Neuronal Response Patterns in the Superior Olivary Complex of the Cat to Sound Stimulation

The Japanese Journal of Physiology 18, pp.267-287, 1968

NEURONAL RESPONSE PATTERNS IN THE SUPERIOR OLIVARY COMPLEX OF THE CAT TO SOUND STIMULATION

Takeshi WATANABE, Ta-Tsai LIAO* AND Yasuji KATSUKI

Department of Physiology, Tokyo Medical and Dental University, Yushima, Bunkyo-ku, Tokyo

From an anatomical viewpoint, the superior olivary complex seems to be a strategically important region for orientation of sound in space, because the complex is the lowest level in the auditory pathway where the binaural interaction of auditory information coming from both ears takes place. A number of electrophysiological investigations have been reported. (GALAMBOS, SCHWARTZKOPFF and RUPERT4), HALL5'8), MOUSHEGIAN, RUPERT and WHIT- COMB7),TSUCHITANI and BOUDREAU5,6), RUPERT, MOUSHEGIANand WHITCOMB12). With the help of anatomy and the psychophysical data, BEKEsY1,2) proposed a model for binaural hearing as a concept of time intensity trade, and a modified BEkEsY theme was presented by VAN BERGEIJK19). The model assumes that the contralateral innervation is excitatory in nature, while the ipsilateral innervation is inhibitory. HALL'S experiment on the accessory nucleus ex- plains well the evidence for this model. The primary purpose of the present study has been aimed for an analysis of the synaptic mechanism of the" time-intensity trading" units by intracellular recording, however relevant data in this respect are not available at present. The present report is concerned mainly with the response patterns of the superior olivary units and recordings obtained from the trapezoid nucleus, accessory nucleus and S-segment nucleus of the superior olive.

METHODS

Eighteen cats weighing from 1.6kg to 3.4kg were used. The animals were anes- thetized with dial by intraperitoneal injection (60mg/kg). They were ascertained to be free of infection by inspection of the ear drum and by an equally good threshold of N1, N2 responses to clicks for each ear.

Received for publication June 7, 1967 * Present address: Department of Otolaryngology , National Taiwan University Hospital, Taipei, Taiwan 渡辺武,*廖大栽,勝木保次

267 268 T . WATANABE, ET AL.

After tracheotomy the operation proceeded to disclose the skull base and both bullae by ventral approach . Then the animal was mounted on a Canberra type stere - otaxic instrument. Each bulla was drilled to make a small hole through which a fine silver wire (100 u in diameter with coiled tip) could be placed on the round window for continuous monitoring of the cochlear response . The access to the superior olivary complex was from the ventral surface of the medulla of ter removal of the bony plate between the bullae . Glass capillary micro- electrodes filled with 3 M KC1 or 2 .6 M K-citrate solution were used for unit recording . The ohmic resistance ranged between 20 and 50 megohms . The microelectrode was positioned stereotaxically according to VERHAARTM , SNIDER and NIEMER"), that is, at the point of P: 4 .5, Right Lateral: 1.5 and at an angle of 30•Ž to the sagittal plane where the electrode penetrates effectively to the trapezoid , accessory and S-segment nuclei. Most recordings were taken from the right superior olivary complex except in unavoidable situations caused by the course of the basilar artery and other large blood vessels. The microelectrode was advanced with a Canberra type microm anipulator or with a specially designed motor-driven micromanipulator under remote control . The sound stimuli were delivered into both ears through a matched pair of con - denser-type earphones with a closed sound system . Both clicks and tone bursts were used. Auditory stimuli were calibrated on a BRUER and KJAER audio -frequency spectro- meter. The reference level of 0 dB corresponds to a maximum SPL of 89 dB with reference to 0 .0002 dyne/cm2. In this sound stimulating system , we ascertained that there was no cross conduction (bone conduction) at the level of -6 dB because the primary auditory neurons or cochlear nuclear units did not fire at this intensity level by cross conduction of contralateral ear stimulation , although the entire frequency range was explored . Frequency modulated (FM) sound was also used to test the directional sensitivity of the neurons . The width of frequency modulation was change- able between 0.5 and 3 octaves , but usually settled at 1.5 octave bandwidth with about 20 msec duration of tone burst . For study of phase relation on binaurally applied sound , a phase shifter was used and displayed on the CRO as a Lissajous figure . Electrical activity from the microelectrode was fed into a cathode follower , then amplified on a Tektronix 565 oscilloscope . In this case, simultaneous DC and high-gain RC recordings were displayed on a separate channel . COCHLEAR responses recorded from each ear were fed into a differential input of the amplifier . Therefore the neural components (N1, N2) of both ears for clicks showed opposite polarity on a single beam . When the amplitude and waveform of N1, N2 responses of both cochleae are equal and simultaneous, a trace does not show any deflection due to the fact that the responses cancel out each other. However , when the N1, N2 responses were evoked with a very small interaural time difference , a complicated waveform was synthetized. Sound stimuli were also displayed on a separate channel . The responses were photographed with a Grass kymograph camera . In several experiments continuous DC recordings were made with an ink writer in order to check the membrane potential level . On several occasions, the responses were recorded on magnetic tape (TEAC data- recorder) at a speed of 30 in/sec for later computation .

