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Auditory space representation in the superior colliculus of the big brown bat, Eptesicus fuscus
289
Brain Research, 311 (1984) 289-296 Elsevier BRE 10350
Auditory Space Representation Big Brown Bat,
in t h e S u p e r i o r C o l l i c u l u s o f t h e
Eptesicus fuscus
TATEO SHIMOZAWA*, XINDE SUN** and PHILIP H.-S. JEN
Division of Biological Sciences, The University of Missouri, Columbia, MO 65211 (U.S.A.) (Accepted March 6th, 1984)
Key words: superior colliculus - - bats - - auditory response areas - - auditory space
The auditory response areas of 123 superior collicular (SC) units of Eptesicusfuscus were studied under free-field acoustic stimulus conditions. A stimulus was delivered from a loudspeaker placed 14 cm in front of a bat. The best frequency of a unit was determined by changing the stimulus frequency until the minimum threshold was measured. A best frequency stimulus was then delivered as the loudspeaker was moved across the auditory space to determine the response center of the auditory response area of each unit. The response center was defined as the direction at which the unit had its lowest minimum threshold. The stimulus intensity was then raised 2-20 dB above the lowest minimum threshold of the unit and the response area for each stimulus intensity was determined. The response area of a unit expands with stimulus intensity, but the expansion is not even in all directions. The size of the response area of a unit does not correlate with its minimum threshold, best frequency, or recording depth. Response centers of 7 units were located directly in front of the animal, but most response centers were located in a limited portion of the contralateral auditory space. Although each unit has a response center which is the point of maximal sensitivity, the point-to-point representation of the auditory space is not systematically organized. We suggest that an animal with highly mobile external pinnae may not need an orderly auditory space map in its neural tissue for accurate sound localization. INTRODUCTION
The superior colliculus (SC) of vertebrates is a multimodal integration center which is involved in orienting the head, eyes, and pinnae toward different sensory stimuli10,ll,27,2s,33,34. Topographic projections of the primary receptors of the visual and somatosensory systems on the SC of various animals have b e e n demonstrated2-SA2,15,17-20,26,29,30. Recent studies on guinea pigs 22 and barn owls 16 indicate that the auditory space is systematically represented in the deep layers of the SC, but a study of the SC of cats 32 suggests that such an auditory map is unlikely to be found. Although the visual centers of bats are generally poorly developed, the SC is an exceptionl. Most basic auditory response properties of SC units of the
FM bat, Eptesicusfuscus, are similar to those of inferior collicular (IC) units ~3. However, SC units are not tonotopically organized along the dorsoventral axis and are more sensitive to frequency modulated signals than are IC unitsl4, 31. Under free-field stimulation conditions, we examined the auditory response areas of SC units to determine if there is a systematical auditory space representation in the SC of EptesiCUSfUSCI2S. MATERIALS AND METHODS
Each of 10 FM bats, Eptesicus fuscus (b.wt. 14.4-24.5 g) was anesthetized with Nembutal (45-50 mg/kg b.wt.) for surgery. The bat was tied to a metal plate and the flat head of a nail (1.8 cm) was mounted on the exposed anterior portion of the bat's
* Present address: Zoological Institute, Faculty of Science, Hokkaido University, Hokkaido, Japan. ** Present address: Department of Biology, East China Normal University, Shanghai, People,s Republic of China. Correspondence and reprint requests: P. H.-S. Jen, Division of Biological Sciences, The University of Missouri, Columbia, MO 65211, U.S.A. 0006-8993/84/$03.00 © 1984 Elsevier Science Publishers B.V.
