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Binaural interaction in the superior colliculus of the chinchilla
Brain Research, 62 (1973) 227-230
227
© Elsevier ScientificPublishing Company, Amsterdam - Printed in The Netherlands
Binaural interaction in the superior colliculus of the chinchilla
TRUMAN E. MAST AND DAVID Y. CHUNG Bioacoustics Laboratory Eye and Ear Hospital and School of Medicine University of Pittsburgh Pittsburgh, Pa. 15213 (U.S.A.)
(Accepted July 31st, 1973)
Several recent studies have shown that certain neurons of the superior colliculus are sensitive to acoustic stimulil,4, 7 and especially to signals from moving sources a& However these studies have used sound sources that were either monaural, or whose parameters were not easily controlled, except for position in space. This report describes some experiments using controlled acoustic signals which show that the superior colliculus is exquisitely sensitive to binaural temporal differences. The results also show that neurons which are primarily sensitive to contralateral signals and unresponsive to ipsilateral signals, may nevertheless be sensitive to binaural differences. Similar neurons have been described in the inferior colliculus 6. Stein and Arigbede 7 have suggested that such 'contralateral units' in the superior colliculus would not be involved in localization. In the experiments reported here, our aim has been to determine if superior collicular neurons are responsive to binaural temporal differences in a manner similar to neurons of the classical auditory system. Adult chinchillas were anesthetized with Dial in urethane (0.45 ml/kg). Stainless steel microelectrodes were used in a stereotaxic approach to the superior colliculus. Histological verification was obtained for every penetration used to compile the present results. The methods used have been described previously 5. Sound was delivered via closed acoustic systems, incorporating two signal channels, which terminated in Audivox 9-C earphones. The earphones were threaded into plastic tubes sewn into the external auditory canals. The acoustic signals employed here were either 0. ! msec clicks or gated tone bursts with 5 msec rise-fall times. Interaural phase of tones was controlled by use of a phase shifter. The two outputs of the phase shifter, the reference-phase tone and the phase-shifted tone were gated separately. Further details of the experimental procedures have been published elsewhere 5. in the present experiments, a combination of evoked potential, multiple-unit and single-unit responses were studied. Prominent evoked potentials were elicited by clicks. Contralateral clicks were much more effective stimuli than ipsilateral clicks which yield little or no response. The responses, obtained using microelectrodes, were localized within the superior colliculus. Histological study showed the recording sites to be in the deep or intermediate layer of the superior colliculus. In addition, the response went through a
228
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SHORT COMMUNICATIONS
[
Fig. 1. Binaural click interaction in the superior colliculus. Note facilitation of evoked potential and the excitation of a single unit on presentation of binaural simultaneous clicks.
maximum as the electrode was advanced through the deep layers of the superior colliculus. The anatomical terminology used is that employed by Berman ~. Fig. 1 shows a case in which binaural clicks (simultaneous) resulted in a facilitated response. Monaural ipsilateral clicks evoked no detectable response while monaural contralateral clicks produced a moderate evoked potential. However, the two presented together elicited a larger evoked potential and also excited a single unit. in other experiments, ipsilateral clicks sometimes reduced the evoked potentials produced by a contralateral click. In one case, interaural delay was introduced. The maximum inhibitory effect was found to occur when the ipsilateral click preceded the contralateral click by 1 msec. A 1-msec difference in interaural arrival time is beyond that found under natural conditions. However, in order for a neuron to code interaural time differences (At) it is only necessary that firing rate be a function of At, over values of At which do occur naturally. The extreme maxima or minima may fall beyond that range. We observed only one type of evoked potential in response to tone bursts. This was a negative wave in association with the onset of the tone. Similarly, single-unit or multiple-unit activity was found only in relation to stimulus onset, it should be pointed out that the microelectrodes used in this study are capable of recording multiple-unit activity when it is present. These electrodes always record such activity in cochlear nucleus or in appropriate areas of the inferior colliculus. When responses are sustained for the duration of the tone bursts, the electrodes record multiple unit activity for that duration. Responses of superior colliculus to tone bursts were not sharply frequency-
229
SHORT COMMUNICATIONS
Fig. 2. Responses to binaural tone bursts (800 Hz, 45 dB SPL). The duration of the tones was 200 msec and repetition rate was approximately 1/5 sec. No response occurred later than the time period shown in the trace. An evoked potential and a single unit are present when the interaural phase angle is 80 °, contralateral leading. At an angle of 260 ° (equivalent to ipsilateral leading by 100°) no response is seen. Neither monaural ipsilateral nor monaural contralateral tones evoked any responses at 45 dB SPL.
