Central projection of auditory receptors in the prothoracic ganglion of the bushcricket Psorodonotus illyricus (tettigoniidae): Computer-aided analysis of the end branch pattern

The projection patterns of morphologically and functionally identified auditory and auditory-vibratory receptor cells of receptor organs (the crista acustica and the intermediate organ) in the foreleg of the tettigoniid Psorodonotus illyricus, were investigated with combined recording and staining techniques, and subsequent histological examination and morphometric measurements. With the application of a computer program (AutoCAD), three-dimensional reconstructions of the axon end branches of receptor cells within the neuropile of the anterior Ring Tract (aRT) were made, in order to determine, the entire shape of each, the pattern and density of the end branches, and the positions of the target areas within the auditory neuropile. Clear differences for different functional types of receptors were found. 1994 John Wiley & Sons, Inc.     

Functional morphology of bushcricket ears: comparison between two species belonging to the Phaneropterinae and Decticinae (Insecta,Ensifera)

Summary The morphology of the complex tibial organs in the forelegs of two bushcricket species belonging to the Phaneropterinae and Decticinae (Tettigoniidae) is described comparatively. In both species the tibial organs are made up of the subgenual organ, the intermediate organ and the crista acustica; the latter are parts of the tympanal organs and serve as auditory receptors. The very thin tympana in the forelegs ofPholidoptera griseoaptera (Decticinae) are protected by tympanal covers whereas inLeptophyes punctatissima (Phaneropterinae) the tympana are thicker and fully exposed. The overall auditory sensitivity ofL. punctatissima is lower and the sensitivity maximum of the hearing threshold lies at higher frequencies compared toP. griseoaptera. The number of scolopidia in the three scolopale organs and the dimensions of parts of the sound conducting system differs in the two species. In the crista acustica ofL. punctatissima a higher number of scolopidia is distributed in a smaller range than inP. griseoaptera; the scolopidia are especially concentrated in the distal part. Morphometrical analyses indicate that the dimensions of the spiracles, the acoustic trachea and the tympana determine the overall auditory sensitivity and that the arrangement of the scolopidia and the dimensions of structures in the crista acustica affect the frequency tuning of the hearing threshold.     

Functional morphology and development of tibial organs in the legs I,II and III of the bushcricketEphippiger ephippiger (Insecta,Ensifera)

Summary The anatomy of the complex tibial organs in the pro-, meso- and metathoracic legs of adults and larvae of the bushcricketEphippiger ephippiger is described comparatively. The subgenual organ and the intermediate organ are differentiated in the same way in legs I, II and III; the anatomy of the crista acustica and the tracheal morphology are significantly different. The final number of scolopidia in the tibial organ of each leg is present at the time of hatching. In the subgenual organ, the number of scolopidia is the same in all legs; in the intermediate organ, and especially in the crista acustica, the number of scolopidia decreases from leg I to legs II and III. In the first larval instar, the morphology of the tibia, the course of the trachea and the anatomy of accessory structures are developed in the same way in each leg. The specific differentiations forming the auditory receptor organ in leg I, such as the acoustic trachea, the tympana and tympanal cavities, develop step by step in subsequent instars. The auditory threshold recorded from the tympanal nerve in the prothoracic leg of adults is remarkably lower than in the meso- and metathoracic legs. Morphometrical analyses of structures that are suggested to play a role in stimulus transduction on scolopidia of the crista acustica reveal significant differences in the three legs.     

Postembryonic development of the complex tibial organ in the foreleg of the bushcricket Ephippiger ephippiger (Orthoptera,Tettigoniidae)

Summary The postembryonic development of the morphology and anatomy of the complex tibial organ in the foreleg of the bushcricket Ephippiger ephippiger is described. All the receptor cells are present in the subgenual organ, the intermediate organ and the crista acustica in the 1st larval instar. Generally, even in the 1st instar, the arrangement of the scolopidia in the three organs resembles the adult structure. The acoustic trachea, the tympana, the tympanal covers and the acoustic spiracle develop step by step in subsequent instars. The acoustic trachea resembles the adult structure for the first time in the 4th instar, although its volume is still small. The auditory threshold curves recorded from the tympanal nerve in instars 4, 5 and 6 show the same frequency maxima as those in the adult. The overall sensitivity significantly increases after the final moult. The dimensions of structures that lie within the crista acustica and that are probably involved in stimulus transduction and in frequency tuning have been analysed. The dorsal wall of the anterior trachea, the tectorial membrane and the cap cells have similar dimensions, especially in the last three instars and in adults.     