RESULTS

FIG. 1 shows the path of a microelectrode penetrating dorso-laterally from the surface of the medulla. The left column in this figure shows the slow potentials for click stimulation recorded from different depths along the path AUDITORY UNITS IN SUPERIOR OLIVE 269

FIG. 1. Schematic diagram of the superior olive. Arrow indicates the microelectrode track. Py: pyramidal tract, ct: trapezoid body, nt: trapezoid nucleus, so: superior olivary nuclei, accessory nucleus located ventromedially to the ST segment nucleus. The left column represents the slow potentials for clicks recorded from different depths along a track indicating numerals. In the bottom traces, R and L indicate N1, N2 responses to clicks recorded froth the round window of the right and left cochleae, respectively. The right column shows the neuronal recordings. The top and middle figures show contralaterally and ipsilaterally responding units, respectively. The bottom figure shows unit recording from the pyramidal tract. In both right and left columns, upward deflection on the microelectrode traces indicates positivity. of penetration. We confirmed the results already reported by GALAMBOS, SCHWARTZKOPFF and RUPERT4), TSUCHITANI and BOUDREAU17). The reversal of the evoked potentials responding to ipsilateral and contralateral ear stimulation occurs at the region of the accessory nucleus. Ventrally to the accessory nucleus along the electrode path, contralateral ear stimulation evokes a negative potential and ipsilateral stimulation evokes a positive potential. When the electrode passes through the accessory nucleus, these potentials re- verse, that is, contralateral ear stimulation evokes a positive potential and ipsilateral stimulatian evokes a negative potential. In general, these characteristic wave patterns provided a good indication of probable electrode placement within the superior olivary complex. These slow potentials are recorded successively with unit recordings. In the right column three different unit recordings are shown. In the bottom figure the recording was taken from the neuron in the pyramidal tract. As can be seen, unit activity in this tract was not correlated to tone burst stimuli for either ear. Immediately after passing through the pyramidal tract, the unit responded to ipsilateral ear 270 T. WATANABE, ET AL. stimulation as shown in the middle figure. With still further advancement of the electrode, the unit responded to contralateral ear stimulation alone as shown in the top figure. Anatomically, this region corresponds to the trapezoid body where second order neurons from both cochlear nuclei cross each other and is composed of nerve fibers only. It seems that tonotopic localization may exist in the trapezoid body but we did not study this system- atically. When an electrode enters the trapezoid nucleus, slow potentials for contralateral ear stimulation became more prominent and negative in sign. With deeper penetration, unit responses were produced by either monaural (ipsilateral and contralateral) or binaural ear stimulation.

Classification. In more than 200 units recorded from the superior olivary complex, 80% responded monaurally to either ipsilateral or contralateral ear stimulation. Of these about 60% were activated by contralateral ear stimulation but not by monaural stimulation of the ipsilateral ear. Binaurally responding units were observed in 20% of the total. Binaural interaction for clicks was tested on 55 monaurally responding units by changing the interaural time-intensity differences. 22% of these

TABLE 1. Classification of units in the superior olivary complex

* Monaurally responding units: neurons activated by either ipsilateral or contralateral ear stimulation only. ** Binaurally responding units: neurons activated by both ipsilateral and contralateral ear stimulation. AUDITORY UNITS IN SUPERIOR OLIVE 271 were found to be "time-intensity trading" units. (TABLE 1) As seen in TABLE 1, the majority of units in the superior olivary complex were activated by contralateral ear stimulation. (3 A a) Histograms of the number of units vs. depth of recording from the surface of the medulla are given in FIG. 2. These histograms are based on 102 superior olivary neurons and classified into three groups, that is, A, units responding monaurally and contralaterally B, units responding monaurally and ipsilaterally and C, units responding binaurally.

