Heiner Römer

Morphology and physiology of auditory interneurons in the metathoracic ganglion of the locust

Summary1.Auditory interneurons in the metathoracic ganglion of the locust were characterized by their intracellularly recorded responses to sound stimuli, and by their morphology as revealed in sectioned preparations of single neurons injected with Lucifer Yellow. Accordingly, nine interneurons were identified as either local, bisegmental, ascending or T-neurons (Figs. 2–6).2.All cells possess arborizations within one or both sides of a prominent area of fine neuropil (frontal auditory neuropil), but the degree of overlap with the endings of tympanic afferents is different. For 2 ascending units (AN2, AN3) there is no overlap at all, indicating that they are interneurons of higher order.3.Two neurons, SN1 and TN1, were found with only excitatory input to low frequency sound, and their tuning reflected that one of low frequency receptor fibres. In contrast, the response of all other neurons to low frequency stimuli was more complex, consisting of excitatory and inhibitory synaptic potentials. The neuronal circuitry which might underlie such physiological behaviour is discussed.4.Recordings made from different parts of individual neurons enabled the sites of synaptic input and output to be localized. The postsynaptic dendrites of the interneurons appear to correspond to smooth endings in contrast to the beaded appearance of the presumptive presynaptic terminals (Fig. 8).5.The results include descriptions of auditory ‘sister-neurons’ (Fig. 6) which have a similar morphology and of ‘twin-neurons’ (Fig. 7), which, using our present physiological and morphological criteria, cannot reliably be distinguished one from another. The problem that arises from such doubling of cells for the concept of identified units is discussed.

High-frequency sound transmission in natural habitats: implications for the evolution of insect acoustic communication

SummaryTransmission and reception of high-frequency sound in the natural environment of bushcrickets (Tettigonia viridissima L.) was studied using the activity of an identified neuron in the insects auditory pathway as a “biological microphone”. Different positions of the receiver within the habitat were simulated by systematic variation of the distance from a loudspeaker and the height above the ground. Attenuation and filtering properties of the habitat were investigated with pure-tone frequencies between 5 and 40 kHz. Sound attenuation in excess of the attenuation due to geometrical spreading alone increased with increasing frequency, distance between sender and receiver, and decreasing height within the vegetation (Figs. 2–4). The data also confirm the existence of two kinds of excess attenuation. The amount of amplitude fluctuations in the sound signals was investigated by analysing the variability of the neuronal responses at a given receiver position. Variability increased with decreasing bandwidth of a noise signal at some distance from the loadspeaker. The variability in the responses to pure tones increased with both increasing frequency and distance from the source (Fig. 7). In the selected habitat, the temporal pattern of the natural calling song of male T. viridissima was very reliably reflected in the activity of the recorded neuron up to a distance of 30 m at the top of the vegetation, and 15–20 m near ground level (Figs. 5, 8). The maximum hearing distance in response to the calling song was about 40 m. Environmental constraints on long-range acoustic communication in the habitat are discussed in relation to possible adaptations of both the signal structure and the behavior of the insects.

Structure and function of acoustic neurons in the thoracic ventral nerve cord ofLocusta migratoria (Acrididae)

Summary1.Individual acoustic neurons were investigated by a combined recording and staining technique (CoS). Recordings were done with CoCl2 filled glass-microelectrodes; structural identification of the fibres was achieved by precipitating the Co2+ with (NH4)2S.2.The fibres of acoustic receptor neurons in the metathoracic ganglion have terminal branches only in the acoustic neuropiles. Fibres of high- and low frequency receptors were found electrophysiologically, which also differ in structure.3.The thoracic low frequency neurons are interneurons of complex structure; they are limited to the thoracic ventral nerve cord.4.The response patterns of acoustic neurons ascending to the supraoesophageal ganglion (B, K, C, I, and D neurons) are essentially generated in the frontal acoustic neuropiles of the metathoracic ganglion. Most of these neurons are connected with non-acoustic neuronal systems by their axon branches.

