EXPERIMENTAL
NEUROLOGY
Click-Evoked
62, 501-509 (1978)
Response at the Superior Colliculus WILLIAM
Department
of Psychology, Received
Lehigh
of the Cat
H. ATKINSON 1 University, Bethlehem,
Pewsylvania
November 9,1976; revision received August
18015
1,1978
Click-evoked response was recorded from deep layers of the superior colliculus of the cat for stimuli from 67 through 115 db SPL. The response was a biphasic waveform with a sharp initial negative peak. Magnitude of response as a function of intensity was a nonmonotonic function which could be fit by a theoretical equation based upon the interplay of excitatory and inhibitory processes. This equation yields Stevens’s power law as a special case.
INTRODUCTION Until recent years, the superior colliculus was considered as a vestigal component of the visual system. However, a considerable body of contemporary research has focused upon this nucleus and it now appears that it plays a major role in the orientation of the organism to the spatial position of a stimulus. Most of those studies were concentrated on the visual function of the superior colliculus. During the past decade, however, a growing accumulation of anatomical and electrophysiological research has pointed to the presence of auditory function in the deep layers of the superior colliculus. Woolard and Harpman (46)) Moore and Goldberg (23, 24), Powell and Hatton (27)) Diamond, Jones, and Powell ( 11) , Harting et al. (17), and Oliver and Hall (25) reported projections from the inferior colliculus to the superior colliculus. Pathways from auditory cortex were noted by Whitlock and Nauta (44), Garey et al. ( 15), Diamond et al., (11)) Siegel et al., (30), Harting et al. (17), and Paula-Barbosa and Sousa-Pinto (26). There were a number of reports that auditory stimulation produced electrical activity in the superior colliculus. (1, 9, 10, 12, 13, 16, 18-22, 1 I wish to thank my wife Ingrid for her assistance in the measurement of records, in the calculation of statistics, and in the preparation of Fig. 1. 501
All
0014-4886/78/0623-0521$002.00/0 Copyright Q 1978 by Academic Press, Inc.
rights
of reproduction
in any
form
reserved.
502
WILLIAM
H.
ATKINSON
29, 31-33, 35-38, 42, 45). Although all those experiments confirmed the presence of auditory response in the superior colliculus, none of them was focused on the classic variables of frequency and intensity. To fill this gap, a series of experiments was undertaken. The evoked response was selected rather than single-unit activity to provide a measure of the characteristics of a population of neurons. The present report is concerned with the variation in the amplitude of the evoked response as a function of different intensities of click stimulation. An earlier paper (2) described the response at the medial geniculate body under the same conditions. METHODS Stimhtio~t and Recording. A pulse 0.9 ms, in width was fed into the high-gain channel of an audio amplifier. The output of the amplifier was led through an attenuator to a wide-range speaker enclosure mounted in an IAC-shielded room. The speaker was placed about 0.5 m directly in front of the cat. The response of the entire audio system was determined with a Sony ECM-16 Electret Condensor Microphone whose output was coupled directly to a B&K 1460 oscilloscope. The microphone faced the speaker enclosure and was positioned where the right or left pinna would be located. Below 4.5 kHz the response from both positions was equal; for the higher frequencies there was a slight increase at the right placement. The response of the audio system was essentially flat with a lo-db resonant peak at 3.2 kHz. The electrical response of the superior colliculus was observed with a WP Instruments DAM-5 differential preamplifier and amplifier placed in the sound chamber close to the cat. The response of the amplifier spread from 0.1 Hz through the upper portion of the audio range. Outside the room, the signal was split between a monitor oscilloscope and a Fabritek 1052 averager. A condenser shunt was placed across the input of the averager to attenuate high-frequency noise. At the conclusion of each experimental session, the contents of the four channels of the averager were read out on a Heath SR-255B strip chart recorder. Response was measured at six different intensities spaced approximately 10 db apart from 67 to 115 db SPL. Because the memory of the averager could be divided into four channels, only four different intensities could be presented in a given experimental session. Because six items taken four at a time yields fifteen combinations, it was decided that fifteen groups of intensities would be presented. For each cat, five groups were given on each of three experimental days. This design produced ten averaged curves for each of the intensities. Each average was composed of the sum of 32 sweeps. To avoid habituation effects, the intensity was changed after every eight stimulations.