specific, a n d a l t h o u g h a best frequency was present, tones at 50 dB S P L were excit a t o r y over a range o f 4 o r m o r e octaves. The responses were always sensitive to i n t e r a u r a l phase differences for tones o f low frequency, i.e., b e l o w a b o u t 2000 Hz. Fig. 2 shows an example o f a n e v o k e d p o t e n t i a l a n d a single unit response. The unit was excited on 9 o f 10 p r e s e n t a t i o n s o f the b i n a u r a l tone o f 800 H z (45 dB SPL), at an i n t e r a u r a l p h a s e angle o f 80 °, c o n t r a l a t e r a l leading. F o r c o m p a r i s o n , the r e c o r d at a phase angle o f 260 ° (i.e., ipsilateral leading by 100 °) is shown to indicate the absence o f a response. N e i t h e r m o n a u r a l c o n t r a l a t e r a l n o r m o n a u r a l ipsilateral tones o f the same frequency a n d intensity elicited a response. I n 3 o t h e r experiments we c o m p a r e d thresholds o f response for b i n a u r a l tones at i n t e r a u r a l phase angles t h a t p r o d u c e m a x i m u m a n d m i n i m u m responses. The differences in t h r e s h o l d so o b t a i n e d were 21 dB, 31 dB, a n d 56 dB. These results are s u m m a r i z e d in Table I. The d a t a show extremely p o w e r f u l effects o f b i n a u r a l interaction.
TABLE I COMPARISON OF RESPONSE THRESHOLDS FOR BINAURAL TONES
Comparison of thresholds (in dB SPL) for evoked potentials at most sensitive and least sensitive phase angles for binaural tones. Thresholds for monaural tones are also shown. Animal
Frequency (Hz)
Threshold for 'best-phase' binaural tones
Threshold for ' worst-phase" binaural tones
Threshold for contralateral tone
Threshold for ipsilateral tone
221 226 227
500 1500 1000
21 12 22
44 68 43
43 41 32
>68 >78 >76
230
SHORT COMMUNICATIONS
The results show that neurons of the deeper layers of the superior colliculus are more sensitive to binaural tones (at an appropriate interaural phase angle) than to monaural tones. The data also demonstrate that binaural responses (as in parts of the classical auditory ~,/~.tem) are not the sum of the monaural responses. Even where there appears to be no response to ipsilateral tones, the presence of such a tone in binaural stimulation can markedly alter the response. The neurons studied by Stein and Arigbede 6 were said to be ' m o n a u r a l ' because they were not excited by ipsilateral tones. However, the above observations suggest that such neurons could possibly be shown to be sensitive to binaural differences, given the appropriate signals. It is also interesting to note the similarity o f response in superior coUiculus and anterior parts o f the inferior colliculus in the anesthetized chinchilla. Our observations on the inferior colliculus (Mast and Chung, in preparation) show that onset responses are prominent anteriorly in the inferior colliculus, suggesting a possible functional similarity. It is k n o w n that electrical stimulation of the inferior colliculus results in evoked potentials in the superior colliculus s. Our results show that significant binaural interaction takes place in the superior colliculus. Its deeoer layers are sensitive to differences in interaural arrival time, as shown by selective responsiveness to appropriate interaural phase differences. The responses shown in this study were obtained from anesthetized animals, which may explain the fact that all responses were 'onset responses.' Our signals were equivalent to those from a stationary source, and it is possible that more sustained activity would have obtained from a simulated moving source. In any case, our results do show a sensitivity to interaural temporal differences in the superior colliculus that is similar to the sensitivity shown by the inferior colliculus and other auditory nuclei. This research was supported by Research G r a n t NS-10413 from the National Institutes of Health.