Behavioral detection of acoustic particle motion by a teleost fish (Astronotus ocellatus): sensitivity and directionality

The physiology and morphology of auditory interneurons of a fly, the parasitoid Therobia leonidei, are described for the first time. 1. The hearing threshold has been determined with summed recordings of the neck connective. Females are most sensitive in a frequency range from 16 to 40 kHz (thresholds: around 45 dB SPL). This broad hearing range matches with the peak frequencies of the song spectra of host bushcricket species. Male flies are 10–20 dB less sensitive than females. 2. The sensory cells of the prosternal tympanal organ of T. leonidei project into the thoracico-abdominal ganglion complex with arborizations in all three thoracic neuromeres. 3. Three types of ascending auditory interneurons were identified by their morphology and response properties. These have arborizations in all three thoracic neuromeres and terminate soma-contralaterally in the brain. At least three other neuron types were also identified according to response properties alone. The neurons show similar spectral tuning but different sensitivities.     

Physiology and tonotopic organization of auditory receptors in the cricketGryllus bimaculatus DeGeer

Summary Physiological recordings were obtained from identified receptors in the tympanal organ ofGryllus bimaculatus. By immersing the prothoracic leg in Ringer solution and removing the anterior tympanic membrane the auditory receptors were exposed without significantly altering the frequency response of the auditory organ (Fig. 1). Each receptor was tuned to a specific sound frequency. For sound frequencies below this characteristic frequency the roll-off in sensitivity decreased from 20–30 dB/octave to 10–15 dB/octave as the characteristic frequency of receptors increased from 3–11 kHz (Fig. 4A). For each individual receptor the slope, dynamic range and maximum spike response were similar for different sound frequencies (Fig. 9A). The receptors were tonotopically organized with the characteristic frequency of the receptors increasing from the proximal to the distal end of the array (Figs. 5, 6). Several receptors had characteristic frequencies of 5 kHz. These receptors were divided into two groups on the basis of their maximum spike response produced in response to pure tones of increasing intensity (Fig. 7). Independent of the tuning of the receptor no two-tone inhibition was observed in the periphery, thus confirming that such interactions are a property of central integration.     

Experimental and Theoretical Explorations of Traveling Waves and Tuning in the Bushcricket Ear

The ability to detect airborne sound is essential for many animals. Examples from the inner ear of mammals and bushcrickets demonstrate that similar detection strategies evolved in taxonomically distant species. Both mammalian and bushcricket ears possess a narrow strip of sensory tissue that exhibits an anatomical gradient and traveling wave motion responses used for frequency discrimination. We measured pressure and motion in the bushcricket ear to investigate physical properties, stiffness, and mass, which govern the mechanical responses to sound. As in the mammalian cochlea, sound-induced fluid pressure and motion responses were tonotopically organized along the longitudinal axis of the crista acustica, the bushcricket’s hearing organ. The fluid pressure at the crista and crista motion were used to calculate the acoustic impedance of the organ-bounded fluid mass (Z_mass). We used a theoretical wave analysis of wavelength data from a previous study to predict the crista acustica stiffness. The wave analysis also predicts Z_mass, and that result agreed reasonably well with the directly measured Z_mass, lending support to the theoretical wave analysis. The magnitude of the crista stiffness was similar to basilar membrane stiffness in mammals, and as in mammals, the stiffness decreased from the high-frequency to the low-frequency region. At a given location, the stiffness increased with increasing frequency, corresponding to increasing curvature of the traveling wave (decreasing wavelength), indicating that longitudinal coupling plays a substantial role in determining crista stiffness. This is in contrast to the mammalian ear, in which stiffness is independent of frequency and longitudinal coupling is relatively small.     