CLICK
RESPONSE
AT
SUPERIOR
COLLICULUS
503
Physiological Procedures. All experiments were conducted with conscious restrained cats. Under Nembutal anesthesia and sterile conditions, the top of the skull was laid bare and a steel bolt was cemented in the frontal sinus. A cement cap was constructed which held two nylon bolts as well as stainless-steel electrode guides. The three bolts were used to immobilize the cat in the stereotaxic frame during later recording sessions. Following a recovery period of several weeks, the cats were taken into the experimental room and fastened with the bolts so that they occupied the same position as during surgery. This procedure was repeated on subsequent days until the cats grew accustomed to the restraint. The cats exhibited no discomfort from this restriction and were used for repeated experiments spanning a period of months. Through a guide over the target site, a stainless-steel electrode of No. 32 Epoxylite-insulated wire was lowered into position. When the tip was close to the calculated depth, potentials evoked by auditory stimulation were monitored to determine the optimal position. The electrode was then cemented into place. At the conclusion of the experiments, the deeply anesthetized cats were perfused with saline and formalin solutions. Several months later, the electrodes were removed and the brains were extracted from the skulls. After the brains were frozen and sliced, sections were photographically enlarged to determine the positions of the recording and reference electrodes. Cat NT had a concentric bipolar electrode in the right superior colliculus at anterior 3.0 and lateral 5.0. The tip was at a depth of 3.0 and the reference on the sheath was 3 mm above. For cat WP the active electrode was in the left superior colliculus at anterior 2.5 and lateral 3.0. The position of the tip could not be accurately determined because the section sp!it along the track during processing ; the calculated depth was 6.0. The reference electrode was placed in the right superior colliculus. Its position could not be confirmed histologically but was calculated to have been at anterior 2.5 and lateral 3.0 with a depth of 5.0. For both animals, the active electrode was in or near the deep layers of the superior colliculus. RESUI>TS The response was a biphasic wave with an initial negative component (N1) followed by a positive peak (PI). Latency was independent of intensity. The polarity of the response was verified by observation of the monopolar response from the active electrode with reference to the bolt cemented in the skull. Table 1 lists the means, medians, and standard deviations of the peak-to-peak amplitudes. Because the distributions were skewed, medians were selected as the
504
WILLIAM
H.
TABLE
PI - Nt Amplitude Cat
Intensity (db SPL)
Man
ATKINSON
1 in Microvolts Median
Standard deviation
NT
115 105 96 86 77 67
140.4 118.6 79.6 51.8 30.9 23.6
139.8 112.8 76.5 51.8 30.1 20.5
4.49 2.51 2.64 1.65 1.38 1.55
WP
115 105 96 86 77 67
116.3 163.0 152.2 116.5 70.1 46.5
111.2 149.8 139.0 91.9 61.0 40.9
3.22 7.55 6.61 4.58 4.58 2.07
measure of central tendency. The results for both animals could be represented by a theoretical equation introduced in an earlier paper (2). However, although the sound pressures delivered to the pinnae were the same for both animals, it is probable that the actual energy transmitted to the cochleas of each animal was different. In addition, the different configurations of the recording electrodes made it likely that the amplitudes of the evoked responsewould differ between the two animals. To transform the data to a common scale, log (P, -N1) was plotted as a function of the intensity expressed in decibels with the points for each animal on a separate graph. When the points were superimposed, they fell on a single smooth curve. To bring the two sets of points into register, it was necessary to subtract 15 db from the abscissavalues for cat NT and to add 0.01 log units to the ordinate. In a mathematical sense,this physical operation of superimposition is equivalent to multiplying PI -Nl and click amplitude by constants. The combined values are presented in Fig. 1, where the relative median magnitude of PI -N1 is plotted as a function of the cube root of the relative click amplitude. The reason for this particular choice of axes will be explained in the following discussion. DISCUSSION Nonmonotonic functions similar to that depicted in Fig. 1 are frequently observed in auditory electrophysiology. Wever and Bray (43) and Fernandez et al. (14) noted maxima in the cochlear microphonic. Carlier and Puiol (8) reported this effect in the action potential of the auditory nerve
CLICK
RESPONSE
AT
SUPERIOR
505
COLLICULUS
in kittens. Boudreau (6) observed it at the medial superior olive, and Tsuchitani and Boudreau (41) noted the presence of maxima at the lateral superior olive. Maxima were reported at the inferior colliculus by Rose et al. (28), at the medial geniculate by Atkinson (2)) and in the auditory cortex by Brugge et al. (7). The appearance of a maximum suggests the presence of some process which attenuates the excitatory effect of the stimulus. One possible mechanism could be movements of the pinna or contractions of the muscles of the middle ear. The reaction time of muscles is of the order of tens of milliseconds. Although this could be a factor in response at the superior colliculus, it could not account for maxima at the lower levels of the auditory system, where the reaction time is of the order of milliseconds. Therefore it seems to be more reasonable to conclude that the response at the superior colliculus reflects processes which are also present at lower levels of the auditory chain. A recent paper presented evidence relevant to the physiological basis for the occurrance of maxima. Carlier and Pujol (8) reported that the maximum appeared in recordings from the auditory nerve of kittens at
l NT
0 WP 100 -
.2 CUBE
.6
.4 ROOT
OF
CLICK
.6
1.0
AMPLITUDE
FIG. 1. Relationship between the peak-to-peak magnitude of the click-evoked response at the superiorcolliculus and the cube root of the click amplitude. On the abscissa, 1.0 represents the reference value of 115 db SPL for cat WP. Units on the ordinate are relative and scaled so that the maximum of the curve occurs at 100.