1 BELL, C., SIERRA, G., BrdENDIA, N., AND SEGUNDO, J. P., Sensory properties of neurons in the mesencephalic reticular formation, J. Neurophysiol., 27 (1964) 961-987. 2 BERMAN,A. L., The Brain Stem of the Cat. A Cytoarchitectonic Atlas with Stereotaxic Coordinates, Univ. of Wisconsin Press, Madison, 1968. 3 GORDON,B., Receptive fields in deep layers of cat superior colliculus, J. Neurophysiol., 36 (1973) 157-178. 4 HORN, G., AND HILL, R. M., Responsiveness to sensory stimulation of units in the superior colliculus and subjacent tectotegmental regions of the rabbit, Exp. NeuroL, 14 (1966) 199-223. 5 MAST, T. E., Binaural interaction and contralateral inhibition in the dorsal cochlear nucleus of chinchilla, J. Neurophysiol., 33 (1970) 108-115. 6 ROSE,J. E., GRoss, N. B., GEISLER, C. D., AND HIND, J. E., Some neural mechanisms in the inferior colliculus of the cat which may be relevant to localization of a sound source, J. Neurophysiol., 29 (1966) 288-314. 7 STEIN,B. E., AND ARIGBEDE,M. O., Unimodal and multimodal response properties of neurons in the cat's superior colliculus, Exp. Neurol., 36 (1972) 179-196. 8 SYKA,J., ANDSTRASCH1LL,M., Activation of superior colliculus neurons and motor responses after electrical stimulation of the inferior colliculus, Exp. Neurol., 28 (1970) 384-392. 9 WICKELGREN, B. G., Superior colliculus: Some receptive field properties of bimodally responsive cells, Science, 173 (1971) 69-72.
227
© Elsevier ScientificPublishing Company, Amsterdam - Printed in The Netherlands
Binaural interaction in the superior colliculus of the chinchilla
TRUMAN E. MAST AND DAVID Y. CHUNG Bioacoustics Laboratory Eye and Ear Hospital and School of Medicine University of Pittsburgh Pittsburgh, Pa. 15213 (U.S.A.)
(Accepted July 31st, 1973)
Several recent studies have shown that certain neurons of the superior colliculus are sensitive to acoustic stimulil,4, 7 and especially to signals from moving sources a& However these studies have used sound sources that were either monaural, or whose parameters were not easily controlled, except for position in space. This report describes some experiments using controlled acoustic signals which show that the superior colliculus is exquisitely sensitive to binaural temporal differences. The results also show that neurons which are primarily sensitive to contralateral signals and unresponsive to ipsilateral signals, may nevertheless be sensitive to binaural differences. Similar neurons have been described in the inferior colliculus 6. Stein and Arigbede 7 have suggested that such 'contralateral units' in the superior colliculus would not be involved in localization. In the experiments reported here, our aim has been to determine if superior collicular neurons are responsive to binaural temporal differences in a manner similar to neurons of the classical auditory system. Adult chinchillas were anesthetized with Dial in urethane (0.45 ml/kg). Stainless steel microelectrodes were used in a stereotaxic approach to the superior colliculus. Histological verification was obtained for every penetration used to compile the present results. The methods used have been described previously 5. Sound was delivered via closed acoustic systems, incorporating two signal channels, which terminated in Audivox 9-C earphones. The earphones were threaded into plastic tubes sewn into the external auditory canals. The acoustic signals employed here were either 0. ! msec clicks or gated tone bursts with 5 msec rise-fall times. Interaural phase of tones was controlled by use of a phase shifter. The two outputs of the phase shifter, the reference-phase tone and the phase-shifted tone were gated separately. Further details of the experimental procedures have been published elsewhere 5. in the present experiments, a combination of evoked potential, multiple-unit and single-unit responses were studied. Prominent evoked potentials were elicited by clicks. Contralateral clicks were much more effective stimuli than ipsilateral clicks which yield little or no response. The responses, obtained using microelectrodes, were localized within the superior colliculus. Histological study showed the recording sites to be in the deep or intermediate layer of the superior colliculus. In addition, the response went through a
228
1 5o.scc
SHORT COMMUNICATIONS
[
Fig. 1. Binaural click interaction in the superior colliculus. Note facilitation of evoked potential and the excitation of a single unit on presentation of binaural simultaneous clicks.