290 skull with dental cement and acrylic glue. The head was then immobilized by fixing the shank of the nail with a set screw. The bat's h e a d was o r i e n t e d t o w a r d a l o u d s p e a k e r with the intersection of its inter-ear line and medial plane corresponding to 0 ° in azimuth and 0 ° in elevation of the bat's auditory space (Fig. 1). Acoustic stimuli (4 ms d u r a t i o n , 0.5 ms rise-decay times) were delivered from a c o n d e n s o r l o u d s p e a k e r ( A K G Model C K 50. d i a m e t e r 2 cm, weight 1.3 g) placed 14 cm in front of the bat's head. The loudspeaker was attached to an aluminum arm and could be placed at any position within 90 ° in azimuth and 50 ° in elevation of the bat's auditory space (Fig. 1). The position of the l o u d s p e a k e r was remotely controlled by two i n d e p e n d e n t servo-controlled motors and was m o n i t o r e d by an oscilloscope outside the sound p r o o f room. The l o u d s p e a k e r was calibrated with a Br/Jel and K j a e r 0.25 inch m i c r o p h o n e placed at the bat's ear. O u t p u t was expressed in dB SPL referred to a 0.0002 dyne/cm z root mean square. A f t e r a small hole was m a d e in the bat's skull, a 3 M KCI glass pipette electrode was inserted into the SC surface to record neural activity E l e c t r o d e s were placed on the central portion of the SC in o r d e r to avoid puncturing the surrounding large b l o o d vessels (Fig. 2). The hole was subsequently enlarged to place electrodes at many places inside the SC. Additional anesthetic (one third of the original dose) was administered during the later phase of the recording, when necessary. R e c o r d e d signals were amplified and sent to an oscilloscope and an audio monitor. All recordings were conducted in a sound p r o o f r o o m ( 3 5 - 3 8 °C). W h e n
an SC unit responding to acoustic stimuli d e l i v e r e d in front of the bat was e n c o u n t e r e d , stimulus frequency was adjusted to a specific value (the best frequency, BF) at which the stimulus intensity required for elicrang a response from the unit was m i n i m u m ~the m i n i m u m threshold, MT). Then, an acoustic stimulus set at the BF and M T of the umt was delivered from the l o u d s p e a k e r as it was moved across the auditory space of the bat. The stimulus intensity was adjusted to d e t e r m i n e the point of maximal sensitivity (referred to as the response center) whithin the response area of the unit at which the M T was the lowest. The response area was m e a s u r e d for at least two stimulus intensities above the lowest MT of the unit. This was done by systematically moving the loudspeaker in azimuth and elevation to locations where the unit failed to respond. The recording e l e c t r o d e was placed as orthogonalty as possible to the SC surface, and the coordinates of the point of e l e c t r o d e puncture were recorded with the aid of two ocular micrometers. The recording depth of each unit was read from the scale of the hydraulic drive. These two pieces of information e n a b l e d us to d e t e r m i n e the app r o x i m a t e location of the isolated unit inside the SC, RESULTS A total of 188 electrode p e n e t r a t i o n s were performed, but. only 78 p e n e t r a t i o n s e n c o u n t e r e d units
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responding to acoustic stimuli (n = 123 units). Twenty penetrations isolated at least two units. All units were isolated at depths between 98 and 1062/~m, with most (102 units, 83%) between 231 and 1000 ktm. The basic response properties of these units were similar to those described previously14,31.
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For convenience, the response area measured with a stimulus intensity at 2 dB above the lowest MT (measured at the response center) of a unit is referred to as a 2-dB response area. Similarly, areas measured with stimulus intensities at 5, 10, 15 and 20 dB above the lowest MT are referred to as 5-dB, 10-dB, 15-dB and 20-dB response areas, respectively. The response area of a unit was defined in azimuth and elevation and it generally expanded with the stimulus intensity (Fig. 3). Although the expansion was not always even in all directions, it generally cov-
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ered a large portion of the auditory space in which the response center of the unit was located. With the exception of 8 20-dB response areas, the response areas were circular or elliptical (Fig. 3). The 20-dB response areas of 8 units expanded so much that a portion of them could not be measured (e.g. Fig. 3D). The mean increase in the size of response area of the SC units with stimulus intensity is shown in Fig. 4. Only 3 units were found (e.g. Fig. 3A) which were highly sensitive to signal direction so that their response areas expanded to a lesser degree than others (e.g. Fig. 3 B - D ) . All correlations between the size of 5-dB response areas and the MTs, BFs, or recording depths of 88 units were very poor (Fig. 5), The response center of a unit is not always the geometric center of its response area (Fig. 3). The recording sites and response centers of all 123 units are shown in Fig. 6. In general, response centers of right SC units are in the left auditory space and those of left SC units are in the right auditory space. The response centers of 7 units are within 2 ° in azimuth and 4 ° in elevation of the auditory space. Those of the remaining 116 units are within 60 ° in azimuth and 30 ° in elevation of the auditory space, but most (80 units, 69%) are within 30 ° in both azimuth and elevation (Fig. 6B).