Morphology and physiology of the prosternal chordotonal organ of the sarcophagid fly Sarcophaga bullata (Parker)

The anatomy and the physiology of the prosternal chordotonal organ (pCO) within the prothorax of Sarcophaga bullata is analysed. Neuroanatomical studies illustrate that the approximately 35 sensory axons terminate within the median ventral association centre of the different neuromeres of the thoracico-abdominal ganglion. At the single-cell level two classes of receptor cells can be discriminated physiologically and morphologically: receptor cells with dorso-lateral branches in the mesothoracic neuromere are insensitive to frequencies below approximately 1 kHz. Receptor cells without such branches respond most sensitive at lower frequencies. Absolute thresholds vary between 0.2 and 8m/s(2) for different frequencies. The sensory information is transmitted to the brain via ascending interneurons. Functional analyses reveal a mechanical transmission of forced head rotations and of foreleg vibrations to the attachment site of the pCO. In summed action potential recordings a physiological correlate was found to stimuli with parameters of leg vibrations, rather than to those of head rotation. The data represent a first physiological study of a putative predecessor organ of an insect ear.     

Lateralization of Travelling Wave Response in the Hearing Organ of Bushcrickets

Travelling waves are the physical basis of frequency discrimination in many vertebrate and invertebrate taxa, including mammals, birds, and some insects. In bushcrickets (Tettigoniidae), the crista acustica is the hearing organ that has been shown to use sound-induced travelling waves. Up to now, data on mechanical characteristics of sound-induced travelling waves were only available along the longitudinal (proximal-distal) direction. In this study, we use laser Doppler vibrometry to investigate in-vivo radial (anterior-posterior) features of travelling waves in the tropical bushcricket Mecopoda elongata. Our results demonstrate that the maximum of sound-induced travelling wave amplitude response is always shifted towards the anterior part of the crista acustica. This lateralization of the travelling wave response induces a tilt in the motion of the crista acustica, which presumably optimizes sensory transduction by exerting a shear motion on the sensory cilia in this hearing organ.     

Effect of temperature on auditory receptor functions in bushcrickets (Orthoptera, Tettigonioidea)

By electrophysiological methods, effect of temperature on bushcricket tympanal organ functions was studied. Activity of auditory receptors was recorded intracellularly in the 5th nerve of I thoracic ganglion in Tettigonia cantans, Metrioptera roeselii, M. bicolor, Platycleis albopunctata, Pholidoptera griseoaptera, and Phaneroptera falcata. The temperature was changed in the range from 17 to 34 degrees C. Heating of the tympanal organ to 30-32 degrees C led to a decrease of impulse amplitude, shortening of their duration, an increase of sensitivity, of the burst instantaneous frequency, and of the number of impulses in responses as well as to a decrease of latent periods (LP) of receptor reaction. The optimal frequency in all studied cells did not change, although range of perceived frequencies was enlarged. The frequency threshold curve of receptors either was shifted down along the ordinate scale without changes of its shape or the thresholds at various frequencies decreased non-uniformly. Thus, the obtained data indicate the absence of changes in the frequency tuning of the auditory receptors with changes of temperature.     

Morphology and physiology of auditory and vibratory ascending interneurones in bushcrickets

