule were occasions when closing velocities of precisely 2 times the standard value were found. In between values were never recorded. While temperature has a large effect on the opening speed and duration, the closing speed has a very smallQ10 (0.07) which is equal to theQ10 of the resonance frequency of the harp. When the harps are removed, the proportionality between tooth spacing and scraper velocity is lost; the velocity is much increased (up to 3-fold) and the variance of the speed is enhanced 5-fold.These results are discussed with respect to 3 hypothetical models explaining the function of the sound generator system. The model describing the cricket sound generator as a clockwork with an escapement system is capable of accommodating all experimental data without any extra assumptions.

Morphological and physiological changes in central auditory neurons following unilateral foreleg amputation in larval crickets

Summary1.In view of the surprising recent demonstration that developmentally one-eared female crickets can track sound sources (Huber et al. 1984), we have looked for correlates in the morphological and physiological properties of auditory interneurons of these animals. One foreleg was amputated in the 3rd/4th or penultimate (8/9th) larval instar; in both cases the leg regenerated without developing a functional ear. In the adult stage, these animals were studied first for their phonotactic behavior and then by intracellular recording and staining; three types of auditory interneurons in the prothoracic ganglion were identified: the omega neuron ON1, and the ascending neurons AN1 and AN2.2.Of these three neuron types, those that normally receive excitatory input from the side now deafferented send dendrites across the midline of the ganglion, along specific pathways, to end in the auditory neuropil of the intact side (Figs. 1–4).3.The new connections are functional, as shown by the responses of the neurons to synthesized calling songs presented to the remaining ear. With respect to the copying of chirp structure, threshold curves and intensity characteristics, these neurons respond like cells in intact animals that are presented with the same stimulus on the side ipsilateral to the main input region of the neurons (Figs. 2–4). The implication is that in animals with one ear missing, functional pathways within the central nervous system are reorganized, resulting in better orientation of one-eared animals.

Analysis of the Cricket Auditory System by Acoustic Stimulation Using a Closed Sound Field

SummaryA closed sound field system for independent stimulation of both cricket hearing organs is described. The system was used to measure acoustic parameters of the peripheral auditory system inGryllus campestris and to analyze inhibitory responses of the omega cell, a segmental auditory interneuron in the prothoracic ganglion.1.Best sound transmission in the tracheal pathway occurs at 5 kHz. Closing of the prothoracic spiracles results in increased sound transmission but does not influence the frequency of best transmission in most animals (Fig. 6 B). Sound transmission is modulated by abdominal contractions associated with the respiratory cycle (Fig. 7).2.AttenuationΔ and phase shift ϕ in the tracheal pathway have been determined for the frequency range of 2 to 10 kHz in animals with closed spiracles.Δ shows a minimum at 5 kHz and ϕ increases almost linearly with frequency (Fig. 11).3.Sound components acting on each side of the large tympanal membrane form a resultant sound pressure based on linear superposition. This resultant sound pressure represents the effective stimulus of the auditory sense organ (Fig. 12).4.The response of the omega cell is dependent upon both intensity and relative phase of sound signals applied to the tympanal membranes (Fig. 10).5.At 5 kHz, the response of the omega cell decreases linearly with increasing contralateral (inhibitory) stimulus intensity over a wide range of intensities. The latency between stimulus onset and response is nearly independent of contralateral inhibition (Figs. 15 and 16).6.Response (spike number) differences between an omega cell and its complementary mirror image cell due to different stimulus intensities at both ears are enhanced by the neuronal mechanism of contralateral inhibition. In one animal the gain in spike number difference at 5 kHz was calculated to be 60% relative to the response difference when contralateral inhibition was disabled.7.Evidence for a low frequency (f≦2 kHz) ipsilateral inhibition of the omega cell is presented (Fig. 17).

Tympanal membrane motion is necessary for hearing in crickets

Summary1.Sound guided through the tracheal tube to the internal tracheal spaces in the region of the cricket ear is capable of eliciting auditory neural responses in the prothoracic ganglion if the tympanal membrane is allowed to vibrate freely. If the tympanal membrane motion is prevented mechanically neural responses are abolished (Fig. 3) whereas the sound pressure in the tracheal air spaces behind the tympanum is increased.2.If the motion of the tympanum, as measured with laser vibrometry, is prevented by adjusting the internal and external sound pressure, then neural responses cease simultaneously (Fig. 5).3.These findings demonstrate that motion of the large tympanum is a necessary requisite in the sound transduction process of the cricket ear.

The role of the medial septum in the acoustic trachea of the cricket Gryllus bimaculatus

The auditory organs of the cricket which are situated in the front legs are joined together by a large transverse trachea which decisively influences their directional characteristics. The transverse trachea is medially divided by a septum. The importance of this septum for the localization of a sound source was tested by means of behavioural experiments in which the phonotactic movements of intact Gryllus bimaculatus females were compared quantitatively with those of the same specimen after perforation of the septum. The septal perforation does not noticeably influence locomotion in the absence of acoustic stimuli but selectively changes essential characteristics of phono taxis: 1) The animals walk in less straight lines. The oscillations around the mean course, typical of phonotaxis, are increased in amplitude, while the frequency decreases. 2) Course deviations from the direction of the sound source become more pronounced. 3) The threshold for phonotaxis is raised by about 10 dB. 4) Both the speed at which the animals walk and the proportion of time during which they are mobile are reduced. The results are discussed in relation to the role of the septum in the mechanism of sound localization, and with regard to its possible importance for the recognition of acoustic patterns.