506
WILLIAM
H.
ATKINSON
approximately the 13th day of postnatal development. They noted that this is the same time when the outer hair cell system of the cochlea is nearing maturity. Both excitatory and inhibitory effects can frequently be observed at a particular recording site. This suggests that the form of the function in Fig. 1 may be the resultant of the interplay of excitatory and autoinhibitory processes. This interpretation forms the basis for the theoretical equation represented by the solid line in Fig. 1. The equation of this line is PI--N1
= 215(A0.33-0.03)
10-0.48A,
where PI-N1 is the relative peak-to-peak magnitude of the evoked response and A is the relative amplitude or sound pressure of the click. In this equation, the magnitude of the evoked response is expressed as the product of excitatory and autoinhibitory processes. The excitatory component is given by the expression
The excitatory process conforms to the power law proposed by Stevens (34), with a subtractive constant reflecting the existence of a threshold. The inhibitory component is given by the term 10~“~48A.It has a value close to unity for low sound pressures, but its magnitude decreases exponentially at the higher levels of sound. Because the relationship between the excitatory and inhibitory processes is multiplicative, the product for suprathreshold stimulation is always positive. However, because the rates of change of the two processes with respect to sound pressure are not proportional, there is a maximum in the magnitude of the evoked potential. The multiplicative relationship between excitatory and inhibitory processes as well as the exponential form of the inhibitory component were first presented in a paper by Beebe-Center et nl. (5) on masking in taste. They found that the diminution in sweetness or saltiness was an exponential function of the concentration of a masking substance. Qualitatively similar effects were observed in studies of lateral inhibition in vision. In a recent paper, Atkinson (4) reported that loudness for speech and for pure tones is an exponential function of the sound pressure level of a masking noise. Atkinson (3) reported that the equation that describes the electrical response at the superior colliculus has the same form with the same exponent as the equation which fits the experimental data on magnitude estimation of stimulation of low to moderate intensity. In that paper, it was also noted that this form of equation with a different exponent can be applied to estimates of the magnitude of taste. This suggests that the equation
CLICK
RESPONSE
AT
SUPERIOR
COLLICULUS
507
describing the points in Fig. 1 may also be a general expression for the psychophysical response. Thus the power law discovered by Stevens (34) can be considered as a special case of a more general psychophysical law. One curious aspect of the form of the evoked response should be noted. The polarity of the response at the superior colliculus is nearly a mirror image of that observed at the medial geniculate body (2). Teas et al. (39) reported that the action potential in the auditory nerve to a click is biphasic with a sharp initial negative peak. Thus the polarity of the response at the periphery is in agreement with that which was observed at the superior colliculus. On the other hand, Thompson et al. (40) noted that the click-evoked response recorded from auditory cortex displays a sharp initial positive response, Thus the polarity of the respotise at the cortex is in agreement with that observed at the medial geniculate body. REFERENCES H. W. 1944. Mid-brain auditory mechanisms in cats. J. NcnropJqsiol. 7 : 415-424. ATKINSON, W. H. 1976. Electrophysiological evidence for Stevens’ power law at the medial geniculate of the cat. Br& Res. 109 : 175-178. ATKINSON, W. H. 1977. A general equation for sensory magnitude. Paper presented at the 48th annual meeting of the Eastern Psychological Association. ATKINSON, W. H. 1979. The growth of loudness in the presence of a masking noise. J. Acozut. Sot. Afrz. Submitted for publication. BEEBE-CENTER, J. G., M. S. ROGERS, W. H. ATKINSON, AND D. N. O’CONNELL. 1959. Sweetness and saltiness of compound solutions of sucrose and NaCl as a function of the concentration of solutes. J. Enp. Psychol. 57: 231-235. BOUDREAU, J. C. 1965. Stimulus correlates of wave activity in the superiorolivary complex of the cat. 1. Arroztsf. Sot. tlm. 37: 779-785. BRUGGE, J. F., N. A. DUBROVSKY, L. M. AITKIN, AND D. J. ANDERSON. 1969. Sensitivity of single neurons in auditory cortex of cat to binaural tone stimulation. J. Nc~~roplz~siol. 32 : 1005-1024. CARLIER, E., AND R. PUJOL. 1978. Role of inner and outer hair cells in coding sound intensity : an ontogenetic approach. Brain Res. 147 : 174-176. COTTER, J. R. 1976. Visual and nonvisual units recorded from the optic tectum of Gallus domesticus. Bra& Bchau. Eejol. 13: l-21. CYNADER, M., AND N. BERMAN. 1972. Receptive field organization of monkey superior colliculus. J. Nczfvoplqsiol. 35 : 187-201. DIAMOND, I. T., E. G. JONES. AND T. P. S. POWELL. 1969. The projection of the auditory cortex upon the diencephalon and brain stem in the cat. Brnirc Res. 15 : 305-340. DRAGER, U. C., AND D. H. HUBEL. 1975. Physiology of visual cells in mouse superior colliculus and correlation with somatosensory and auditory input.