Response areas of units isolated within electrode penetrations A m o n g the electrode penetrations which isolated more than one unit, 9 isolated two units, 6 isolated 3 units, two isolated 4 units, and 3 isolated 5 units. The
response centers and 5-dB response areas of sequentially encountered units of two representative penetrations are shown in Fig. 7. The shape, size, and response center of the response area vary among units isolated within each penetration. There is no clear correlation between the size of the response area and the BF or recording depth of each unit. However. (it is interesting to note that) the variation of response centers among sequentially encountered units was smaller than 14.2 +_ 8.19 ° in azimuth and 7.9 + 6.2 ° in elevation. In other words, units isolated from the same electrode penetration generally responded to a c o m m o n portion of the auditory space.
Auditory space representation It is clear that every SC auditory unit is most sensitive to a sound placed at a specific point in the auditory space of the bat (Fig. 6). However• the representation of the auditory space in the SC does not appear to be systematic. For example, as the electrode was moved posteroanteriorly in the right SC (i.e. from a to d in Fig. 6), the response centers of sequentially encountered units did not systematically shift positions in the left auditory space. The same phen o m e n o n was observed as the electrode was moved mediolateratty as well as posteroanteriorly in the left SC (i.e. from e to j, and k to m in Fig. 6). Thus, response centers of sequentially encountered units did not shift in a predictable manner in the right auditory space either. This unpredictable and unsystemauc representation of auditory space is also evident in the correlation of the electrode positions of the response centers of units encountered in the same bat (Fig. 8).
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In order to quantitatively examine the r e p r e s e n t a t i o n of the auditory space in the SC, the correlation of the response centers of the isolated units with the posteroanterior, mediolateral and dorsoventral axes of the SC were studied. It is clear that all correlations are very p o o r (Fig. 9). DISCUSSION
of
O u r study demonstrates that each of the SC units Eptesicusfuscus is maximally tuned to an acoustic
stimulus p r e s e n t e d at a specific point in the auditory space. H o w e v e r , the point-to-point representation of the auditory space in the SC of bats differs from that of units in the optic tectum of owls. In an owl, the sizes and locations of auditory response areas of tectal units are unaffected by stimulus intensity and the auditory space is r e p r e s e n t e d topographically in the tectum 16. In a bat, the response center of an SC unit remains unchanged, but the size of its response area expands with stimulus intensity (Figs. 3 and 4). Furthermore, a systematic r e p r e s e n t a t i o n of the audito-
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ry space on the SC is not evident (Figs. 6 and 8). The locations of response centers of SC units in the auditory space do not correlate with the recording sites of the units in the m e d i o l a t e r a l , p o s t e r o a n t e r i o r , and dorsoventral axes of the SC ( F i g t)). Studies of the p r i m a r y auditory cortex 2] and inferior colliculus 24 of cats report similar findings, In ~ study of the binaural p r o p e r t i e s and auditory response areas of d e e p SC units of cats. Wise and Itvine32 suggest that an auditorx representation of space in the SC of a cat is unlikely. O u r ongoing study of the inferior colliculus of Epteszcusfuscus also suggests that such an auditory m a p of space in this nucleus is unlikely. On the one hand, we suggest that differences m the auditory space r e p r e s e n t a t i o n may be attributed to the fact that bats and cats have highly mobile external pinnae During localization of an echo source, conjunctive and/or disjunctive movements of pinnae by a b a t would change the relationship between interaural intensity difference and the angle of incidence of a sound source, which would shift the response center of an SC unit in the auditory space. Thus, an animal with highly mobile external ears may not need a precise auditory space m a p in its neural tissue for sound localization. On the other hand. it is also possible that an