Cockroach homologs of praying mantis peripheral auditory system components

This study identifies the cuticular metathoracic structures in earless cockroaches that are the homologs to the peripheral auditory components in their sister taxon, praying mantids, and defines the nature of the cuticular transition from earless to eared in the Dictyoptera. The single, midline ear of mantids comprises an auditory chamber with complex walls that contain the tympana and chordotonal transduction elements. The corresponding area in cockroaches, between the furcasternum and coxae, has many socketed hairs arranged in discrete fields and the Nerve 7 chordotonal organ, the homolog of the mantis tympanal organ. The Nerve 7 chordotonal organ attaches at the apex of the lateral ventropleurite (LVp), which has the same shape and general structure as an auditory chamber wall. High-speed video shows that when the coxa moves toward the midline, the LVp rotates medially to stimulate socketed hairs, and also moves like a triangular hinge giving the chordotonal organ maximal in-out stimulation. Formation of the mantis auditory chamber from the LVp and adjacent structures would involve only enlargement, a shift toward the midline, and a mild rotation. Almost all proprioceptive function would be lost, which may constitute the major cost of building and maintaining the mantis ear. Isolation from leg movement dictates the position of the mantis ear in the midline and the rigid frame, formed by the cuticular knobs, which protects the chordotonal organs.     

The midline metathoracic ear of the praying mantis,Mantis religiosa

Summary The praying mantis, Mantis religiosa, is unique in possessing a single, tympanal auditory organ located in the ventral midline of its body between the metathoracic coxae. The ear is in a deep groove and consists of two tympana facing each other and backed by large air sacs. Neural transduction takes place in a structure at the anterior end of the groove. This tympanal organ contains 32 chordotonal sensilla organized into three groups, two of which are 180° out of line with the one attaching directly to the tympanum. Innervation is provided by Nerve root 7 from the metathoracic ganglion. Cobalt backfills show that the auditory neuropile is a series of finger-like projections terminating ipsilaterally near the midline, primarily near DC III and SMC. The auditory neuropile thus differs from the pattern common to all other insects previously studied.     

Hearing and frequency dependence of auditory interneurons in the parasitoid fly <Emphasis Type="Italic">Homotrixa alleni</Emphasis> (Tachinidae: Ormiini)

The parasitoid tachinid fly Homotrixa alleni detects its hosts by their acoustic signals. The tympanal organ of the fly is located at the prothorax and contains scolopidial sensory units of different size and orientation. The tympanal membrane vibrates in the frequency range of approximately 4–35 kHz, which is also reflected in the hearing threshold measured at the neck connective. The auditory organ is not tuned to the peak frequency (5 kHz) of the main host, the bush cricket Sciarasaga quadrata. Auditory afferents project in the three thoracic neuromeres. Most of the ascending interneurons branch in all thoracic neuromeres and terminate in the deutocerebrum of the brain. The interneurons do not differ considerably in frequency tuning, but in their sensitivity with lowest thresholds around 30 dB SPL. Suprathreshold responses of most neurons depend on frequency and intensity, indicating inhibitory influence at higher intensities. Some neurons respond particularly well at low frequency sounds (around 5 kHz) and high intensities (80–90 dB SPL), and thus may be involved in detection of the primary host, S. quadrata. The auditory system of H. alleni contains auditory interneurons reacting in a wide range of temporal patterns from strictly phasic to tonic and with clear differences in frequency responses.     

The bimodal auditory-vibratory system of the thoracic ventral nerve cord in Locusta migratoria (Acrididae, Locustinae, Oedipodini).