1. ADES, 2.
3. 4. 5.
6. 7.
8.
9. 10. 11.
12.
Nature
13.
(Loftdon)
253 : 203-204.
U. C., AND D. H. HLJBEL. 1975. Responses to visual stimulation and relationship between visual, auditory and somesthetic inputs in mouse superior colliculus. J. Ncz~rophysiol. 38 : 690-713.
DRAGER,
508
WILLIAM
H.
ATKINSON
14. FERNANDEZ, C., R. BUTLER, T. KONISHI, V. HONRUBIA, AND I. TASAKI. 1962. Cochlear potentials in the rhesus and squirrel monkey. 1. Acoust. Sot. Am. 34 : 1411-1417. 15. GAREY, L. J., E. G. JONES, AND T. P. S. POWELL. 1968. Inter-relationships of striate and extrastriate cortex with the primary relay sites of the visual pathway. .I. Ncurol. Neurosurg. Psychiat. 31 : 135-1.57. 16. GORDON, B. 1973. Receptive fields in deep layers of cat superior colliculus. J. Neurophysiol. 36 : 157-178. 17. HARTING, J. K., W. C. HALL, I. T. DIAMOND, AND G. F. MARTIN. 1973. Anterograde degeneration study of the superior colliculus in Tzlpaia glis: evidence for subdivision between superficial and deep layers. J. Camp. Neural. 148: 361368. 18. HORN, G., AND R. M. HILL. 1966. Responsiveness to sensory stimulation of units in the superior colliculus and subjacent tectotegmental regions of the rabbit. Exp. Neural. 14: 199-223. 19. HUMPHREY, N. K. 1968. Responses to visual stimuli of units in the superior colliculus of rats and monkeys. Exp. Neurol. 20: 312-340. 20. JUNGERT, S. 1958. Auditory pathways in the brainstem. Acta. Otolaryngol. Scan& .Su#d. 138: l-67. 21. MASLAND, R. H., K. L. CHOW, AND D. L. STEWART. 1971. Receptive field characteristics of superior colliculus neurons in the rabbit. J. Neurophysiol 34: 148-156. 22. MAST, T. E., AND D. Y. CHUNG. 1973. Binaural interaction in the superior colliculus of the chinchilla. Brain Res. 862.: 227-230. 23. MOORE, R. Y., AND J. M. GOLDBERG. 1963. Ascending projections of the inferior colliculus in the cat. J. Cowzp. NezbroZ. 121 : 109-136. 24. MOORE, R. Y., AND J. M. GOLDBERG. 1966. Projections of the inferior colliculus in the monkey. Exp. Neural. 14: 429438. 25. OLIVER, D. L., AND W. C. HALL. 1975. Subdivisions of the medial geniculate body in the tree shrew (Tzhpaia gZis) . Brain Res. 86 : 217-227. 26. PAULA-BARBOSA, M. M., AND A. SOUSA-PINTO. 1973. Auditory cortical projections to the superior colliculus in the cat. Brain Res. 50: 47-61. 27. POWELL, E. W., AND J. B. HATTON. 1969. Projections of the inferior colliculus in the cat. J. Comp. Neural. 136: 183-192. 28. ROSE, J. E., D. D. GREENWOOD, J. M. GOLDBERG, AND J. E. HIND. 1963. Some discharge characterists of single units in the inferior colliculus of the cat. I. Tonotopical organization, relation of spike counts to tone intensity and firing patterns of single elements. J. Neurophysiol. 26 : 294-320. 29. SHIMIZU, K. 1959. Superior colliculus, its functional significance relative to the optic and auditory systems. Med. J. Osaka U+riv. 10: 39-62. 30. SIEGEL, A., L. SASSO, AND J. P. TASSONI. 1971. Fiber connections of the temporal lobe with the corpus striatum and related structures in the cat. Erp. Neural. 33 : 130-146. 31. STEIN, B. E. 1978. Nonequivalent visual, auditory, and somatic corticotectal influences in cat. .I. Nezdropltysiol. 41 : 55-64. 32. STEIN, B. E., AND M. 0. ARIGBEDE. 1972. Unimodal and multimodal response properties of neurons in the cat’s superior colliculus. Exp. Neurol. 36: 179-196. 33. STEIN, B. E., E. LABOS, AND L. KRUGER. 1973. Sequence of changes in properties of neurons of superior colliculus of the kitten during maturation. J. Neurophysiol.