maximum as the electrode was advanced through the deep layers of the superior colliculus. The anatomical terminology used is that employed by Berman ~. Fig. 1 shows a case in which binaural clicks (simultaneous) resulted in a facilitated response. Monaural ipsilateral clicks evoked no detectable response while monaural contralateral clicks produced a moderate evoked potential. However, the two presented together elicited a larger evoked potential and also excited a single unit. in other experiments, ipsilateral clicks sometimes reduced the evoked potentials produced by a contralateral click. In one case, interaural delay was introduced. The maximum inhibitory effect was found to occur when the ipsilateral click preceded the contralateral click by 1 msec. A 1-msec difference in interaural arrival time is beyond that found under natural conditions. However, in order for a neuron to code interaural time differences (At) it is only necessary that firing rate be a function of At, over values of At which do occur naturally. The extreme maxima or minima may fall beyond that range. We observed only one type of evoked potential in response to tone bursts. This was a negative wave in association with the onset of the tone. Similarly, single-unit or multiple-unit activity was found only in relation to stimulus onset, it should be pointed out that the microelectrodes used in this study are capable of recording multiple-unit activity when it is present. These electrodes always record such activity in cochlear nucleus or in appropriate areas of the inferior colliculus. When responses are sustained for the duration of the tone bursts, the electrodes record multiple unit activity for that duration. Responses of superior colliculus to tone bursts were not sharply frequency-
229
SHORT COMMUNICATIONS
Fig. 2. Responses to binaural tone bursts (800 Hz, 45 dB SPL). The duration of the tones was 200 msec and repetition rate was approximately 1/5 sec. No response occurred later than the time period shown in the trace. An evoked potential and a single unit are present when the interaural phase angle is 80 °, contralateral leading. At an angle of 260 ° (equivalent to ipsilateral leading by 100°) no response is seen. Neither monaural ipsilateral nor monaural contralateral tones evoked any responses at 45 dB SPL.
specific, a n d a l t h o u g h a best frequency was present, tones at 50 dB S P L were excit a t o r y over a range o f 4 o r m o r e octaves. The responses were always sensitive to i n t e r a u r a l phase differences for tones o f low frequency, i.e., b e l o w a b o u t 2000 Hz. Fig. 2 shows an example o f a n e v o k e d p o t e n t i a l a n d a single unit response. The unit was excited on 9 o f 10 p r e s e n t a t i o n s o f the b i n a u r a l tone o f 800 H z (45 dB SPL), at an i n t e r a u r a l p h a s e angle o f 80 °, c o n t r a l a t e r a l leading. F o r c o m p a r i s o n , the r e c o r d at a phase angle o f 260 ° (i.e., ipsilateral leading by 100 °) is shown to indicate the absence o f a response. N e i t h e r m o n a u r a l c o n t r a l a t e r a l n o r m o n a u r a l ipsilateral tones o f the same frequency a n d intensity elicited a response. I n 3 o t h e r experiments we c o m p a r e d thresholds o f response for b i n a u r a l tones at i n t e r a u r a l phase angles t h a t p r o d u c e m a x i m u m a n d m i n i m u m responses. The differences in t h r e s h o l d so o b t a i n e d were 21 dB, 31 dB, a n d 56 dB. These results are s u m m a r i z e d in Table I. The d a t a show extremely p o w e r f u l effects o f b i n a u r a l interaction.