In locusts the auditory receptors of the tympanal organs and many of the vibratory receptors of all 6 legs converge at the level of the thoracic ventral nerve cord, forming a combined auditory-vibratory sensory system; it is represented by the VS-, S-, and V-neurons ascending to the supraesophageal ganglion. The connections between vibratory receptors of the different legs and the dendritic inputs of the bimodal ascending neurons are investigated in this report. As an example, the dendritic branches of the G- and V3-neurons for auditory and vibratory input could be localized by simultaneous recording at 2 different positions of the axon. The vibratory input from the receptors of the different legs was determined. Segmental and/or intersegmental thoracic interneurons are intercalated between the receptors and the ascending auditory-vibratory neurons (G- and V3-neurons). The morphology and function of 2 intersegmental vibratory interneurons (VI1- and VI2-neurons) are described. They probably connect the vibratory receptors of 1 (or 2) leg(s) of 1 thoracic segment with the different bimodal auditory-vibratory neurons. The importance of the anterior Ring Tract for synaptic connection between receptor cells, first order interneurons, and bimodal auditory-vibratory neurons is discussed on the basis of morphological and physiological data.     

Sexual dimorphism of auditory function and structure in praying mantises (Mantodea; Dictyoptera)

Sexual dimorphism of tympanate auditory systems in insects has bees described in only a few taxonomically isolated cases. However, widespread sexual dimorphism occurs in the ultrasound-sensitive, midline ear of the praying mantis.
In dimorphic species, it is always the female mantis that shows a reduction in ultrasonic hearing. The dimorphism may be mild—a difference in tuning and small reduction in sensitivity—or extreme with no evidence of audition in the female. In all but the mildest cases, the reduction in hearing is accompanied by significant anatomical divergence from the male ear structure. Two distinct metathoracic groove ('ear') types are linked to hearing reduction in the females.
Anatomical evidence of auditory sexual dimorphism appears in 34% of the 183 mantis genera examined. The dimorphic genera are widely but non-uniformly distributed within three of the four largest mantis families.
Auditory sexual dimorphism is closely correlated with dimorphism in wing length. In general, mantises with functional wings have sensitive ultrasonic hearing while those with short wings do not. These findings support the hypothesis that ultrasonic hearing in mantises is part of a defensive system against attack by echolocating bats.     

Neuroplasticity and phonotaxis in monaural adult female crickets (Gryllus bimaculatus de Geer)

Summary One foreleg was amputated at mid-femur in adultGryllus bimaculatus females. In phonotaxis tests these monaural crickets show course deviations and circling towards the intact side (Fig. 1). Mean course stability is best at 60 and 70 dB (Fig. 2). Here it differs significantly from a threshold value for orientated walking in females operated on the day of adult moult, but not in those operated two weeks later. The orientational performance improves with the interval between amputation and test (Fig. 3).Centripetal cobalt backfills reveal degeneration of tympanal nerve fibers on the amputated side (Fig. 4B, C). The mean number of intact afferents crossing the midline of the prothoracic ganglion is increased in monaural versus binaural crickets. Maximum transmidline extension is not correlated with the period of deafferentation (Fig. 5).Intracellular recording and staining of prothoracic auditory interneurons shows some axonal sprouts in ON1i (intact side) and ON2, but no significant physiological changes (Figs. 6A, D; 8A, C, E, G). Apart from axonal sprouts ON1a (amputated side) may show a few dendritic sprouts into the intact auditory neuropil (Figs. 6C, 7). Excitation in some ON1a-cells reveals functional contacts to intact auditory afferents (via crossing dendrites or possibly crossing afferents, Figs. 6e, 7, 8F). Morphological and associated physiological changes start early in AN2a (amputated side). The degree of crossing dendrites and contralateral excitation increases with postoperative age (Figs. 8H, 9).     

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.     