Auditory/vibratory interneurones of the bushcricket species Decticus albifrons and Decticus verrucivorus were studied with intracellular dye injection and electrophysiology. The morphologies of five physiologically characterised auditory/vibratory interneurones are shown in the brain, subesophageal and prothoracic ganglia. Based on their physiology, these five interneurones fall into three groups, the purely auditory or sound neurones: S-neurones, the purely vibratory V-neurones, and the bimodal vibrosensitive VS-neurones. The S1-neurones respond phasically to airborne sound whereas the S4-neurones exhibit a tonic spike pattern. Their somata are located in the prothoracic ganglion and they show an ascending axon with dendrites located in the prothoracic, subesophageal ganglia, and the brain. The VS3-neurone, responding to both auditory and vibratory stimuli in a tonic manner, has its axon traversing the brain, the suboesophageal ganglion and the prothoracic ganglion although with dendrites only in the brain. The V1- and V2-neurones respond to vibratory stimulation of the fore- and midlegs with a tonic discharge pattern, and our data show that they receive inhibitory input suppressing their spontaneous activity. Their axon transverses the prothoracic ganglion, subesophageal ganglion and terminate in the brain with dendritic branching. Thus the auditory S-neurones have dendritic arborizations in all three ganglia (prothoracic, subesophageal, and brain) compared to the vibratory (V) and vibrosensitive (VS) neurones, which have dendrites almost only in the brain. The dendrites of the S-neurones are also more extensive than those of the V-, VS-neurones. V- and VS-neurones terminate more laterally in the brain. Due to an interspecific comparison of the identified auditory interneurones the S1-neurone is found to be homologous to the TN1 of crickets and other bushcrickets, and the S4-neurone also can be called AN2. J. Exp. Zool. 286:219-230, 2000.     

Processing of simple and complex acoustic signals in a tonotopically organized ear

Processing of complex signals in the hearing organ remains poorly understood. This paper aims to contribute to this topic by presenting investigations on the mechanical and neuronal response of the hearing organ of the tropical bushcricket species Mecopoda elongata to simple pure tone signals as well as to the conspecific song as a complex acoustic signal. The high-frequency hearing organ of bushcrickets, the crista acustica (CA), is tonotopically tuned to frequencies between about 4 and 70 kHz. Laser Doppler vibrometer measurements revealed a strong and dominant low-frequency-induced motion of the CA when stimulated with either pure tone or complex stimuli. Consequently, the high-frequency distal area of the CA is more strongly deflected by low-frequency-induced waves than by high-frequency-induced waves. This low-frequency dominance will have strong effects on the processing of complex signals. Therefore, we additionally studied the neuronal response of the CA to native and frequency-manipulated chirps. Again, we found a dominant influence of low-frequency components within the conspecific song, indicating that the mechanical vibration pattern highly determines the neuronal response of the sensory cells. Thus, we conclude that the encoding of communication signals is modulated by ear mechanics.     

Complex tibial organs in fore-, mid-, and hindlegs of the bushcricket Gampsocleis gratiosa (Tettigoniidae): Comparison of morphology of the organs

The structure of the complex tibial organs in the fore-, mid-, and hindlegs of the East Asian bushcricket Gampsocleis gratiosa (Tettigoniidae, Decticinae) is described comparatively. In each leg the tibial organs consist of three scolopale organs: the subgenual organ, the intermediate organ, and the crista acoustica. Only in the forelegs are the tibial organs differentiated as tympanal organs, and sound transmitting structures (acoustic trachea, tympana, and tympanal covers) are present. The morphology of the tracheae in the mid- and hindlegs is significantly different from that found in the forelegs. The number of scolopidia in the subgenual organ is highest in the midleg and lowest in the foreleg; in the intermediate organ the number is also highest in the midleg, and the fore- and hindleg contain 40% fewer scolopidia. In the crista acoustica, the number of scolopidia decreases from, the fore- to the mid- and hindlegs. The morphology and the dimensions of the scolopidia and the attachment structures within the crista acoustica of the mid- and hindlegs differ strongly from those in the foreleg. The results indicate that, in addition to the presence of a sound transmitting system, the specific differentiations within the crista acoustica are important for the high auditory sensitivity of the tibial organs in the forelegs. © 1994 Wiley-Liss, Inc.     