TABLE I COMPARISON OF RESPONSE THRESHOLDS FOR BINAURAL TONES
Comparison of thresholds (in dB SPL) for evoked potentials at most sensitive and least sensitive phase angles for binaural tones. Thresholds for monaural tones are also shown. Animal
Frequency (Hz)
Threshold for 'best-phase' binaural tones
Threshold for ' worst-phase" binaural tones
Threshold for contralateral tone
Threshold for ipsilateral tone
221 226 227
500 1500 1000
21 12 22
44 68 43
43 41 32
>68 >78 >76
230
SHORT COMMUNICATIONS
The results show that neurons of the deeper layers of the superior colliculus are more sensitive to binaural tones (at an appropriate interaural phase angle) than to monaural tones. The data also demonstrate that binaural responses (as in parts of the classical auditory ~,/~.tem) are not the sum of the monaural responses. Even where there appears to be no response to ipsilateral tones, the presence of such a tone in binaural stimulation can markedly alter the response. The neurons studied by Stein and Arigbede 6 were said to be ' m o n a u r a l ' because they were not excited by ipsilateral tones. However, the above observations suggest that such neurons could possibly be shown to be sensitive to binaural differences, given the appropriate signals. It is also interesting to note the similarity o f response in superior coUiculus and anterior parts o f the inferior colliculus in the anesthetized chinchilla. Our observations on the inferior colliculus (Mast and Chung, in preparation) show that onset responses are prominent anteriorly in the inferior colliculus, suggesting a possible functional similarity. It is k n o w n that electrical stimulation of the inferior colliculus results in evoked potentials in the superior colliculus s. Our results show that significant binaural interaction takes place in the superior colliculus. Its deeoer layers are sensitive to differences in interaural arrival time, as shown by selective responsiveness to appropriate interaural phase differences. The responses shown in this study were obtained from anesthetized animals, which may explain the fact that all responses were 'onset responses.' Our signals were equivalent to those from a stationary source, and it is possible that more sustained activity would have obtained from a simulated moving source. In any case, our results do show a sensitivity to interaural temporal differences in the superior colliculus that is similar to the sensitivity shown by the inferior colliculus and other auditory nuclei. This research was supported by Research G r a n t NS-10413 from the National Institutes of Health.
1 BELL, C., SIERRA, G., BrdENDIA, N., AND SEGUNDO, J. P., Sensory properties of neurons in the mesencephalic reticular formation, J. Neurophysiol., 27 (1964) 961-987. 2 BERMAN,A. L., The Brain Stem of the Cat. A Cytoarchitectonic Atlas with Stereotaxic Coordinates, Univ. of Wisconsin Press, Madison, 1968. 3 GORDON,B., Receptive fields in deep layers of cat superior colliculus, J. Neurophysiol., 36 (1973) 157-178. 4 HORN, G., AND HILL, R. M., Responsiveness to sensory stimulation of units in the superior colliculus and subjacent tectotegmental regions of the rabbit, Exp. NeuroL, 14 (1966) 199-223. 5 MAST, T. E., Binaural interaction and contralateral inhibition in the dorsal cochlear nucleus of chinchilla, J. Neurophysiol., 33 (1970) 108-115. 6 ROSE,J. E., GRoss, N. B., GEISLER, C. D., AND HIND, J. E., Some neural mechanisms in the inferior colliculus of the cat which may be relevant to localization of a sound source, J. Neurophysiol., 29 (1966) 288-314. 7 STEIN,B. E., AND ARIGBEDE,M. O., Unimodal and multimodal response properties of neurons in the cat's superior colliculus, Exp. Neurol., 36 (1972) 179-196. 8 SYKA,J., ANDSTRASCH1LL,M., Activation of superior colliculus neurons and motor responses after electrical stimulation of the inferior colliculus, Exp. Neurol., 28 (1970) 384-392. 9 WICKELGREN, B. G., Superior colliculus: Some receptive field properties of bimodally responsive cells, Science, 173 (1971) 69-72.