FIG. 2. Histograms of the nu-nber of units vs. depth of recording from the surface of the medulla. A: contralaterally and monaurally responding units. B: ipsilaterally and monaurally responding units. C: binaurally responding units.

DC Recording. When a microelectrode was inserted into the superior olivary complex during acoustic stimulation at the rate of 2/sec, spikes of considerable amplitude appeared together with sudden negative deflection. This negative deflection was considered to be a sign that the microelectrode had just penetrated a neuron. In many cases, the membrane potential returned very rapidly to the original level and the amplitude of spikes gradually diminished, after which the unit was lost. The relation between membrane potential and amplitude of spikes seems to be closely correlated. The time course of the membrane potential change differs from neuron to neuron. In favorable cases a rather steady membrane potential level was recorded for 5 to 6 minutes. The resting potentials in 18 units whose transient peaks ranged from-10 mV 272 T. WATANABE, ET AL.

to -63.1 mV, averaged -41.6 mV. However, the amplitude of action potentials never exceeded the resting value.

(I) Monaurally responding units. As already mentioned there are many monaurally responding units in the superior olivary nuclei which have been classified according to the ear stimulated, i. e., ipsilaterally and contralaterally responding units. Binaural interaction with click stimulation was examined on 55 units. 15 units produced binaural interaction. Here, only the results obtained from these units are presented.

〝Time -intensity trading" units with click stimulation. The characters of "time- intensity trading "cells in the accessory nucleus were studied intensively by Hall using click stimulation. His electrophysiological data explained well the model proposed by VAN BERGEIJK. We observed two kinds of cells which showed time-intensity trade. For convenience, they will be referred to as types "I" and "II".

SO-26-12

R.click―30dB L.click(-20dB)leads

R-clickby 0.15msec

FIG. 3. Type I neuron. The left figure shows unit responses elicited to monaural click stimulation of the right ear (-30 dB) with 100% of firing probability as shown in the dotted pattern. The right figure shows inhibition of responses when the left click (-20 dB) leads the right (-30 dB) by 150 a sec. Sample records show (top to bottom) round window responses, DC unit recordings, RC unit recordings. This order also applies to FIGS. 5, 12 AUDITORY UNITS IN SUPERIOR OLIVE 273

A. Type I Units in this group responded only to monaural stimulation of the ipsilateral ear but not to monaural stimulation of the contralateral ear

(cf. FIG. 3). Responses were elicited to monaural click stimulation of the ipsilateral ear with 100% of firing probability (left figure), but when the contralateral click stimulation leads ipsilateral stimulation by 150ƒÊ sec, unit responses were inhibited (right figure). These neurons were encountered in 6

SO-15-3

FIG. 4. Response pattern of type I neurons to clicks with changing interaural time difference between R (right) and L (left) ears as indicated at the extreme right. The left column shows sample records and its dotted expression is shown at the right. 274 T. WATANABE, ET AL.

units and recorded from the trapezoid and S-segment nuclei in the superior olive. Perhaps these neurons receive axons from both cochlear nuclei; one as an excitatory input from the ipsilateral ear and the other as an inhibitory input from the contralateral ear. When the interaural time difference was changed, an extremely short time course of inhibition was observed (FIG. 4). In this case, the unit responded to ipsilateral click stimulation (RE) with double spikes but not to contralateral click stimulation (LE) at all. There is no binaural interaction when the ipsilateral click leads the contralateral one by more than 1.8 msec. When the time difference between the ipsilateral and contralateral click is 0.5 msec (RE leads LE) or simultaneous, the second spike was inhibited, but the first spike was not affected. When the interaural time relation was reversed, that is, the contralateral click lead, marked inhibition was observed at 0.15 msec . At longer time differences inhibition gradually recovered. B. Type II As shown in FIG. 5, unit responses were elicited only by contralateral clicks (left figure), and when the ipsilateral click (RE) lead the contralateral one by 200 p sec, the responses were inhibited completely (right figure). Thus the inhibitory manner of binaural interaction in this group of