auditory spatial m a p may indeed exist in the SC of a bat, but such a m a p may be a subtle and complicated one with built-in corrections for ear position. Perhaps, one should look for a m a p only a m o n g the sharply directional units (e.g. Fig. 3A). H o w e v e r , the fact that only 3 such units were e n c o u n t e r e d in this study makes it difficult for us to reach a conclusion about such a h3 pothesis. The response centers of sequentially e n c o u n t e r e d units within an electrode p e n e t r a t i o n were all l o c a t e d within a c o m m o n p o r u o n of the auditory space (Fig. 7), Since electrodes were inserted orthogonally to the surface of the SC. it is t e m p t i n g to suggest that units with similar response centers are aggregated along the dorsoventral axis of the SC. H o w e v e r . there were only 20 penetrations which isolated m o r e than two units and most of the auditory units encountered from one SC had their response centers located within a comparatively small portion of the contralateral auditory space of the bat (Fig. 6L Thus. it is difficult to decide if this observation is valid o r purely coincidental.
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The nearly symmetrical distribution of the response centers of SC units in a limited portion of the right and left half of the auditory space suggests a symmetrical representation of the auditory space in the left and right SC (Fig. 6). Since the response areas of SC units expand with sound intensity (Figs. 3 and 4), these units certainly can be activated by an intense sound placed within a large portion of the auditory space. The maximal sensitivity of the echolocation system of a bat is within a rather limited space of about 30 ° cone shape which extends outward from the bat's mouth9,23, 25. In the present study, the response centers of most SC units were located within the same limited portion of the auditory space of the bat (Fig. 6). If the SC of a bat is involved in orienting
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the bat toward a sound source as in other animals]l, 17, our study suggests that the SC of a bat can orient the animal toward the most sensitive space of its echolocation system. ACKNOWLEDGEMENTS
This work was supported by a grant from the National Science Foundation (BNS 80-07348), a Research Career Development Award from the National Institutes of Health (USPH 1-K04-NS-00433) to P.H.-S. Jen. We thank Dr. G. Summers for comments and correcting the English in this paper. We also thank Mr. W. P. Zhang, Ms. G. H. Gu and R. Dalke for their technical assistance.
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33
34
The visuotopic organization of the superior colliculus of the owl monkey (Aotus mvirgatusl and the bush baby (Galago senalgalensis)+ Brain Research, 60 (1973) 335-349. Middlebrooks. J. C. and Pettigre~v. J D.. Functional class+ es of neurons m primary auditory cortex of the cat distinguished by sensitivity to sound location..I. Neurosci.. I (1978+ 107-120. Palmer, A. R. and King, A. J.. The representatton ot audttory space in the mammalian superior colliculus. Nature ~Lond. ), 299 11982) 248-249. Schnitzler. H.-H. and Grinnell, A. D.. Directional senmtivitv of echolocation in the horseshoe bat Rhinolophus ferrumequinum. I. Directionality of sound emission. J. comp. Physiol., 116 ~1977) 51-61 Semple. M. N.. Aitkin. K. M.. (altord. M B.. Pettigrew. J. D and Phillips. D. P. Spatial receptive fields in the cat inferior colliculus. Hear. Res. 10 Et983) 203-215. Shimozawa. T.. Suga, N.. Hendtet. I'+ and Schuetzc. S.. Directional sensitivity of echolocating system in bats producing frequency-modulated signals, I exp. Biol. 60 (1974) 53-59. Siminoff. R.. Schwassermann, H. O. and Kruger, L.. An electrophysiological study of the visual projection to the superior colliculus of the rat. J. comp. Neurol. 127 (1966~ 435-444 Sprague. J. M. and Meikle. T. H . J~+. The role of the superior colliculus in visually guided behaviour_ Exp. Neuroi.. 11 (1965) 115-146. Stein. B. E.. Goldberg, S. J. andClamann. H. P.. The control of eve movement by the superior collicutus in the alert cat. Brain Research. 118 ~19761 469-474. Stein. B E.. Magalhaes-Castro. B. and Kruger, L.. Superior colliculus: visuotopic-somatotopic overlap, Science. 189 (19751 224-226. Tiao. Y. C. and Blakemore. C.. Functional organization in the superior colliculus of the golden hamster. J. comp. Neurol.. 168 (1976) 483-504. Sun. X.. Jen. P H.-S. and Kamada, F., Neurons in the superior colliculus of echolocating bats respond to ultrasonic signals. Brain Research. 275 (t983) 148-152 Wise. L. Z and Irvine, D. R. F., Auditory response properties of neurons in deep layers of cat superior collieulus, J Neurophysiol., 49 {1983) 674-685. Wurtz. R H. and Albano. J. E.. Visuo-motor function ot the primates superior colliculus. Ann. Rev. Neurosci.. 3 t 1980) 189-226. Wurtz. R H and Goldberg. M. E,, Superior colliculus cell responses related to eye movements in awake monkeys, Science. t71 (1971~ 82-84.