Morphological and physiological regeneration in the auditory system of adult <Emphasis Type="Italic">Mecopoda elongata</Emphasis> (Orthoptera: Tettigoniidae)

Orthopterans are suitable model organisms for investigations of regeneration mechanisms in the auditory system. Regeneration has been described in the auditory systems of locusts (Caelifera) and of crickets (Ensifera). In this study, we comparatively investigate the neural regeneration in the auditory system in the bush cricket Mecopoda elongata. A crushing of the tympanal nerve in the foreleg of M. elongata results in a loss of auditory information transfer. Physiological recordings of the tympanal nerve suggest outgrowing fibers 5 days after crushing. An anatomical regeneration of the fibers within the central nervous system starts 10 days after crushing. The neuronal projection reaches the target area at day 20. Threshold values to low frequency airborne sound remain high after crushing, indicating a lower regeneration capability of this group of fibers. However, within the central target area the low frequency areas are also innervated. Recordings of auditory interneurons show that the regenerating fibers form new functional connections starting at day 20 after crushing.     

The tympanal hearing organ of the parasitoid fly Ormia ochracea (Diptera,Tachinidae, Ormiini)

Tympanate hearing has evolved in at least 6 different orders of insects, but had not been reported until recently in the Diptera. This study presents a newly discovered tympanal hearing organ, in the parasitoid tachinid fly, Ormia ochracea. The hearing organ is described in terms of external and internal morphology, cellular organization of the sensory organ and preliminary neuroanatomy of the primary auditory afferents. The ear is located on the frontal face of the prothorax, directly behind the head capsule. Conspicuously visible are a pair of thin cuticular membranes specialized for audition, the prosternal tympanal membranes. Directly attached to these membranes, within the enlarged prosternal chamber, are a pair of auditory sensory organs, the bulbae acusticae. These sensory organs are unique among all auditory organs known so far because both are contained within an unpartitioned acoustic chamber. The prosternal chamber is connected to the outside by a pair of tracheae. The cellular anatomy of the fly's scolopophorous organ was investigated by light and electron microscopy. The bulba acustica is a typical chordotonal organ and it contains approximately 70 receptor cells. It is similar to other insect sensory organs associated with tympanal ears.The similarity of the cellular organization and tympanal morphology of the ormiine ear to the ears of other tympanate insects suggests that there are potent constraints in the design features of tympanal hearing organs, which must function to detect high frequency auditory signals over long distances. Each sensory organ is innervated by a branch of the frontal nerve of the fused thoracic ganglia. The primary auditory afferents project to each of the pro-, meso-, and metathoracic neuropils. The fly's hearing organ is sexually dimorphic, whereby the tympanal membranes are larger in females and the spiracles larger in males. The dimorphism presumably reflects differences in the acoustic behavior in the two sexes.     

Axonal degeneration within the tympanal nerve of Schistocerca gregaria

This study describes time course and ultrastructural changes during axonal degeneration of different neurones within the tympanal nerve of the locust Schistocerca gregaria. The tympanal nerve innervates the tergit and pleurit of the first abdominal segment and contains the axons of both sensory and motor neurones. The majority of axons (approx. 97%) belong to several types of sensory neurones: mechano- and chemosensitive hair sensilla, multipolar neurones, campaniform sensilla and sensory cells of a scolopidial organ, the auditory organ. Axons of campaniform sensilla, of auditory sensory cells and of motor neurones are wrapped by glial cell processes. In contrast, the very small and numerous axons (diameter <1 microm) of multipolar neurones and hair sensilla are not separated individually by glia sheets. Distal parts of sensory and motor axons show different reactions to axotomy: 1 week after separation from their somata, distal parts of motor axons are invaded by glial cell processes. This results in fascicles of small axon bundles. In contrast, distal parts of most sensory axons degenerate rapidly after being lesioned. The time to onset of degeneration depends on distance from the lesion site and on the type of sensory neurone. In axons of auditory sensory neurones, ultrastructural signs of degeneration can be found as soon as 2 days after lesion. After complete lysis of distal parts of axons, glial cell processes invade the space formerly occupied by sensory axons. The rapid degeneration of distal auditory axon parts allows it to be excluded that they provide a structure that leads regenerating axons to their targets. Proximal parts of severed axons do not degenerate.     