3’6 : 667-679.
CLICK
34. 35.
36. 37.
38.
RESPONSE
41.
42. 43.
44. 45. 46.
SUPERIOR
COLLICULUS
509
S. S. 1970. Neural events and the psychophysical law. Science 170: 1043-1050. STRASCHILL, M., AND K. P. HOFFMAN. 1968. Relationship between localization and functional properties of movement-sensitive neurons in the cat’s tectum opticum. Braix Res. 8: 382-385. STRASCHILL, M., AND K. P. HOFFMAN. 1969. Functional aspects of localization in the cat’s tectum opticum. Brain Res. 13 : 274-283. SYKA, J., AND M. STRASCHILL. 1970. Activation of superior colliculus neurons and motor responses after electrical stimulation of the inferior colliculus. ExP. Neurol. 28 : 384-392. SYKA, J., AND T. RADIL-WEISS. 1972. Reaction of superior colliculus neurons to binaural clicks and contralateral collicular stimulation in cat. Physiol. Bolre-
%wENS,
7?ZOSlO. 21: 113. 39. TEAS, D. C., D. H. ELDREDGE,
40.
AT
AND H. DAVIS. 1962. Cochlear responses to acoustic transients: an interpretation of whole-nerve action potentials. J. Acoust. Sot. Ant. 34: 1438-1459. THOMPSON, R. F., R. H. JOHNSON, AND J. HOOPES. 1963. Organization of auditory, somatic sensory, and visual projection to association fields of cerebral cortex in the cat. J. Neztrophysiol. 216: 343-364. TSUCHITANI, C., AND J. C. BOUDREAU. 1969. Stimulus level of dichotically presented tones and cat superior olive S segment cell discharge. J. Acoust. Sot. Am. 46 : 979-988. UPDYKE, B. V. 1974. Characteristics of unit responses in superior colliculus of the Cebus monkey. J. NezrvophJ~siol. 37: 896909. WEVER, E. G., AND C. W. BRAY. 1936. The nature of acoustic response: the relation between sound intensity and the magnitude of response in the cochlea. J. Exp. Psyckol. 19: 129-143. WHITLOCK, D. G., AND W. J. H. NAUTA. 1956. Subcortical projections from the temporal neocortex in dlaraca mulafta. J. Cof~zp. Neztrol. 106: 183-212. WICKELGREN, B. G. 1971. Superior colliculus. . some receptive field properties of bimodally responsive cells. Science 173 : 69-72. WOOLARD, H. H., AND J. A. HARPMAN. 1940. The connections of the inferior colliculus and of the dorsal nucleus of the lateral lemniscus. J. Aflat. 74: 441-457.
NEUROLOGY
Click-Evoked
62, 501-509 (1978)
Response at the Superior Colliculus WILLIAM
Department
of Psychology, Received
Lehigh
of the Cat
H. ATKINSON 1 University, Bethlehem,
Pewsylvania
November 9,1976; revision received August
18015
1,1978
Click-evoked response was recorded from deep layers of the superior colliculus of the cat for stimuli from 67 through 115 db SPL. The response was a biphasic waveform with a sharp initial negative peak. Magnitude of response as a function of intensity was a nonmonotonic function which could be fit by a theoretical equation based upon the interplay of excitatory and inhibitory processes. This equation yields Stevens’s power law as a special case.