Brain Research, 311 (1984) 289-296 Elsevier BRE 10350
Auditory Space Representation Big Brown Bat,
in t h e S u p e r i o r C o l l i c u l u s o f t h e
Eptesicus fuscus
TATEO SHIMOZAWA*, XINDE SUN** and PHILIP H.-S. JEN
Division of Biological Sciences, The University of Missouri, Columbia, MO 65211 (U.S.A.) (Accepted March 6th, 1984)
Key words: superior colliculus - - bats - - auditory response areas - - auditory space
The auditory response areas of 123 superior collicular (SC) units of Eptesicusfuscus were studied under free-field acoustic stimulus conditions. A stimulus was delivered from a loudspeaker placed 14 cm in front of a bat. The best frequency of a unit was determined by changing the stimulus frequency until the minimum threshold was measured. A best frequency stimulus was then delivered as the loudspeaker was moved across the auditory space to determine the response center of the auditory response area of each unit. The response center was defined as the direction at which the unit had its lowest minimum threshold. The stimulus intensity was then raised 2-20 dB above the lowest minimum threshold of the unit and the response area for each stimulus intensity was determined. The response area of a unit expands with stimulus intensity, but the expansion is not even in all directions. The size of the response area of a unit does not correlate with its minimum threshold, best frequency, or recording depth. Response centers of 7 units were located directly in front of the animal, but most response centers were located in a limited portion of the contralateral auditory space. Although each unit has a response center which is the point of maximal sensitivity, the point-to-point representation of the auditory space is not systematically organized. We suggest that an animal with highly mobile external pinnae may not need an orderly auditory space map in its neural tissue for accurate sound localization. INTRODUCTION
The superior colliculus (SC) of vertebrates is a multimodal integration center which is involved in orienting the head, eyes, and pinnae toward different sensory stimuli10,ll,27,2s,33,34. Topographic projections of the primary receptors of the visual and somatosensory systems on the SC of various animals have b e e n demonstrated2-SA2,15,17-20,26,29,30. Recent studies on guinea pigs 22 and barn owls 16 indicate that the auditory space is systematically represented in the deep layers of the SC, but a study of the SC of cats 32 suggests that such an auditory map is unlikely to be found. Although the visual centers of bats are generally poorly developed, the SC is an exceptionl. Most basic auditory response properties of SC units of the
FM bat, Eptesicusfuscus, are similar to those of inferior collicular (IC) units ~3. However, SC units are not tonotopically organized along the dorsoventral axis and are more sensitive to frequency modulated signals than are IC unitsl4, 31. Under free-field stimulation conditions, we examined the auditory response areas of SC units to determine if there is a systematical auditory space representation in the SC of EptesiCUSfUSCI2S. MATERIALS AND METHODS
Each of 10 FM bats, Eptesicus fuscus (b.wt. 14.4-24.5 g) was anesthetized with Nembutal (45-50 mg/kg b.wt.) for surgery. The bat was tied to a metal plate and the flat head of a nail (1.8 cm) was mounted on the exposed anterior portion of the bat's
* Present address: Zoological Institute, Faculty of Science, Hokkaido University, Hokkaido, Japan. ** Present address: Department of Biology, East China Normal University, Shanghai, People,s Republic of China. Correspondence and reprint requests: P. H.-S. Jen, Division of Biological Sciences, The University of Missouri, Columbia, MO 65211, U.S.A. 0006-8993/84/$03.00 © 1984 Elsevier Science Publishers B.V.