Neuronal basis of phonotactic behaviour in Tettigonia viridissima : processing of behaviourally relevant signals by auditory afferents and thoracic interneurons

Information transmission in the auditory pathway of Tettigonia viridissima was investigated using song models and artificial stimuli. Receptor cells respond tonically to song models and copy the syllable pattern within a wide intensity range. The omega-neuron responds tonically to soma-ipsilateral stimuli. Contralateral stimuli elicit IPSPs both within dendritic (ipsilateral) and axonal (contralateral) branches, thereby emphasizing directionality. Both AN1 and AN2 respond with tonic, non-adapting responses, precisely copying the syllable pattern of the song. While AN1 is excited by sonic frequencies and inhibited by ultrasonic frequencies, AN2 responds predominantly to ultrasound. The TN1 only responds to the ultrasonic components of the song, with phasic responses, which adapt quickly. In the adapted state, it responds selectively to the time pattern of the conspecific song, but not to the song patterns of two syntopic Tettigonia species. TN2, which has not been described up until now, is tuned to ultrasonic frequencies. Its responses to song models vanish after a few syllables, because of quick adaptation. The morphology is unusual with the axon running contralateral to the input site. The behavioural relevance of auditory interneurons is discussed and compared with the auditory system of crickets. Accepted: 3 November 1996     

Neuroethology of ultrasonic hearing in nocturnal butterflies (Hedyloidea)

Nocturnal Hedyloidea butterflies possess ultrasound-sensitive ears that mediate evasive flight maneuvers. Tympanal ear morphology, auditory physiology and behavioural responses to ultrasound are described for Macrosoma heliconiaria, and evidence for hearing is described for eight other hedylid species. The ear is formed by modifications of the cubital and subcostal veins at the forewing base, where the thin (1–3 μm), ovoid (520 × 220 μm) tympanal membrane occurs in a cavity. The ear is innervated by nerve IIN1c, with three chordotonal organs attaching to separate regions of the tympanal membrane. Extracellular recordings from IIN1c reveal sensory responses to ultrasonic (>20 kHz), but not low frequency (<10 kHz) sounds. Hearing is broadly tuned to frequencies between 40 and 80 kHz, with best thresholds around 60 dB SPL. Free flying butterflies exposed to ultrasound exhibit a variety of evasive maneuvers, characterized by sudden and unpredictable changes in direction, increased velocity, and durations of ∼500 ms. Hedylid hearing is compared to that of several other insects that have independently evolved ears for the same purpose-bat detection. Hedylid hearing may also represent an interesting example of evolutionary divergence, since we demonstrate that the ears are homologous to low frequency ears in some diurnal Nymphalidae butterflies.     

The tympanal hearing organ of the parasitoid fly Ormia ochracea (Diptera, Tachinidae, Ormiini)

Tympanate hearing has evolved in at least 6 different orders of insects, but had not been reported until recently in the Diptera. This study presents a newly discovered tympanal hearing organ, in the parasitoid tachinid fly, Ormia ochracea. The hearing organ is described in terms of external and internal morphology, cellular organization of the sensory organ and preliminary neuroanatomy of the primary auditory afferents. The ear is located on the frontal face of the prothorax, directly behind the head capsule. Conspicuously visible are a pair of thin cuticular membranes specialized for audition, the prosternal tympanal membranes. Directly attached to these membranes, within the enlarged prosternal chamber, are a pair of auditory sensory organs, the bulbae acusticae. These sensory organs are unique among all auditory organs known so far because both are contained within an unpartitioned acoustic chamber. The prosternal chamber is connected to the outside by a pair of tracheae. The cellular anatomy of the fly's scolopophorous organ was investigated by light and electron microscopy. The bulba acustica is a typical chordotonal organ and it contains approximately 70 receptor cells. It is similar to other insect sensory organs associated with tympanal ears. The similarity of the cellular organization and tympanal morphology of the ormiine ear to the ears of other tympanate insects suggests that there are potent constraints in the design features of tympanal hearing organs, which must function to detect high frequency auditory signals over long distances. Each sensory organ is innervated by a branch of the frontal nerve of the fused thoracic ganglia. The primary auditory afferents project to each of the pro-, meso-, and metathoracic neuropils. The fly's hearing organ is sexually dimorphic, whereby the tympanal membranes are larger in females and the spiracles larger in males. The dimorphism presumably reflects differences in the acoustic behavior in the two sexes.     