Bilateral coding of sound direction in the CNS of the bushcricketTettigonia viridissima L. (Orthoptera, Tettigoniidae)

Summary1.By means of simultaneous recordings with hook-electrodes the response behavior of a pair of homologous auditory interneurons on either side of the CNS of the bushcricketTettigonia viridissima L. was studied with particular emphasis on bilateral symmetry and directional coding.2.In about 50% of the preparations the threshold curves of both interneurons were symmetrical, tested within a frequency range from 5 to 40 kHz (Fig. 4a). In the remaining cases significant bilateral asymmetries at frequencies above 20 kHz and/or below 12 kHz could be observed (Figs. 4 and 5). Therefore, in this bushcricket species symmetrical thresholds seem to be guaranteed only within a rather limited frequency band around 20 kHz. This frequency coincides with one (the higher) of the two spectral bands within the conspecific call (Fig. 2).3.From recordings of unilaterally activated interneurons it can be inferred that the directional sensitivity of the single tympanic organ is as well tuned to this stimulus frequency of about 20 kHz. Maximal intensity differences of 15 to 20 dB between ipsiversus contralateral stimulation could be found (Fig. 3). Above and below this frequency the directionality of the ear was much lower.4.This frequency dependence of directional hearing could be confirmed on the level of the CNS. Only at a stimulus frequency of about 20 kHz the directional curves of both interneurons were very pronounced (Fig. 10) with precisely encoding the lateralization of the sound source starting at about 10 dB above neuronal thresholds (Figs. 7, 8 and 9).5.Though in single preparations the intensity-response curves of the two interneurons were notably different (Fig. 6), with respect to right versus left discrimination no auditory ‘handedness’ could be observed.6.As some insects already orient to a single or a small number of stimuli, individual neuronal responses of the right versus the left interneuron were compared at different sound directions (Figs. 11 and 12). Surprisingly, with frontal stimulation the probability of ‘correct’ (symmetrical) responses was only 17% which abruptly increased as soon as the sound source became lateral. These results are discussed in terms of the zig-zag walk of the localizing insect.

Representation of auditory distance within a central neuropil of the bushcricketMygalopsis marki

SummaryThe functional organization of the afferent auditory system was studied in the bushcricketMygalopsis marki. The acoustic stimuli were computer simulated signals equivalent to the song of a male recorded at various distances in the habitat.1.Individual receptor fibres have different tuning and absolute sensitivities and therefore differ in the specific distance at which they start to respond (‘threshold distance’, Fig. 3). This resulted in a range-fractionation in the distance of a conspecific signaller.2.The target areas of receptor fibre endings in the auditory neuropil of the prothoracic ganglion differed in the rostro-caudal and dorso-ventral axis (Fig. 4). This tonotopic arrangement and the range-fractionation of tympanic receptor fibres result in a specific spatial distribution of afferent nervous activity in the neuropil. The distribution depends on the distance away from a singing conspecific male (Fig. 5).3.Distance response characteristics of interneurons differed in both their shape and ‘threshold distance’ (Fig. 6). Certain neurons showed maximum responses which corresponded to an intermediate distance. These responses are based on a frequency-dependent synaptic interaction of excitation and inhibition (Fig. 7). The different distance response characteristics of interneurons can be related in part to the dendritic branching pattern within the neuropil.

Spike synchronization of tympanic receptor fibres in a grasshopper (Chorthippus biguttulus L., Acrididae): a possible mechanism for detection of short gaps in model songs

Summary1.In recordings from single tympanic receptor fibres inC. biguttulus, the response to synthesized sounds (rectangularly modulated white noise) interrupted by very brief (a few milliseconds) gaps was examined. In behavioral tests, females of the species respond very differently to such ‘model syllables’ at moderate intensities, depending on the gap width. If the gaps (in a moderateintensity syllable) are larger than 2 ms, the stimulus fails to elicit a response, whereas stimuli with gaps smaller than 1 ms are as effective as uninterrupted yllables (D. von Helversen 1972; O. von Helversen 1979).2.Neither the mean spike count nor the interspike-interval distribution of the single receptor response contains the information sufficient to distinguish uninterrupted syllables from syllables with gaps (Figs. 2 and 3). On the other hand, examination of the temporal distribution of the spikes reveals that gaps (or the pulse onsets following the gaps) cause spike synchronization (Fig. 4).3.An index of synchronization (IS) was defined as a measure of this gap-induced effect (Figs. 5 and 6). Analysis of the receptor responses based on IS revealed differences that correspond quantitatively to the abrupt abolition of the behavioral response at a gap-width between 1 and 2 ms. From the hypothesis that such brief gaps are detected by the nervous system by way of spike synchronization in the tympanic nerve, one can predict certain features of the behavioral response to highintensity stimuli.4.The gap-induced spike synchronization was more pronounced at higher temperatures. This effect was demonstrated in both summated recordings from the tympanic nerve and single fibre recordings (Fig. 8).5.Experiments with primary auditory fibres ofLocusta migratoria showed that the receptors in this species respond very similarly to the same stimuli. That is, the receptors ofC. biguttulus are not specially adapted for detecting very brief gaps. Synchronization of the spikes in parallel receptor fibres of the tympanal nerve is probably a general feature of acridids; we infer that inC. biguttulus this gap-induced synchronized activity is detected by special processing in higher auditory centres.