290 skull with dental cement and acrylic glue. The head was then immobilized by fixing the shank of the nail with a set screw. The bat's h e a d was o r i e n t e d t o w a r d a l o u d s p e a k e r with the intersection of its inter-ear line and medial plane corresponding to 0 ° in azimuth and 0 ° in elevation of the bat's auditory space (Fig. 1). Acoustic stimuli (4 ms d u r a t i o n , 0.5 ms rise-decay times) were delivered from a c o n d e n s o r l o u d s p e a k e r ( A K G Model C K 50. d i a m e t e r 2 cm, weight 1.3 g) placed 14 cm in front of the bat's head. The loudspeaker was attached to an aluminum arm and could be placed at any position within 90 ° in azimuth and 50 ° in elevation of the bat's auditory space (Fig. 1). The position of the l o u d s p e a k e r was remotely controlled by two i n d e p e n d e n t servo-controlled motors and was m o n i t o r e d by an oscilloscope outside the sound p r o o f room. The l o u d s p e a k e r was calibrated with a Br/Jel and K j a e r 0.25 inch m i c r o p h o n e placed at the bat's ear. O u t p u t was expressed in dB SPL referred to a 0.0002 dyne/cm z root mean square. A f t e r a small hole was m a d e in the bat's skull, a 3 M KCI glass pipette electrode was inserted into the SC surface to record neural activity E l e c t r o d e s were placed on the central portion of the SC in o r d e r to avoid puncturing the surrounding large b l o o d vessels (Fig. 2). The hole was subsequently enlarged to place electrodes at many places inside the SC. Additional anesthetic (one third of the original dose) was administered during the later phase of the recording, when necessary. R e c o r d e d signals were amplified and sent to an oscilloscope and an audio monitor. All recordings were conducted in a sound p r o o f r o o m ( 3 5 - 3 8 °C). W h e n
an SC unit responding to acoustic stimuli d e l i v e r e d in front of the bat was e n c o u n t e r e d , stimulus frequency was adjusted to a specific value (the best frequency, BF) at which the stimulus intensity required for elicrang a response from the unit was m i n i m u m ~the m i n i m u m threshold, MT). Then, an acoustic stimulus set at the BF and M T of the umt was delivered from the l o u d s p e a k e r as it was moved across the auditory space of the bat. The stimulus intensity was adjusted to d e t e r m i n e the point of maximal sensitivity (referred to as the response center) whithin the response area of the unit at which the M T was the lowest. The response area was m e a s u r e d for at least two stimulus intensities above the lowest MT of the unit. This was done by systematically moving the loudspeaker in azimuth and elevation to locations where the unit failed to respond. The recording e l e c t r o d e was placed as orthogonalty as possible to the SC surface, and the coordinates of the point of e l e c t r o d e puncture were recorded with the aid of two ocular micrometers. The recording depth of each unit was read from the scale of the hydraulic drive. These two pieces of information e n a b l e d us to d e t e r m i n e the app r o x i m a t e location of the isolated unit inside the SC, RESULTS A total of 188 electrode p e n e t r a t i o n s were performed, but. only 78 p e n e t r a t i o n s e n c o u n t e r e d units
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responding to acoustic stimuli (n = 123 units). Twenty penetrations isolated at least two units. All units were isolated at depths between 98 and 1062/~m, with most (102 units, 83%) between 231 and 1000 ktm. The basic response properties of these units were similar to those described previously14,31.