SO-14-3

L.click・30dB R.click(-30dB)leads L.clickby0.2msec

Fig. 5. Type II neuron. The left figure shows unit responses elicited to monaural click stimulation of the left ear (-30 dB) with 100% of firing probability

as shown in the dotted pattern. The right figure shows inhibition of responses

when the right click (-30 dB) leads the left (-30 dB) by 200 ƒÊ sec. AUDITORY UNITS IN SUPERIOR OLIVE 275 units is exactly the opposite of type I with regard to the interaural time relation. C. Facilitation Facilitation was observed in three contralaterally responding units. These neurons did not respond at all to ipsilateral ear stimulation at various intensity levels. When sound stimuli were applied simultaneously to both ears, the neurons responded more than to stimulation of only the contralateral ear. The degree of facilitation was determined by measuring the change of threshold with click stimulation. In one example which was recorded from the trapezoid nuclear unit, the threshold was -45 dB with contralateral stimulation alone. When both ears were stimulated simultaneously, if the ipsilateral ear was stimulated at -40 dB, the threshold for the contra-

FIG. 6. Binaurally responding unit. The time interval between R (right: 12 kc, -30 dB) and L (left: 11. 5 kc, -10 dB) was changed as shown at the right. Time: 40 msec. 276 T. WATANABE, ET AL.

lateral ear was lowered to -53 dB . This property was not studied further at this time.

(II) Binaurally responding units. By binaurally responding units we mean unit responses elicited independently by dichotic stimulation of the two ears , and not temporo-spatial facilitation .

Responses to tones. As seen in FIG. 6, unit responses were elicited independently by tone burst applied to both right (12 kc, -30 kB) and left (11.5 kc. -10dB) ears. The number of these units was considerably large and the recording sites ranged from 1.8mm to 6.25mm from the surface of the medulla . This shows that binaurally responding units are distributed throughout the superior complex. (see FIG. 2). On these units the response areas were determined separately by monaur - al stimulation of the two ears. FIG. 7 A illustrates the paired response areas of 8 units recorded from the right superior olive . Each neuron has almost the same characteristic frequency for the activation of either ear but with different thresholds for each . 19 of 32 units possessed a dominant threshold for ipsilateral stimulation and 13 units for contralateral stimulation . An example of a post-stimulus time histogram (PST histogram) of the latter is shown in FIG. 7 B. In this case the stimulating frequencies and intensities for both ears were the same but interaural time interval was different . In order to study the binaural interaction of the two ears , the interaural time intervals were changed as shown in FIG. 6. When the time intervals were sufficiently large, i. e., either the right or left preceded by more than 100 msec, reponses were produced independently . However, when the contralateral ear stimulation preceded the ipsilateral stimulation by 33 or 55 msec , unit responses to ipsilateral stimulation were completely inhibited . At longer intervals the number of spikes increased . The relationship between the average number of spikes during a 20 msec tone burst and the time interval between the stimulation of the two ears in shown in FIG. 8. Zero on the abscissa indicates the simultaneous stimulation of both ears. At intervals of less than 20 msec, the tone bursts to each ear over- lapped, so that the number of spikes could not be determined separately . In these cases the total number of spikes is shown by a star in FIG. 8. A marked inhibition was produced when the left ear stimulation lead the right by intervals of up to 60 msec, then the number gradually returned to the original level which was reached when the interval was about 130 msec . This long-lasting inhibition was also observed in other neurons. The time course is quite long and the mechanism may be different from that of the 〝timp -intensity trading" units with click stimulation. This inhibition may occur due to the action of inhibitory interneurons . The character of such inhibitory interneurons will be described later. AUDITORY UNITS IN SUPERIOR OLIVE 277

R-SOUnlts

SO-26-1B

FIG. 7. A: Paired response areas of eight binaurally responding units. The solid line indicates stimulation of the ipsilateral ear (R). The dotted line indicates stimulation of the contralateral ear (L). B: PST histograms showing the difference of responsiveness when both ears are stimulated by the same frequency and intensity but with different interaural time differences, Sample number: 200. 278 T. WATANABE, ET AL.