Sexual differences in auditory sensitivity: mismatch of hearing threshold and call frequency in a tettigoniid (orthoptera, tettigoniidae: Zaprochilinae)

SummarySexual dimorphism of the ear of an undescribed species of zaprochiline tettigoniid is described. The internal trachea, dedicated to hearing in other tettigoniids, is unmodified in the male but fully developed in the female. The external auditory spiracle is also lost in the male. In contrast, there is no difference between the sexes in the number of sensilla within the hearing organ. The male is 10 dB less sensitive than the female. The characteristic frequency of the hearing organ at 35 kHz does not match the carrier frequency of the males call at 51 kHz. As a result of this mismatch the female is remarkably insensitive to the males call (threshold at 75 dB SPL), and the male is even less sensitive (thresholds⩾80 dB SPL). In nature this provides a maximum hearing range of the male of less than 50 cm.

Responses to model songs of auditory neurons in the thoracic ganglia and brain of the locust

Summary1.Locust interneurons in the ventral nerve cord and the brain were tested with models of the stridulatory song. These models had the conspecific frequency composition (Fig. 1) but were varied with respect to the duration of the interchirp-interval.2.In most ascending interneurons such model songs elicited complex responses comprising EPSP and IPSP of different thresholds and amplitude. As a consequence of EPSP and IPSP interaction neurons exhibit optimised intensity-response characteristics with each having a ‘best intensity’ at a different absolute intensity value (Figs. 2–4). Only a few neurons show sigmoid IR-characteristics; these are little inhibited or not at all.3.The strength of inhibition seems to be correlated with the degree to which ascending interneurons habituate to a repeated stimulus (Fig. 5). When blocking the inhibitory synapses pharmacologically with picrotoxin, habituation is strongly reduced (Fig. 6). The suprathreshold responses of some neurons thus match the amplitude modulation of the conspecific song whereas others do not and give only on-responses. No tuning to the conspecific interchirp-interval was observed in ascending interneurons (Fig. 7).4.In the brain (supraoesophageal ganglion) 5 out of 24 recorded interneurons responded selectively to the temporal configuration of the conspecific model song (Fig. 9). In contrast to ascending neurons these units failed to demonstrate a matching of their spike response with the chirp structure of the model song.5.Such brain interneurons are not only tuned to the conspecific temporal configuration of the song, but also to a rather narrow range of sound intensity where the response is maximal (Fig. 10).6.The results are discussed with respect to neural processing of auditory information at different levels of the afferent pathway and with respect to the selectivity of the recognition process as observed in the behaviour of other grasshoppers.

Akustische Neuronen im Bauchmark vonLocusta migratoria

Summary1.The influence of the direction of the sound source on the response patterns of neurons in the auditory system ofLocusta migratoria has been investigated electrophysiologically. The new types C1, E, F, and I are introduced.2.The F-neuron reacts very sharply to a change in the direction of the sound source (Figs. 8 and 9), the C1-neuron shows no reaction to a change in the position of the sound source. Between these two extremes there are some neurons, which react to a change in direction in a graduated way.3.The response patterns of the C-neuron depend upon the position of the sound source. This dependence holds for the whole range of intensity and frequency to which this neuron responds (Pig. 17).4.The E-neuron signals only the direction of high level sounds (Pig. 11), the B-neuron signals only the direction of low level sounds (Pigs. 15 and 16). The G-neuron reacts only to sounds of middle frequencies and intensities (Pigs. 12, 13, and 14).5.The interactions between the neurons of both sides of the nerve cord can be shown by the rotation of the sound source before and after the destruction of one tympanum. The neuronal mechanisms which are responsible for the dependence of single neurons on the direction of the sound source are discussed.Zusammenfassung1.Der Einfluß der Schallrichtung auf die Antwortmuster der akustischen Neuronentypen vonLocusta migratoria wird elektrophysiologisch untersucht. Es werden neue Neuronentypen (C1, E, F und I) beschrieben.2.Das F-Neuron antwortet auf unterschiedliche Schallrichtungen sehr gut (Abb. 8 und 9), die Antworten des C1-Neurons dagegen sind unabhängig von der Schallrichtimg. Zwischen diesen beiden Extremen gibt es Neuronen, die die Richtung in abgestufter Weise verarbeiten.3.Die Antwortmuster des C-Neurons zeigen eine deutliche Richtungsabhängigkeit. Dies gilt für den gesamten Prequenz- und Intensitätsbereich, der von diesem Neuron beantwortet wird (Abb. 17).4.Von dem E-Neuron wird nur im oberen Intensitätsbereich eine genaue Richtungsverarbeitung vorgenommen (Abb. 11). Das G-Neuron verarbeitet die Schallrichtung nur im mittleren Frequenz- und Intensitätsbereich (Abb. 12–14). Die Richtungsbestimmung schwellennaher Laute wird vom B-Neuron durchgeführt (Abb. 15 und 16).5.Durch Drehung der Schallquelle und gleichzeitiger Ableitung vor und nach der Ausschaltung eines Tympanalorgans können mögliche Interaktionen zwischen ren Neuronen beider Seiten des Bauchmarks sichtbar gemacht werden. Die neurodalen Mechanismen, die die Richtungsabhängigkeit der einzelnen Neuronen hervornufen, werden diskutiert.