INTRODUCTION Until recent years, the superior colliculus was considered as a vestigal component of the visual system. However, a considerable body of contemporary research has focused upon this nucleus and it now appears that it plays a major role in the orientation of the organism to the spatial position of a stimulus. Most of those studies were concentrated on the visual function of the superior colliculus. During the past decade, however, a growing accumulation of anatomical and electrophysiological research has pointed to the presence of auditory function in the deep layers of the superior colliculus. Woolard and Harpman (46)) Moore and Goldberg (23, 24), Powell and Hatton (27)) Diamond, Jones, and Powell ( 11) , Harting et al. (17), and Oliver and Hall (25) reported projections from the inferior colliculus to the superior colliculus. Pathways from auditory cortex were noted by Whitlock and Nauta (44), Garey et al. ( 15), Diamond et al., (11)) Siegel et al., (30), Harting et al. (17), and Paula-Barbosa and Sousa-Pinto (26). There were a number of reports that auditory stimulation produced electrical activity in the superior colliculus. (1, 9, 10, 12, 13, 16, 18-22, 1 I wish to thank my wife Ingrid for her assistance in the measurement of records, in the calculation of statistics, and in the preparation of Fig. 1. 501
All
0014-4886/78/0623-0521$002.00/0 Copyright Q 1978 by Academic Press, Inc.
rights
of reproduction
in any
form
reserved.
502
WILLIAM
H.
ATKINSON
29, 31-33, 35-38, 42, 45). Although all those experiments confirmed the presence of auditory response in the superior colliculus, none of them was focused on the classic variables of frequency and intensity. To fill this gap, a series of experiments was undertaken. The evoked response was selected rather than single-unit activity to provide a measure of the characteristics of a population of neurons. The present report is concerned with the variation in the amplitude of the evoked response as a function of different intensities of click stimulation. An earlier paper (2) described the response at the medial geniculate body under the same conditions. METHODS Stimhtio~t and Recording. A pulse 0.9 ms, in width was fed into the high-gain channel of an audio amplifier. The output of the amplifier was led through an attenuator to a wide-range speaker enclosure mounted in an IAC-shielded room. The speaker was placed about 0.5 m directly in front of the cat. The response of the entire audio system was determined with a Sony ECM-16 Electret Condensor Microphone whose output was coupled directly to a B&K 1460 oscilloscope. The microphone faced the speaker enclosure and was positioned where the right or left pinna would be located. Below 4.5 kHz the response from both positions was equal; for the higher frequencies there was a slight increase at the right placement. The response of the audio system was essentially flat with a lo-db resonant peak at 3.2 kHz. The electrical response of the superior colliculus was observed with a WP Instruments DAM-5 differential preamplifier and amplifier placed in the sound chamber close to the cat. The response of the amplifier spread from 0.1 Hz through the upper portion of the audio range. Outside the room, the signal was split between a monitor oscilloscope and a Fabritek 1052 averager. A condenser shunt was placed across the input of the averager to attenuate high-frequency noise. At the conclusion of each experimental session, the contents of the four channels of the averager were read out on a Heath SR-255B strip chart recorder. Response was measured at six different intensities spaced approximately 10 db apart from 67 to 115 db SPL. Because the memory of the averager could be divided into four channels, only four different intensities could be presented in a given experimental session. Because six items taken four at a time yields fifteen combinations, it was decided that fifteen groups of intensities would be presented. For each cat, five groups were given on each of three experimental days. This design produced ten averaged curves for each of the intensities. Each average was composed of the sum of 32 sweeps. To avoid habituation effects, the intensity was changed after every eight stimulations.
CLICK
RESPONSE
AT
SUPERIOR
COLLICULUS
503
Physiological Procedures. All experiments were conducted with conscious restrained cats. Under Nembutal anesthesia and sterile conditions, the top of the skull was laid bare and a steel bolt was cemented in the frontal sinus. A cement cap was constructed which held two nylon bolts as well as stainless-steel electrode guides. The three bolts were used to immobilize the cat in the stereotaxic frame during later recording sessions. Following a recovery period of several weeks, the cats were taken into the experimental room and fastened with the bolts so that they occupied the same position as during surgery. This procedure was repeated on subsequent days until the cats grew accustomed to the restraint. The cats exhibited no discomfort from this restriction and were used for repeated experiments spanning a period of months. Through a guide over the target site, a stainless-steel electrode of No. 32 Epoxylite-insulated wire was lowered into position. When the tip was close to the calculated depth, potentials evoked by auditory stimulation were monitored to determine the optimal position. The electrode was then cemented into place. At the conclusion of the experiments, the deeply anesthetized cats were perfused with saline and formalin solutions. Several months later, the electrodes were removed and the brains were extracted from the skulls. After the brains were frozen and sliced, sections were photographically enlarged to determine the positions of the recording and reference electrodes. Cat NT had a concentric bipolar electrode in the right superior colliculus at anterior 3.0 and lateral 5.0. The tip was at a depth of 3.0 and the reference on the sheath was 3 mm above. For cat WP the active electrode was in the left superior colliculus at anterior 2.5 and lateral 3.0. The position of the tip could not be accurately determined because the section sp!it along the track during processing ; the calculated depth was 6.0. The reference electrode was placed in the right superior colliculus. Its position could not be confirmed histologically but was calculated to have been at anterior 2.5 and lateral 3.0 with a depth of 5.0. For both animals, the active electrode was in or near the deep layers of the superior colliculus. RESUI>TS The response was a biphasic wave with an initial negative component (N1) followed by a positive peak (PI). Latency was independent of intensity. The polarity of the response was verified by observation of the monopolar response from the active electrode with reference to the bolt cemented in the skull. Table 1 lists the means, medians, and standard deviations of the peak-to-peak amplitudes. Because the distributions were skewed, medians were selected as the
504
WILLIAM
H.