R Leading L Leading FIG. 8. Time course of inhibition on a binaurally responding unit when the binaural interaction occurred. Zero on the abscissa indicates the simultaneous stimulation of both ears. Ordinate indicates the number of spikes within 20 msec duration of tone bursts both ipsiexcited (solid line) and contraexcited (brokenline) .

Phase relation. In binaurally responding units the effect of dichotic tone bursts with phase difference was studied. FIG. 9 represents a unit with a characteristicfrequency of 17 kc. The phasedifference of the stimulation is indicated as aLissajous figure. In this case there were no remarkable changes in spike discharge with various phase differences . The same trial was made on a"time-intensitytrading" unit which showed a characteristic frequency of 3 kc, and asimilar tendency was observed. Since our exploration was limited to units with a characteristicfrequency of more than 3 kc, we were unable to observe an interaction such as ROSE, GROSS, GEISLER and HIND 11) reported in theinferior collicular neurons which produced cyclic changes depending on the small time differences of the two ears.

Responses to clicks. Quantitative study by computer was made of the latency of units responding binaurally to click and illustrated as a PST histogram (FIG. 10). In this particular case, the unit was more responsive to contralateral click stimulation (LE) than to ipsilateral stimulation (RE) , as seenin A. In B, with high resolution of analysis time, both peaks of the PST histograms coincided exactly in time. Thus there seems to be no latencydif- ference in binaurally responding units. FIG. 11 shows unit responses produced by binaural click stimulation at various time intervals. The right andleft columns show opposite interaural time relations, that is, the contralateral leads the ipsilateral click stimulation AUDITORY UNITS IN SUPERIOR OLIVE 279

SO-23-15s

FIG. 9. Effect upon a binaurally responding

unit of dichotic tone burst stimulation to the two

ears with different phase. From top to bottom, R

(right ear) leads L(leftear), 0, 45, 90, 135, 180 (indicated by the Lissajous figure). •K

20mS

in the right column and the ipsilateral leads the contralateral click stimulation in theleft column. The bottom figure represents simultaneous click stimulation of both ears. Stimulus intensity was the same throughout in this series. When the ipsilateral lead the contralateral stimulation by more than 1.0 msec, unit responses still occurred independently. However when the time relation b3tween right and left stimulation was reversed and maintained at 1.2 msec, only a single spike was elicited. This discrepancy of the interaural time dif- 280 T. WATANABE, ET AL.

SO-26-5B

7.81msec FIG. 10.A: PST histograms for clicks in a binaurally responding unit. Inten- sity of click stimulation to both ears was the same . Responsiveness to click stimulation dominated in the contralateral ear rather than the ipsilateral one. B: With high resolution of analysis time, the upper histogram shows response to right ear stimulation and the lower histogram toleft ear stimulation .

ference necessary to produce fusion of spikes cannot be explained merely by the refractory period, but it might be due to the threshold difference between the ipsilateral and contralateral ear stimulation as described previously .

Burst discharges for clicks. FIG. 12 shows unit responses to contralateral click stimulation with burst discharges of varying duration . The burst discharge rate was 380 pulses per sec in this case . The duration was not constant, but rangedfrom 32 to 144 msec. Sometimes the discharges were interrupted with hyperpolarization as seen in the bottom figure . We observed three such cells activated by contralateral click stimulation. The best frequencies of two of these were determined to be 2 kc and 2.3 kc. They were recordedfrom the trapezoid nucleus. It is conceivable that these neurons may be the interneurons, presumably presynaptically connected to the contralateral excitatory neuron for the binaurally responding units. Therefore, the long-lasting inhi- AUDITORY UNITS IN SUPERIOR OLIVE 281

14ms 12.5ms

3.2 3.0

1,5

1.2

1.0

0.5

FIG. 11. Effect of interaural time difference uponfusion of spikes in a binaurally responding unit. The number indicates the interaural time difference in msec. Leftcolumn: R (right ear stimulation) leads L (left ear stimulation). Right column: L leads R. In each figure, the traces from top to bottom show unit responses, right N1, N2 responses andleft N1,N2 responses.Calibration: 2 mV and 25 msec. bition of the binaurally responding units as shown in FIG. 8 can be explained as due to the action of these interneurons.

Responses to frequency modulated (FM) sound. In order to examine the directional sensitivity of the superior olivary neurons,frequency modulated 282 T. WATANABE, ET AL.

