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146. Electrophysiological Studies on Hearing in Common Insects in Japan

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146. Electrophysiological Studies on Hearing in Common Insects in Japan No. 9] 633 146. Electrophysiological Studies on Hearing in Common Insects in Japan By Yasuji KATSUKI and Nobuo SuGA Department of Physiology,Tokyo Medicaland Dental University (Comm. by T. FURUHA,TA,M.J.A., Nov. 12, 1958) Sound reception in insects has been studied electrophysiologically a great deal since Wever and Bray (1933),1' and some proposals were also submitted on its mechanism.2'3' However, the definite conclusion has not yet been given because of the technical difficulties in the experimentation. Recent development of the experimental technique in the electrophysiology and the electro-acoustics, however, has opened the way to explore this problem further. This preliminary report is concerned with the studies on the reception of air-borne sonic as well as ultrasonic waves in several kinds of most common insects in Japan. Materials used were some kinds of Cicadidae, Acridiidae, Tettigo- niidae, and Gryllidae. Each of these insects has the tympanal organ at the different part of the body. The nerve response to sonic and ultrasonic stimulation were recorded with a fine silver wire electrode from the tympanal and the cereal nerve and also from the central nerve cord of these animals. Further the peripheral neural mechanism on sound reception was elucidated by recording the single unit response with a superfine microelectrode technique which has been reported elsewhere.4' Sonic and ultrasonic waves used as stimuli were 44 tone bursts with duration of scores milliseconds and different fixed frequencies between 30 cps and 100 kcps. They were produced automatically in succession by a specially designed apparatus, details of which have also been described elsewhere.5' For the production of ultrasonic waves a specially designed condenser speaker was used. Pure tone stimuli were also used when necessary. All experiments were performed in the soundproof room, during the summer and the autumn. Results. Response area. The frequency range in which the tympanal or cercal nerve is activated by tone bursts of a certain intensity can be determined on the records which have been photo- graphed on a running film by the use of a long recording camera. Such serial records obtained by tone bursts in successive different intensities give the thresholds of the nerve response for respective frequencies of sound. Thus the response areas of those nerves, i.e. of the endorgan innervated by them, can be figured by plotting their thresholds against the frequency of sound on the abscissa and the X34 Y. IKATSUKIand N. SUGA [vol. 34, intensity in decibel unit on the ordinate. Fig. 1 shows one of the examples obtainedd with. Tanna japonensis (Cicadidae). Each of them was of course located at a different frequency range with a different single maximum value which means the most sensitive frequency for Fig. 1. Response area obtained from tympanal nerve of Tanna japonensis (Cicadidae). Nerve response (top) and tone burst in AC current (bottom) are simultaneously :recorded on a running film. Frequency and intensity of sound are shown at left side and at bottom of column respectively. respective animals. Table I shows the average response frequency range and the most sensitive frequency of the tympanal organ and also of the cereal hair sensilla of those insects examined. It is of great inter- est that the tympanal organ of Acridiidae and Tettigoniidae can well No. 9] Electrophysiological Studies on Hearing in Common Insects in Japan 635 Table I. The average response frequency range and the most sensitive frequency of the tympanal organ and the cercal hair sensilla respond to unusually high frequency ultrasonic waves and the most sensitive frequency of the latter is very high, even higher than 10 kcps. The response ranges of the other two families, Cicadidae and Gryllidae, are found to be within that of human being. The response areas of these cercal and tympanal nerves of Gryl- lidae are partly overlapping, the lower range being under the charge of the cercal nerve and the higher under that of the tympanal. Relation between nerve responses to the natural stridulatoon of the company and the sound. Responses of the tympanal nerve were recorded to the natural stridulatoon of a company from Meimuna opalif era, Gampsocleis buergeri, and Mecopoda elongata simultaneously with the stridulatory sound. In the record it was obviously recognized that small and large spikes completely synchronized with the pulsatory sound. Here a question arose what component frequencies were in- volved in the stridulatory sound. The stridulatory sound recorded by a tape recorder which was specially designed for both sonic and ultra- sonic waves at the Technical Laboratory of Japan Broadcasting Corpora- 636 Y. KATSUKI and N. SUGA [Vol. 34, Lion, was analized by means of a sonagraph. The stridulatory sound is a kind of noise, so that the results of analysis