Akustische Neuronen mit T-Struktur im Bauchmark von Tettigoniiden

Summary1.The auditory system of the ventral nervous cord was studied in the following species of Tettigoniidae:Tettigonia viridissima, Decticns albifrons, Eupholidoptera chabrieri, Ephippigera spec.2.The response patterns of 4 second order neurons can be found and classified in both sides of the nervous cord in male and female Tettigoniidae. One type (TT-neuron) is the equivalent of the T-neuron found by Suga and Katsuki (1961) inGampsocleis buergeri.3.The AT-neuron shows a tonic reaction to frequencies in the range of 1–25 kcps. The number of spikes increases with increasing intensity and duration of stimulation (Fig. 10).4.The reaction of the DT-neuron is independent of stimulus intensity, duration and frequency (1–40 kcps). It responds with only one spike per stimulus.5.The TT-neuron responds to frequencies in the range of 5–40 kcps. The stimulus duration of 10–40 ms produces the highest numbers of spikes. The response patterns of the TT-neuron in both sides of the nervous cord are dependent on the position of the sound source. The different response patterns of the ipsi- and contralateral sides are produced by inhibitory interactions (Figs. 2 and 3).6.The neuron of “large latency” shows a tonic reaction to frequencies in the range of 1–35 kcps. Intensities of 60–80 dB are preferred. This neuron is characterized by its latency of 20–30 ms. It was found only in the suboesophageal ganglion.The neurons specified by the index T have a T-structure. Their impulses are conducted with the same discharge patterns to the supraoesophageal, meso-, and metathoracic ganglia.Zusammenfassung1.Die Hörbahn im Bereich des Bauchmarks wurde bei folgenden Tettigoniidenarten elektrophysiologisch untersucht:Tettigonia viridissima, Decticus albifrons, Eupholidoptera chabrieri, Ephippigera spec.2.Die Antwortmuster von 4 Sekundärneuronen wurden sowohl bei Männchen als auch bei Weibchen auf beiden Seiten des Bauchmarks gefunden. Ein Neuronentyp (TT-Neuron) entspricht dem von Suga und Katsuki (1961) beschriebenen T-Neuron, abgeleitet beiGampsocleis buergeri.3.Das AT-Neuron reagiert tonisch in einem Frequenzbereich von 1–25 kHz. Mit steigender Intensität und Reizdauer nimmt die Anzahl der Impulse zu (Abb. 10).4.Das DT-Neuron reagiert immer nur mit einem Spike auf Schallreize beliebiger Intensität, Dauer und Frequenz (1–40 kHz).5.Das TT-Neuron reagiert in einem Frequenzbereich von 5–40 kHz bevorzugt auf Schallreize von 10–40 ms Dauer. Längere Reize rufen on-Antworten hervor. Die Antwortmuster der TT-Neuronen beider Seiten des Bauchmarks sind von der Richtung der Schallquelle abhängig. Die unterschiedlichen Antwortmuster — abgeleitet auf der ipsi- und kontralateralen Seite — werden durch hemmende Interaktionen hervorgerufen (Abb. 2 und 3).6.Das Neuron mit „großer Latenz” reagiert tonisch in einem Frequenzbereich von 1–35 kHz bevorzugt auf mittlere Intensitäten (60–80 dB). Wesentliches Charakteristikum dieses Neurons ist seine große Latenz (20–30 ms). Dieses Neuron wurde nur im Unterschlundganglion gefunden.Alle anderen mit dem Index T versehenen Neuronentypen haben T-Struktur. Sie leiten ihre Impulse in gleichen Antwortmustern sowohl zum Oberschlundals auch zum Mesobzw. Metathorakalganglion.