FIG. 12. Burst discharges in response to click stimulation. In each figure, the traces (top to bottom) indicate N1, N2 responses recordedfrom theleft round window, DC unit recordings, and RC unit recordings. N1N2

L.Click-30dB

sound was used. FIG. 13 shows the effect of FM stimulus to a contralaterally and monaurally responding unit with a characteristic frequency of 1 kc. Figure A illustrates unit responses to a 1 kc tone burst at -30 dB. In B and C, ascending and descending FM sounds were applied. The bandwidth of frequency modulation in this case was about 1.5 octaves. The number of spikes for ascending FM sounds was larger than for descending sounds. A similar tendency wasfound in mostunits tested with FM sounds. In several units a descending FM sound was more effective than an ascending one in terms of impulse discharges of the neuron. Two units showed no change in the number of spikes for either ascending or descending FM sounds. AUDITORY UNITS IN SUPERIOR OLIVE 283

SO-18-3c

A B C

A. 1Kc -30dB B. FM0.8-2.5Kc C.FM2.5-0.8Kc

FIG. 13. Responses of a contralaterally and monaurally responding unit to frequency-modulated sound. In B and C the intensity of FM sounds is the same as in A. See text.

DISCUSSION

In addition to several studies on the units in the superior olivary complex, the present study has shown the mode of binaural interaction, that is, both ears activate the superior olivary complex which is composed of afunctional aggregate of"time-intensitytrading" units and binaurally responding units.

Monaurally responding units. Monaurally responding units are divided into ipsilaterally activated and contralaterally activated units. Themajority of units in the superior olivary complex were of the latter type. Concerning binaural interaction, attention was focussed on the"time- intensitytrading" cells. These neurons are classified as type I and type II, that is, type I neurons are excited by ipsilateral ear stimulation and inhibited by contralateral ear stimulation, and type II neurons are excited by contralateral stimulation and inhibited by ipsilateral stimulation. The ratio between the number of type I and type II neurons was equal in the present experiment. The trading characteristics of these units were similar to what HALL has already reported. While type II neurons werefound in the accessory nucleus, type I neurons were mainly encountered in the trapezoid and S-segment nuclei. One of the theories of binaural localization is that of lower level phenomena associated with neural processing and encoding in contrast to the cortical 284 T. WATANABE, ET AL. phenomena. This postulates that localization judgment is based on thecorn- parison of the amounts of response activity on both sides of the nuclei, particularly the accessory nuclei according to VAN BERGEIJK'S model. The response properties of binaural interaction between type I and type II neurons are the opposite of each other. Both type I and type II neurons may actually play an important role in the mechanism underlying the localization judgment, but the final decision probably takes place at a higher auditory level. An interestingfact about the "time-intensity trading" cells is the synaptic mechanisms governing the activity of these cells. No light was shed on this problem by intracellular recording. Further study is now being undertaken to clarify this problem.

Binaurally responding units. About 20% of the units examined in the superior olivary nuclei responded to acoustic stimulation of both ears. These units were recordedfrom any nuclei in thesuperior olive. Severalauthors4,5,7) have already noted the response patterns of these neurons.HALL5,6) found "cyclic" interaction in these units . Similar interaction was also reportedfor the units in the inferior colliculus by ROSE,GROSS, GEISLER andHIND11). RUPERT, MOUSHEGIAN andWHITCOMB") found that the neurons interact at considerable longer intervals, and they described them as leading-ear neurons. Their explorations were made using clicks. In the present study response characteristics were examined using tones as well as clicks. The response areas were determined separately by monaural stimulation of the two ears. They were shown to possess almost the same characteristic frequencies butdifferent thresholds, as shown in FIG. 7. It is a significant fact that binaurally responding units receive axons which carry similar inf or- mation from both ears. The latency of responses to clicks is also importantfor binaural theory because equal latencies are evoked by stimulation of either ear. Thisfact is also pointed out by GALAMBOS andMOUSHEGIAN4'8). Binaural interaction in this group showed an extremely long-lasting inhibition. This may be due to the action of the interneurons which show burst discharges to clicks. Binaurally responding units may not play a role in localization judgment. The physiological meaning of such long-lasting inhibition is still obscure.