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For convenience, the response area measured with a stimulus intensity at 2 dB above the lowest MT (measured at the response center) of a unit is referred to as a 2-dB response area. Similarly, areas measured with stimulus intensities at 5, 10, 15 and 20 dB above the lowest MT are referred to as 5-dB, 10-dB, 15-dB and 20-dB response areas, respectively. The response area of a unit was defined in azimuth and elevation and it generally expanded with the stimulus intensity (Fig. 3). Although the expansion was not always even in all directions, it generally cov-
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ered a large portion of the auditory space in which the response center of the unit was located. With the exception of 8 20-dB response areas, the response areas were circular or elliptical (Fig. 3). The 20-dB response areas of 8 units expanded so much that a portion of them could not be measured (e.g. Fig. 3D). The mean increase in the size of response area of the SC units with stimulus intensity is shown in Fig. 4. Only 3 units were found (e.g. Fig. 3A) which were highly sensitive to signal direction so that their response areas expanded to a lesser degree than others (e.g. Fig. 3 B - D ) . All correlations between the size of 5-dB response areas and the MTs, BFs, or recording depths of 88 units were very poor (Fig. 5), The response center of a unit is not always the geometric center of its response area (Fig. 3). The recording sites and response centers of all 123 units are shown in Fig. 6. In general, response centers of right SC units are in the left auditory space and those of left SC units are in the right auditory space. The response centers of 7 units are within 2 ° in azimuth and 4 ° in elevation of the auditory space. Those of the remaining 116 units are within 60 ° in azimuth and 30 ° in elevation of the auditory space, but most (80 units, 69%) are within 30 ° in both azimuth and elevation (Fig. 6B).
Response areas of units isolated within electrode penetrations A m o n g the electrode penetrations which isolated more than one unit, 9 isolated two units, 6 isolated 3 units, two isolated 4 units, and 3 isolated 5 units. The
response centers and 5-dB response areas of sequentially encountered units of two representative penetrations are shown in Fig. 7. The shape, size, and response center of the response area vary among units isolated within each penetration. There is no clear correlation between the size of the response area and the BF or recording depth of each unit. However. (it is interesting to note that) the variation of response centers among sequentially encountered units was smaller than 14.2 +_ 8.19 ° in azimuth and 7.9 + 6.2 ° in elevation. In other words, units isolated from the same electrode penetration generally responded to a c o m m o n portion of the auditory space.
Auditory space representation It is clear that every SC auditory unit is most sensitive to a sound placed at a specific point in the auditory space of the bat (Fig. 6). However• the representation of the auditory space in the SC does not appear to be systematic. For example, as the electrode was moved posteroanteriorly in the right SC (i.e. from a to d in Fig. 6), the response centers of sequentially encountered units did not systematically shift positions in the left auditory space. The same phen o m e n o n was observed as the electrode was moved mediolateratty as well as posteroanteriorly in the left SC (i.e. from e to j, and k to m in Fig. 6). Thus, response centers of sequentially encountered units did not shift in a predictable manner in the right auditory space either. This unpredictable and unsystemauc representation of auditory space is also evident in the correlation of the electrode positions of the response centers of units encountered in the same bat (Fig. 8).