Central projections of fibers in the auditory and tensor nerves of cicadas (Homoptera: Cicadidae)

Summary The auditory and tensor nerves of cicadas are mixed nerves containing both afferent and efferent elements. In 17-year cicadas, and in Okanagana rimosa, the auditory nerve contains afferents from body hairs, from the detensor tympani-chordotonal organ, and some 1300–1500 afferents from the hearing organ. Within the fused metathoracic-abdominal ganglionic complex the receptors from both the auditory and tensor nerves form a neuropilar structure that reveals the metameric organization of this complex. A few fibers run anteriorly, projecting into the meso and prothoracic ganglia. Within the ganglionic complex a division of auditory nerve afferents into a dense intermediate and a more diffuse ventral neuropile is observed. In addition, a dorsal motor neuropile is outlined by arborizations of the timbal motor neuron. This neuron is one of several efferent cell types associated with the auditory nerve, and there is an indication that several efferent fibers innervate the timbal muscle. There is anatomical evidence for a possible neuronal coupling between the bilaterally symmetrical large timbal motor neurons. In general, central projections from the auditory and tensor nerves support evidence of a structural layering within the CNS of insects.     

Regeneration of the projection and synaptic connections of tympanic receptor fibers of Locusta migratoria (Orthoptera) after axotomy

The tergite nerve N6 of the first abdominal segment of the locust Locusta migratoria contains receptor fibers, from the tympanic organ, and hair sensilla as well as motoric axons. The nerve was axotomized in nymphal instars or adults, and the regeneration of nerve fibers was studied. The sensory fibers regrow and regenerate their projection pattern within the central nervous system. They recognize their specific neuropile areas even after entering the ganglion through different pathways. The receptor fibers of the tympanic organ reestablish synaptic connections to auditory interneurons, even though the physiological characteristics of the interneurons are not fully restored. This regenerative capability contrasts with the lack of regeneration of peripheral structures in locusts, but supports the described plasticity in the auditory system of monaural locusts (Lakes, Kalmring, and Engelhard, 1990). The motor fibers do not regenerate nerves innervating muscles of the body wall.     

Spatial organization of tettigoniid auditory receptors: Insights from neuronal tracing

The auditory sense organ of Tettigoniidae (Insecta, Orthoptera) is located in the foreleg tibia and consists of scolopidial sensilla which form a row termed crista acustica. The crista acustica is associated with the tympana and the auditory trachea. This ear is a highly ordered, tonotopic sensory system. As the neuroanatomy of the crista acustica has been documented for several species, the most distal somata and dendrites of receptor neurons have occasionally been described as forming an alternating or double row. We investigate the spatial arrangement of receptor cell bodies and dendrites by retrograde tracing with cobalt chloride solution. In six tettigoniid species studied, distal receptor neurons are consistently arranged in double‐rows of somata rather than a linear sequence. This arrangement of neurons is shown to affect 30–50% of the overall auditory receptors. No strict correlation of somata positions between the anterio‐posterior and dorso‐ventral axis was evident within the distal crista acustica. Dendrites of distal receptors occasionally also occur in a double row or are even massed without clear order. Thus, a substantial part of auditory receptors can deviate from a strictly straight organization into a more complex morphology. The linear organization of dendrites is not a morphological criterion that allows hearing organs to be distinguished from nonhearing sense organs serially homologous to ears in all species. Both the crowded arrangement of receptor somata and dendrites may result from functional constraints relating to frequency discrimination, or from developmental constraints of auditory morphogenesis in postembryonic development. J. Morphol. © 2012 Wiley Periodicals, Inc.     

Central projections of sensory cells of the midleg of the locust,Schistocerca gregaria

The central projections of trichoid hairs and of some scolopidial organs of the mesothoracic leg of the locust Schistocerca gregaria were studied by using nickel chloride backfilling and single cell recording. Trichoid hair sensilla on different parts of the legs project somatotopically in the ventral part of the ipsilateral neuropile of the mesothoracic ganglion. Generally, distally located receptors have their terminal arborizations in ventro-lateral areas of the neuropile, and proximally located receptors in ventro-medial areas. The axons of the subgenual organ and tarsal chordotonal organs project into the intermediate neuropile.     