Responses to frequency modulated sound. Recently, severalpapers9,15,16,21) have reported on unit responses to frequency modulated (FM) sound stimulus. WHITFIELD and EVANS")studied the cortical auditory units in unanes- thetized and unrestrained cats.SuGA.15'16) worked on bats using FM tone pulses. NELSON andERULKAR9) studied the units in theinferior colliculus of cat. These authors stated that numerous auditory neurons in the upper AUDITORY UNITS IN SUPERIOR OLIVE 285 level of the brain showed directional sensitivity to either ascending or descending FM sounds and some units showed this sensitivity to both types of FM sound. In the present study it was found that the directional sensitivity of neurons to FM stimuli is located in the superior olive. No directional sensitivity of neurons wasfound in the cochlear nucleus. It is interesting to note that the cries of the bat are succession of short- duration(few msec) ultrasonic FM tones. Directionally sensitive neurons in the bat are important for echo-location.SuGA15) concluded that directional sensitivity of neurons to FM tone pulses can be explained by the presence of inhibitory areas beside the response area. It is conceivable that thefunction of directionally sensitive neurons may be closely correlated with the perception of complex sounds.

Anatomical considerations. According to the report bySTOTLER14), the cells of the S-segment nucleus receive theirafferent input predominantlyfrom the homolateral cochlear nucleus. The observation of the slow wave patterns within this nucleus can be explained by such neural connections. In the present study the number of ipsilaterally and monaurally responding units in the S-segment nucleus was not large, as seen in FIG. 2 B. Perhaps this is due to a lack of exploration in this deep region or to thefact that the micro- electrodes were broken when they reached it. There are several type of synaptic patterns in the superior olivarynuclei; for instance, the calyces of HERD in the trapezoid nucleus and the peculiar dendrites in the accessorynucleus3). Recently, PFEIFFER10) noticed that the

A B C

FIG. 14. Possible synaptic pattern of the neurons in the superior olive which produced binaural interaction. A: Type II"time-intensitytrading" neuron. B: Type I"time-intensitytrading" neuron. C: Binaurally responding neuron. An inhibitory interneuron which connects presynaptically to the ipsilateral axon is interposed between the contralateral and ipsilateral axons. I and C indicate the axons coming from the ipsilateral and contralateral cochlear nuclei, respectively. 286 T. WATANABE, ET AL.

trapezoid nuclear neurons as well as the antero-ventral cochlear neurons showed an early response (P component) which might be due to the specific structure of the synaptic ending . There are many monaurally responding units which did not show any binaural interaction at all. The three modes of synaptic pattern which did produce binaural interaction in this experiment are presented in FIG. 14. In this figure, A and B represent typeII and type I"time-intensitytrading" neurons, respectively. C represents the binaurally responding units and shows the interneuron which is presumably presynaptically connected to the contralateral excitatory path. In order to establish this idea, more elaborate approaches are needed , that is, recording of EPSP or IPSP, intracellular recording changing the membrane potential level by polarized current, pharmacological study using strychnine , -erythroidin and other drugs β , etc.

SUMMARY 1. The response pattern of binaural interaction of single auditory neurons in the trapezoid, accessory and S-segment nuclei of the superior olivary complex of the cat was described . Neurons in these nuclei were classified as monaurally responding units and binaurally responding units . The former were further classified into ipsiexcited (type I) and contraexcited (type II)"time- intensitytrading" neurons. 2. Trading characteristics to interaural time and intensitydifferences were the same in both type I and type II neurons. An extremely short time course of inhibition was found. 3. On binaurally responding units the response areas were determined separately by monaural stimulation of the two ears. The response areas were similar, with almost the same characteristicfrequency but adifferent threshold . Comparing the latency to click stimuli of the two ears, a surprising coincidence in latency of responses was found by means of computer analysis. Binaural interaction was produced in these units with long-lasting inhibition . Inter- neuron action with burst discharges may participate in the mechanism of this interaction. 4. Directional sensitivity of auditory neurons tofrequency modulated sound was observed at this level. Since no directionally sensitive neurons could be found at a more peripheral level, the superior olivary nuclei is the lowest level in the auditory pathway where such neurons exist. 5."Time-intensitytrading" neurons may play an important role in the localization judgment. However, the binaurally responding units which produced a sustained inhibitory interaction between both ears must have some other function besides the localization judgment. AUDITORY UNITS IN SUPERIOR OLIVE 287

REFERENCES

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