Acoustic orientation in adult, female crickets (Gryllus bimaculatus de Geer) after unilateral foreleg amputation in the larva

SummaryInGryllus bimaculatus females one foreleg was amputated at the coxa-trochanter joint in the 2nd, 4th or 8th/9th larval instar. A leg of up to normal length is regenerated (Fig. 1) but it lacks a functional ear. In spite of the, usually shorter, regenerated foreleg, the adult one-eared crickets show no impairments in walking when tested on a locomotion compensator. Without sound they walk erratically and most of them weakly circle towards the intact side (Fig. 2).With calling song presentation three response types can be distinguished:tracking (Fig. 3A), ‘hanging on’ (Fig. 3B) or continuouscircling towards the intact side (Fig. 3C, D). Turning tendencies in monaurals increase with song intensity and exceed those of intact and bilaterally operated animals (Fig. 4). Course deviations towards the intact side also slightly increase with intensity (Fig. 5). Course stability is reduced compared to that of intact animals but exceeds that of bilaterally operated crickets (Figs. 5, 6). It is best at 60 dB and deteriorates at higher sound intensities (Fig. 6). The percentage of monaurals tracking or ‘hanging on’ decreases with increasing intensity (Fig. 7B). Tracking is established in most animals but it is limited to a narrow intensity range (Fig. 7A, C). Apart from an increased percentage of tracking after early operations (Fig. 7D), there are no prominent changes in orientational parameters with the date of foreleg amputation.Reamputation of the regenerated leg in the adult monaurals does not significantly impair acoustic orientation (Figs. 8, 9), but occlusion of the ipsilateral prothoracic spiracle does (Figs. 10, 11).An attempt is made to correlate the behavioral performance with the activity of auditory interneurons which have undergone morphological and physiological changes (Fig. 12).

Structure, geography and origin of dialects in the traditive song of the Forest weaver Ploceus bicolor sclateri in Natal, S. Africa

From a 21-year-long combined field and laboratory study we describe the general song structure and local song dialects of this species. These dialects differ in syntactic and phonological charateristics. Within its first 24 months the individual learns a song from its parents and keeps that song constant throughout life. In free-living populations dialects remained constant over the total study period. We could exclude that the dialects are an acoustic window phenomenon. We found individual song variations within dialects which suggest a derivation of local dialects from family-specific songs, enhanced by man-induced habitat fragmentation.

Sound Localization in Intact and One-Eared Crickets

SummaryIntact and one-eared crickets,Gryllus bimaculatus, were tested for phonotactic behavior in a closed-loop and an open-loop situation and for related physiological characteristics of an identified auditory neuron pair, the left and the right AN2.Intact animals that performed phonotaxis in the closed-loop condition showed intended turning tendencies in the open-loop condition that correlated with the directional characteristics of their AN2s (Figs. 1–3).Animals in which one foreleg had been amputated during postembryonic development (one-eared regenerates) were classified according to their phonotactic performance as tracking or unoriented animals. The ability of one-eared regenerates to track a sound source was closely correlated with the direction of turning tendencies in the open-loop behavior and to specific features of their AN2 pair (Figs. 4–6).Some animals with one foreleg amputated as adults (one-eared amputees) perform stable phonotactic walking. Their open-loop behavior, however, is different from that of the tracking one- eared regenerates (Fig. 7).One-eared amputees showed stable phonotactic walking when calling song was presented from above and the sound intensity was varied according to the actual walking angle of the animal. The only orientational cue under this condition is the difference of sound intensity at different walking directions (Figs. 8–11).Different mechanisms are discussed for sound localization in one-eared regenerates and one- eared amputees based on turning tendencies which depend on the instantaneous stimulus intensity or on the intensity change between successive stimuli.

Descending neurons in the cricket's suboesophageal ganglion with activity modulated by localized body cooling

Despite the fact that thermosensitivity of the central nervous system of insects is believed to affect many aspects of behavior [1] the effects of temperature on identified central neurons have been explored only rarely [2]. In a recent study [3] heterogeneity among suboesophageal neurons of crickets in terms of response to temperature variations was reported. Here we describe one class of those neurons in detail. Experiments were performed on adult male Gryllus bimaculatus De Geer bred in laboratory cultures at 24 ~ The crickets were mounted on a holder and the suboesophageal ganglion (SOG) was exposed for intracellular recording by dorsal dissection. Head temperatures between 8 and 32 ~ were produced by perfusing the head with Ringer solution of the appropriate temperature. Inevitably, the temperature of the surrounding tissues followed to some extent the temperature changes in the head. However, such effects were confined to the first thoracic segment and the proximal half of the antennae, the rest of the body remaining at ambient temperature. All temperature measurements were made using thermocouples with rapid response time constant, and abdominal respiratory movements were monitored with a photosensor. The morphology of the identified neurons within the SOG is presented in Fig. 1 (insets). Their somata are located ventrally and their axons descend in the left or right connective but were stained only as far as the prothoracic ganglion. At all tested head temperatures activity correlated with abdominal respiratory pumping was observed (Fig. 2). The neurons were also excited by stimulation of the cerci with low-frequency air vibration (for method see [4]) and by visual stimulation (pocket lamp flashes). The most marked response to thermostimulation was an increase in spike frequency during a temperature drop from 20 to about 10 ~ The maximum firing rate occurred somewhat above the lowest temperature (Fig. 1 A). The response was adapting but at lowest steady state temperature the firing rate was still higher than at 20 ~ (Fig. 2A, B). The response to temperature decrease from 20 to about 10 ~ was much less pronounced or even totally absent in cells with low background activity at 20 ~ but was substantially increased when depolarizing current was injected into the neurons (Fig. 1 B, C). Minor changes of discharge rates were also observed in depolarized cells when temperature was decreased from 32 to 20 ~ (arrows in Fig. 1 B, C).