TABLE
PI - Nt Amplitude Cat
Intensity (db SPL)
Man
ATKINSON
1 in Microvolts Median
Standard deviation
NT
115 105 96 86 77 67
140.4 118.6 79.6 51.8 30.9 23.6
139.8 112.8 76.5 51.8 30.1 20.5
4.49 2.51 2.64 1.65 1.38 1.55
WP
115 105 96 86 77 67
116.3 163.0 152.2 116.5 70.1 46.5
111.2 149.8 139.0 91.9 61.0 40.9
3.22 7.55 6.61 4.58 4.58 2.07
measure of central tendency. The results for both animals could be represented by a theoretical equation introduced in an earlier paper (2). However, although the sound pressures delivered to the pinnae were the same for both animals, it is probable that the actual energy transmitted to the cochleas of each animal was different. In addition, the different configurations of the recording electrodes made it likely that the amplitudes of the evoked responsewould differ between the two animals. To transform the data to a common scale, log (P, -N1) was plotted as a function of the intensity expressed in decibels with the points for each animal on a separate graph. When the points were superimposed, they fell on a single smooth curve. To bring the two sets of points into register, it was necessary to subtract 15 db from the abscissavalues for cat NT and to add 0.01 log units to the ordinate. In a mathematical sense,this physical operation of superimposition is equivalent to multiplying PI -Nl and click amplitude by constants. The combined values are presented in Fig. 1, where the relative median magnitude of PI -N1 is plotted as a function of the cube root of the relative click amplitude. The reason for this particular choice of axes will be explained in the following discussion. DISCUSSION Nonmonotonic functions similar to that depicted in Fig. 1 are frequently observed in auditory electrophysiology. Wever and Bray (43) and Fernandez et al. (14) noted maxima in the cochlear microphonic. Carlier and Puiol (8) reported this effect in the action potential of the auditory nerve
CLICK
RESPONSE
AT
SUPERIOR
505
COLLICULUS
in kittens. Boudreau (6) observed it at the medial superior olive, and Tsuchitani and Boudreau (41) noted the presence of maxima at the lateral superior olive. Maxima were reported at the inferior colliculus by Rose et al. (28), at the medial geniculate by Atkinson (2)) and in the auditory cortex by Brugge et al. (7). The appearance of a maximum suggests the presence of some process which attenuates the excitatory effect of the stimulus. One possible mechanism could be movements of the pinna or contractions of the muscles of the middle ear. The reaction time of muscles is of the order of tens of milliseconds. Although this could be a factor in response at the superior colliculus, it could not account for maxima at the lower levels of the auditory system, where the reaction time is of the order of milliseconds. Therefore it seems to be more reasonable to conclude that the response at the superior colliculus reflects processes which are also present at lower levels of the auditory chain. A recent paper presented evidence relevant to the physiological basis for the occurrance of maxima. Carlier and Pujol (8) reported that the maximum appeared in recordings from the auditory nerve of kittens at
l NT
0 WP 100 -
.2 CUBE
.6
.4 ROOT
OF
CLICK
.6
1.0
AMPLITUDE
FIG. 1. Relationship between the peak-to-peak magnitude of the click-evoked response at the superiorcolliculus and the cube root of the click amplitude. On the abscissa, 1.0 represents the reference value of 115 db SPL for cat WP. Units on the ordinate are relative and scaled so that the maximum of the curve occurs at 100.
506
WILLIAM
H.