Projection areas and branching patterns of the tympanal receptor cells in migratory locusts,Locusta migratoria and Schistocerca gregaria

Summary In Locusta migratoria and Schistocerca gregaria, the projection areas and branching patterns of the tympanal receptor cells in the thoracic ganglia were revealed. Four auditory neuropiles can be distinguished on each side of the ventral cord, always located in the anterior part of the ring tract in each neuromere (two in the meta-, one in the meso-, and one in the prothoracic ganglion). Some of the receptor fibres ascend to the suboesophageal ganglion. There are distinct subdivisions within the auditory, frontal metathoracic and mesothoracic neuropiles. The arrangement of the terminal arborisations of the four types of tympanal receptor cells according to their different frequency-intensity responses is somatotopic and similar in the two ganglia. Here the receptor cells of type-1 form a restricted lateroventral arborisation. Cells of type-4 occupy the caudal part with a dorsorostral extension. Cells of type-2 and -3 arborise in a subdivision between both. Most of the stained low-frequency receptors (type-1, -2, and -3) terminate either in the metathoracic or, predominantly, in the mesothoracic ganglion. In contrast, the high-frequency cells (type-4) ascend to the prothoracic ganglion. The receptor fibres of the different types of receptor cells differ in diameter.Abbreviations aRT anterior part of the ring tract - cf characteristic frequency - MVT median ventral tract - SEG suboesophageal ganglion - SMC supramedian commissure - VMT ventral median tract - VIT ventral intermediate tract Supported by the Deutsche Forschungsgemeinschaft; part of program A7 in Sonderforschungsbereich 305 (Ecophysiology)     

A locust chordotonal organ coding for proprioceptive and acoustic stimuli

A chordotonal organ in the prothoracic segment of a locust combines features of a proprioceptive mechanoreceptor and an acoustic organ. This organ is closely associated with the tracheal system in the neck. The central nervous projections of the sensory cells contact neuropiles in all thoracic ganglia with the most dense arborizations in the metathoracic ganglion in close proximity, and even with some overlap, to the projections of tympanic fibres. Physiological experiments show that this organ responds to mechanical displacement of its receptor apodeme and, in addition, to acoustic stimulation via either a region of the cervical membrane which may act as a functional tympanic membrane, or via the tracheal system. Accepted: 14 October 1998     

Processing of calling songs by an L-shaped neuron in the prothoracic ganglion of the female cricket, Acheta domesticus

ABSTRACT. An L-shaped auditory intemeuron (LI) has been recorded from extracellularly and intracellularly, and identified morphologically (by Lucifer yellow or cobalt injection) in the prothoracic ganglion of mature female Acheta domesticus. The morphology of the LI is very similar to ascending, prothoracic acoustic interneurons that are most sensitive to higher carrier frequencies in both A. domesticus and other gryllid species. Its terminations in the brain are similar to ascending acoustic interneurons found in other gryllids. The LI neuron is most sensitive to 4–5 kHz model calling songs (CSs), the main carrier frequency of the natural call. Thresholds to high frequencies (8–15 kHz) are 15–20 dB higher. Increasing CS intensities of up to 15 dB above threshold at 4–5 kHz result in increased firing rates by the LI. More than 15 dB increase in intensity causes saturation with little increase in spiking rate until the intensity surpasses 80 dB. In response to 70 dB or higher stimulus intensities, the LI responds to the second and third CS syllables with one or two spikes, pauses, and then produces a burst of nerve impulses with the same or greater latency than for lower intensity stimuli. In response to CS syllables of changing duration (10–30 ms) this neuron responds with a rather constant duration burst of impulses. Syllable periods of the CS stimuli were accurately encoded by the LI. Progressively stronger injection of hyperpolarizing current reduces, and ultimately stops spiking of the LI in response to CS stimuli. More intense stimulation with reduced hyperpolarization shows an initial spike, pause and burst of spikes. Intracellular recording from axonal regions of the neuron shows large spikes, small EPSPs and a developing hyperpolarization through the response to a CS chirp. Inhibitory input to the LI is demonstrated at 4.5, 8 and 16 kHz. This probably explains the specialized response characteristics of the LI which enhanced its encoding of CS syllable period.