Directional characteristics of the auditory system of cicadas: is the sound producing tymbal an integral part of directional hearing?

Abstract. Directional hearing is investigated in males of two species of cicadas, Tympanistalna gastrica (Stål) and Tettigetta josei Boulard, that are similar in size but show different calling song spectra. The vibrational response of the ears is measured with laser vibrometry and compared with thresholds determined from auditory nerve recordings. The data are used to investigate to what extent the directional characteristic of the tympanal vibrations is encoded by the activity of auditory receptors. Laser measurements show complex vibrations of the tympanum, and reveal that directional differences are rather high (>15 dB) in characteristic but limited frequency ranges. At low frequencies, both species show a large directional difference at the same frequency (3–5 kHz) whereas, above 10 kHz, the directional differences correspond to the different resonant frequencies of the respective tymbals. Consequently, due to the mechanical resonance of the tymbal, the frequency range at which directional differences are high differs between the two species that otherwise show similar dimensions of the acoustic system. The directional differences observed in the tympanal vibrations are also observed in the auditory nerve activity. These recordings confirm that the biophysically determined directional differences are available within the nervous system for further processing. Despite considerable intra as well as interindividual variability, the ears of the cicadas investigated here exhibit profound directional characteristics, because the thresholds determined from recordings of the auditory nerve at 30° to the right and left of the longitudinal axis differ by more than 5 dB.     

Vibratory interneurons in the non-hearing cave cricket indicate evolutionary origin of sound processing elements in Ensifera

Tympanal hearing organs in the front tibiae of ensiferan insects supposedly evolved from vibration-sensitive tibial organs (TO), like those in the cave cricket Troglophilus neglectus (Rhaphidophoridae). If this is true, one expects to find interneurons in the cave cricket that are homologous to auditory neurons from hearing Ensifera. Therefore, we examined the central projections of the foreleg TO of the cave cricket, as well as morphology and response properties of interneurons responding to foreleg vibration. Sensory axons of the TO adjoined to the "tympanal nerve" terminate in the equivalent portion of the ring tract neuropile in the prothoracic ganglion as corresponding receptors of crickets and weta. We found nine putatively homologous elements to sound- and/or vibration-sensitive interneurons of Ensifera--one local neuron (unpaired median, DUM), three T-fibres (TN), three descending (DN) and two ascending neurons (AN). Presumable first-order interneurons arborising in the ring tract correspond to a local auditory DUM cell of bush crickets and to TN1, DN1 and AN2 of various Ensifera, respectively. Homologues of some prominent auditory cells, the "omega" neuron(s) and the ascending neuron 1 (AN1), however, were not found. We conclude that (a) T. neglectus interneurons are morphologically primitive with respect to those of hearing taxa, (b) significant changes in the dendritic structure/synaptic connectivity have taken place during the evolution of the most specialised first-order auditory interneurons of Ensifera, (c) the data do not contradict independent evolution of hearing in Grylloidea and Tettigonoidea. Other interneurons appear morpho-physiologically conserved across hearing and non-hearing species, possibly as a part of a multimodal "alert" system.     