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In order to quantitatively examine the r e p r e s e n t a t i o n of the auditory space in the SC, the correlation of the response centers of the isolated units with the posteroanterior, mediolateral and dorsoventral axes of the SC were studied. It is clear that all correlations are very p o o r (Fig. 9). DISCUSSION
of
O u r study demonstrates that each of the SC units Eptesicusfuscus is maximally tuned to an acoustic
stimulus p r e s e n t e d at a specific point in the auditory space. H o w e v e r , the point-to-point representation of the auditory space in the SC of bats differs from that of units in the optic tectum of owls. In an owl, the sizes and locations of auditory response areas of tectal units are unaffected by stimulus intensity and the auditory space is r e p r e s e n t e d topographically in the tectum 16. In a bat, the response center of an SC unit remains unchanged, but the size of its response area expands with stimulus intensity (Figs. 3 and 4). Furthermore, a systematic r e p r e s e n t a t i o n of the audito-
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ry space on the SC is not evident (Figs. 6 and 8). The locations of response centers of SC units in the auditory space do not correlate with the recording sites of the units in the m e d i o l a t e r a l , p o s t e r o a n t e r i o r , and dorsoventral axes of the SC ( F i g t)). Studies of the p r i m a r y auditory cortex 2] and inferior colliculus 24 of cats report similar findings, In ~ study of the binaural p r o p e r t i e s and auditory response areas of d e e p SC units of cats. Wise and Itvine32 suggest that an auditorx representation of space in the SC of a cat is unlikely. O u r ongoing study of the inferior colliculus of Epteszcusfuscus also suggests that such an auditory m a p of space in this nucleus is unlikely. On the one hand, we suggest that differences m the auditory space r e p r e s e n t a t i o n may be attributed to the fact that bats and cats have highly mobile external pinnae During localization of an echo source, conjunctive and/or disjunctive movements of pinnae by a b a t would change the relationship between interaural intensity difference and the angle of incidence of a sound source, which would shift the response center of an SC unit in the auditory space. Thus, an animal with highly mobile external ears may not need a precise auditory space m a p in its neural tissue for sound localization. On the other hand. it is also possible that an auditory spatial m a p may indeed exist in the SC of a bat, but such a m a p may be a subtle and complicated one with built-in corrections for ear position. Perhaps, one should look for a m a p only a m o n g the sharply directional units (e.g. Fig. 3A). H o w e v e r , the fact that only 3 such units were e n c o u n t e r e d in this study makes it difficult for us to reach a conclusion about such a h3 pothesis. The response centers of sequentially e n c o u n t e r e d units within an electrode p e n e t r a t i o n were all l o c a t e d within a c o m m o n p o r u o n of the auditory space (Fig. 7), Since electrodes were inserted orthogonally to the surface of the SC. it is t e m p t i n g to suggest that units with similar response centers are aggregated along the dorsoventral axis of the SC. H o w e v e r . there were only 20 penetrations which isolated m o r e than two units and most of the auditory units encountered from one SC had their response centers located within a comparatively small portion of the contralateral auditory space of the bat (Fig. 6L Thus. it is difficult to decide if this observation is valid o r purely coincidental.
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The nearly symmetrical distribution of the response centers of SC units in a limited portion of the right and left half of the auditory space suggests a symmetrical representation of the auditory space in the left and right SC (Fig. 6). Since the response areas of SC units expand with sound intensity (Figs. 3 and 4), these units certainly can be activated by an intense sound placed within a large portion of the auditory space. The maximal sensitivity of the echolocation system of a bat is within a rather limited space of about 30 ° cone shape which extends outward from the bat's mouth9,23, 25. In the present study, the response centers of most SC units were located within the same limited portion of the auditory space of the bat (Fig. 6). If the SC of a bat is involved in orienting
REFERENCES l Baron, G., Signification 6co-6thologique du d6veloppement allom6trique des deux syst6mes visuels chez les chiropt~res, Rev. canad. Biol., 36 (1977) 1-16. 2 Cynader, M. and Berman, N., Receptive-field organization of monkey superior colliculus, J. Neurophysiol., 35 (1972) 187-201. 3 Dr/iger, U. C. and Hubel, D. H., Responses to visual stimu-
the bat toward a sound source as in other animals]l, 17, our study suggests that the SC of a bat can orient the animal toward the most sensitive space of its echolocation system. ACKNOWLEDGEMENTS
This work was supported by a grant from the National Science Foundation (BNS 80-07348), a Research Career Development Award from the National Institutes of Health (USPH 1-K04-NS-00433) to P.H.-S. Jen. We thank Dr. G. Summers for comments and correcting the English in this paper. We also thank Mr. W. P. Zhang, Ms. G. H. Gu and R. Dalke for their technical assistance.
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