ATKINSON
approximately the 13th day of postnatal development. They noted that this is the same time when the outer hair cell system of the cochlea is nearing maturity. Both excitatory and inhibitory effects can frequently be observed at a particular recording site. This suggests that the form of the function in Fig. 1 may be the resultant of the interplay of excitatory and autoinhibitory processes. This interpretation forms the basis for the theoretical equation represented by the solid line in Fig. 1. The equation of this line is PI--N1
= 215(A0.33-0.03)
10-0.48A,
where PI-N1 is the relative peak-to-peak magnitude of the evoked response and A is the relative amplitude or sound pressure of the click. In this equation, the magnitude of the evoked response is expressed as the product of excitatory and autoinhibitory processes. The excitatory component is given by the expression
The excitatory process conforms to the power law proposed by Stevens (34), with a subtractive constant reflecting the existence of a threshold. The inhibitory component is given by the term 10~“~48A.It has a value close to unity for low sound pressures, but its magnitude decreases exponentially at the higher levels of sound. Because the relationship between the excitatory and inhibitory processes is multiplicative, the product for suprathreshold stimulation is always positive. However, because the rates of change of the two processes with respect to sound pressure are not proportional, there is a maximum in the magnitude of the evoked potential. The multiplicative relationship between excitatory and inhibitory processes as well as the exponential form of the inhibitory component were first presented in a paper by Beebe-Center et nl. (5) on masking in taste. They found that the diminution in sweetness or saltiness was an exponential function of the concentration of a masking substance. Qualitatively similar effects were observed in studies of lateral inhibition in vision. In a recent paper, Atkinson (4) reported that loudness for speech and for pure tones is an exponential function of the sound pressure level of a masking noise. Atkinson (3) reported that the equation that describes the electrical response at the superior colliculus has the same form with the same exponent as the equation which fits the experimental data on magnitude estimation of stimulation of low to moderate intensity. In that paper, it was also noted that this form of equation with a different exponent can be applied to estimates of the magnitude of taste. This suggests that the equation
CLICK
RESPONSE
AT
SUPERIOR
COLLICULUS
507
describing the points in Fig. 1 may also be a general expression for the psychophysical response. Thus the power law discovered by Stevens (34) can be considered as a special case of a more general psychophysical law. One curious aspect of the form of the evoked response should be noted. The polarity of the response at the superior colliculus is nearly a mirror image of that observed at the medial geniculate body (2). Teas et al. (39) reported that the action potential in the auditory nerve to a click is biphasic with a sharp initial negative peak. Thus the polarity of the response at the periphery is in agreement with that which was observed at the superior colliculus. On the other hand, Thompson et al. (40) noted that the click-evoked response recorded from auditory cortex displays a sharp initial positive response, Thus the polarity of the respotise at the cortex is in agreement with that observed at the medial geniculate body. REFERENCES H. W. 1944. Mid-brain auditory mechanisms in cats. J. NcnropJqsiol. 7 : 415-424. ATKINSON, W. H. 1976. Electrophysiological evidence for Stevens’ power law at the medial geniculate of the cat. Br& Res. 109 : 175-178. ATKINSON, W. H. 1977. A general equation for sensory magnitude. Paper presented at the 48th annual meeting of the Eastern Psychological Association. ATKINSON, W. H. 1979. The growth of loudness in the presence of a masking noise. J. Acozut. Sot. Afrz. Submitted for publication. BEEBE-CENTER, J. G., M. S. ROGERS, W. H. ATKINSON, AND D. N. O’CONNELL. 1959. Sweetness and saltiness of compound solutions of sucrose and NaCl as a function of the concentration of solutes. J. Enp. Psychol. 57: 231-235. BOUDREAU, J. C. 1965. Stimulus correlates of wave activity in the superiorolivary complex of the cat. 1. Arroztsf. Sot. tlm. 37: 779-785. BRUGGE, J. F., N. A. DUBROVSKY, L. M. AITKIN, AND D. J. ANDERSON. 1969. Sensitivity of single neurons in auditory cortex of cat to binaural tone stimulation. J. Nc~~roplz~siol. 32 : 1005-1024. CARLIER, E., AND R. PUJOL. 1978. Role of inner and outer hair cells in coding sound intensity : an ontogenetic approach. Brain Res. 147 : 174-176. COTTER, J. R. 1976. Visual and nonvisual units recorded from the optic tectum of Gallus domesticus. Bra& Bchau. Eejol. 13: l-21. CYNADER, M., AND N. BERMAN. 1972. Receptive field organization of monkey superior colliculus. J. Nczfvoplqsiol. 35 : 187-201. DIAMOND, I. T., E. G. JONES. AND T. P. S. POWELL. 1969. The projection of the auditory cortex upon the diencephalon and brain stem in the cat. Brnirc Res. 15 : 305-340. DRAGER, U. C., AND D. H. HUBEL. 1975. Physiology of visual cells in mouse superior colliculus and correlation with somatosensory and auditory input.
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