Central projections of the thympanic fibres in noctuid moths

The receptor mechanism mediating the avoidance behaviour of flying noctuid moths in response to brief ultrasonic pulses may require only a single pair of acoustic sense cells, one A1 cell in each tympanic organ (Roeder, 1966c). Introduction of the fluorescent dye, procion yellow, into the nerve fibres leaving the tympanic organ has allowed the reconstruction of the central morphology of A1, the more sensitive of the two acoustic cells. The A1 axon follows a superficial course for the first ～100 μ auterior to its dorsal root of entry (3N1) into the thoracic ganglia, then plunges ventrally into the posterior mesothoracic neuropil where it branches. The posterior part reaches through two-thirds of the metathoracic ganglion. The anterior branch bifurcates in the anterior mesothoracic ganglion to give rise to a posteriorly directed branch extending through the ventral mesothoracic neuropil and an anterior branch which passes through the connective into the posterior half of the prothoracic ganglion. Here it ramifies along the midline. The cell remains strictly ipsi-lateral with numerous processes extending right up to the midline in the ventral neuropil of all three ganglia. This morphology correlates well with the map of sites from which A1 acoustic responses can be recorded in the central nervous system.     

Presynaptic contributions to response shape in an auditory neuron of the grasshopper

Neuron 714 is morphologically one of the most prominent neurons in the central auditory pathway of the grasshopper with arborizations extending from the abdominal neuromeres of the metathoracic ganglion to the brain. The aim of this study is to explore auditory information flow involving neuron 714 at the level of the ventral nerve cord. Paired intracellular recordings were made from neuron 714 in the mesothorax on the one hand, and from candidate presynaptic auditory neurons of the metathorax on the other. Electrical stimulation of the tympanal nerves provides an estimate of the synaptic distance between these interneurons and auditory afferents. Four, including neuron 714, are monosynaptically connected to afferents, the remainder disynaptically. Current-injection and spike-triggered averaging reveal that of nine neurons examined, seven make either monosynaptic, disynaptic or polysynaptic connections onto neuron 714. All connections are excitatory. Paired recordings show that response duration and response amplitude in synaptically linked cells vary according to the frequency of the stimulus. Measurements of the latency of the first excitatory post-synaptic potential evoked in neuron 714 by afferents and by metathoracic interneurons show how the synaptic drive from these sources shapes the auditory response of neuron 714. Accepted: 14 October 1998     

The responses of auditory ventral-cord neurons ofLocusta migratoria to vibration stimuli

Summary Most of the auditory neurons in the ventral nerve cord ofLocusta migratoria carry information not only from the tympanal organs but also from the subgenual organs (vibration sensors). Six of the eight neuron types studied electrophysiologically respond to at least these two modalities. Artificial sounds (white noise and pure tones varying in frequency and intensity) and sinusoidal vibration (200 Hz with an acceleration of 15.8 cm/s₂ or 2000 Hz and 87 cm/s₂) were used as stimuli.Complex excitatory and/or inhibitory interactions of the signals from both tympanal organs form the discharge patterns of auditory ventral-cord neurons in response to stimulation with air-borne sound. Normally the input of the ipsilateral sense organ dominates. The response patterns of these same neurons elicited by vibration stimuli are formed differently, as follows: (1) the sensory inputs of all subgenual organs are integrated in the responses of the ventral-cord neurons; in a single neuron they have either excitatory or inhibitory effects, but not both. (2) The more legs vibrated, the larger is the response. (3) The subgenual organs in the middle legs are most effective, those in the hind legs least so. (4) Ipsilateral vibration has more effect than contralateral.The six auditory neurons react to vibration combined with air-borne sound in different ways. The B neuron is the only one inhibited by vibration stimuli. The G neuron has been studied more intensively; because its anatomical arrangement and the location of the endings of the subgenual receptor fibers are known, it could be inferred from effects of transection of the connectives that interneurons are interposed between receptor cells and the G neuron.Part of the program Sonderforschungsbereich 114 (Bionach) Bochum, under the auspices of the Deutsche Forschungsgemeinschaft, with the support of the Slovenic Research Society (RSS)