were shown as con- tinuous sound spectra. The upper limit frequency and the dominant frequency range involved in the stridulatory sound are shown in Table II. Table II. The upper limit frequency and the dominant frequency range involved in the stridulatory sound It is a matter of surprise that the dominant frequency range involved in sounds produced by the animal itself shows a good agreement with the most sensitive frequency range in the ear of that animal (Tables I and II). It is well conceivable that for the recognition of each individual of the company such an agreement is very convenient and even very important. It has been well known that the ear of the human being has the ability to hear most sensitively the sounds which compose most dominantly the voice produced by itself. This agreement may be the common nature of the organ for sound reception in the animal kingdom. Sound localization and ultrasonic waves. It is reasonably con- ceived that the ultrasonic wave produced by stridulation may play a critical role for the orientation of the insect. The production as well as the reception of the ultrasonic waves was recently confirmed on bats s' and noctuid moths 7' electrophysiologically. Examination was performed on the ear of Locusta migratoria danica to find the dif- ference of sensitivity of the ear to sonic as well as ultrasonic waves coming from various directions. The thresholds of tympanal nerve responses were measured to those incident waves coming from different directions and the more distinct difference of threshold was found between the ears of both right and left sides for the ultrasonic waves than for the sonic. This result reveals that the ultrasonic waves have the sharp directivity to the ear of the insect in spite of the small size of the body. Frequency discrimination. Pumphrey (1940)2) and later Autrum (1955) 3' made proposals that insects might be unable to discriminate the frequency of sounds. However we have now still no definite evidence for it. It is a matter of course that the insect has no sound- analizer, such as the cochlea of the higher animals. The chordotonal organ attached to the tympanum is only one which can transmit the No. 9] ElectrophysiologicalStudies on Hearing in CommonInsects in Japan 637 sound stimuli to the tympanal nerve. It may thus be predicted that the recording of responses of a single neuron to sonic and ultrasonic stimuli can provide the conclusive answer. The present authors suc- ceeded in it by the insertion of a superfine microelectrode into the prothoracic ganglion of Gampsocleis buergeri (Tettigoniidae) from the tympanal nerve root after making a small hole at its ventral surface. Unitary repetitive responses to stimulation could be obtained from a single tympanal neuron extracellularly, and. very rarely intracellularly, which were distinguished from the nerve cord responses to the same stimulation. The response areas of single neurons were determined by the same method as described above. Those areas obtained from more than ten neurons were divided into two types. All neurons which belong to either one of those two types showed almost the same re- sponse areas, in other words the response area obtained from the whole tympanal nerve already mentioned is composed of two areas, each of which partly overlaps. The neurons activated only by stimuli with higher frequencies were more sensitive to stimuli than the others activated by those with lower frequencies. On each neuron the relation between the num- ber of spikes per second and the intensity of stimuli in decibel unit was explor- ed for different stimulus frequencies. The relations were sigmoid and almost parallel to each other for different frequencies ex- cept for those at the ex- treme end of its response range (Fig. 2). The upper- most curve in the figure shows the case of a sound, the frequency of which is the characteristic fre- quency of the neuron it- self. The others are the cases of those sounds with either higer or lower fre- Fig. 2. Relation between number of spikes per quencies than the charac- second of a single tympanal neuron (ordinate) and intensity of sound (abscissa), obtained from teristic one. It is quite Gampsocleis buergeri (Tettigoniidae). Fre- obvious that a neuron quency of sound is shown on each curve. 638 Y. KATSUKIand N. SUGA [vol. 34, responds with the most frequent spikes to the sound, to which the neuron is the most sensitive, among many sounds with different fre- quencies, but of the constant intensity. From these results it can be said that the number of spikes per second responding to stimulation depends upon both the frequency and the intensity of stimulus and it may therefore be concluded that this kind of insect may at most discriminate the stimuli only by two kinds of nerve fibers in the tym- panal nerve and the number of spikes per second which depends reg- ularly upon the intensity of a stimulus with a certain frequency but differently upon its frequency, although such discrimination as that observed in higher animals is certainly impossible.
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