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A comparison of acoustic nerve and cochlear nucleus responses during acoustic habituation
562
Brain Research, 173 (1979) 562-566 © Elsevier/North-Holland Biomedical Press
A comparison of acoustic nerve and cochlear nucleus responses during acoustic habituation
CHI-MING HUANG and J. S. BUCHWALD Department of Physiology, University of South Alabama, Mobile, Ala. 36688 and Department of Physiology, Mental Retardation Center and Brain Research Institute, UCLA Medical Center, Los Angeles, Calif. 90024 (U.S.A.)
(Accepted May 24th, 1979)
Even though habituation has been viewed as learning in its simplest form 9, the behavioral responses are many and complex and their neurophysiological mechanisms vary not only with the form of the behavior but also with the temporal parameters of the repetitive stimulus. Although many electrophysiological analyses of acoustic habituation have been carried out, general statements are not possible 5. The results obtained with unit vs evoked potential recordings further complicated the interpretation. For example, unit response decrements occur as peripherally as the cochlear nucleus 3, while evoked potential changes do not occur below the thalamic level 17; such data have made conceptualization of the neural substrates relevant to habituation difficult. Other studies on the responses of the acoustic nerve fibers 1°,11,15,19 and neurons in the cochlear nucleus v and superior olive 8 either employed tonal repetition rates exceeding 10/sec, not those typically used in acoustic habituation, or were done under the effect of anesthesia 12-14,18. The use of widely different combinations of stimulus duration and inter-tone interval has further complicated the resolution of these data into a coherent whole. In this report we present multiple unit data on the response decrement of the acoustic nerve (AN) and cochlear nucleus (CN) in unanesthetized cats over temporal parameters for the repetitive acoustic stimulus typically used in acoustic habituation studies. Recordings were carried out on 11 cats. The surgical and recording procedures have been detailed elsewhere 3. Briefly, the cats were initially anesthetized with a mixture of N20, 02 and methoxyflurane. Anesthesia was terminated after a mid-collicular decerebration. The preparation was then paralyzed with Flaxedil 3,4. Recordings of multiple unit activity were made with concentric or bipolar electrodes (15-30 K f~ at 1000 Hz)3,L A silver ball electrode was implanted on the round window to monitor the stability of the cochlear microphonic potentiaP. The entire amplification and recording system had a frequency response range from 30-5000 Hz. Acoustic stimuli were pure tones between 500-5000 Hz. Sound intensities of 70 or 80 dB spl (re 0.0002 dyne/sq. cm) at the central end of the earbar were used. Data analysis of the multiple unit activity was done by a special-purpose integrator circuit described previously 4. The
563
Acoustic Nerve 123
rain
5 I
, ~ ' ~ J ~ '~"~
rain
'
Cochleor Nucleus
i
,
50 sec
'!r,
w
i
control
1.5 sec tones
recovery
3 rain lone recovery
Fig. 1. Typical pattern of multiple unit responses to repetitive tones (1.5 sec tone every 5 sec) and continuous tones (3 min) in the acoustic nerve and the cochlear nucleus. The data were taken from 4 different preparations which showed variations in the signal-to-noise ratio. The acoustic nerve data showed no response decrement during repetitive stimulation, but the spontaneous activity dropped below control level at the end of the continuous tone. In the cochlear nucleus, response decrement could also be seen during repetitive tone stimulation.
removal of the microphonics from the acoustic nerve activities was accomplished through a sharp notch filter (24 dB/octave). The cochlear nucleus responses were free from microphonic contamination and were analyzed without filtering. In a few cases where the filter was used, the results were unchanged. Each experiment involved only one C N and one A N recording site. At the end of the experiment, the recording sites were marked with current and the brain perfused with 10 % formalin. Verification of electrode placement confirmed all 11 A N recording sites. Three C N recording sites were found in anteroventral CN, two in posteroventral CN, and 4 in dorsal CN, two more recording sites were in the border area between anteroventral and posteroventral CN. A typical protocol contained 3 steps. First, five 1.5 sec control test tones were given once every 10 sec. Following a silent period of 30 sec, the second step consisted of 25 tones with a predetermined combination of tone duration and inter-tone interval. In the CN, responses to individual tones generally decreased and reached a steadystate level (Fig. 1). In the AN, the response decrement was less obvious, but the spontaneous activity level was often seen decreased, particularly following prolonged sound stimulation. In the third step, test tones of 1.5 sec duration were given once every 10 sec to monitor the recovery which was exponential or near exponential. Longer periods were necessary for recovery from larger amounts of response decrements. In general, response recovery was complete within 1 min. Each series of 25 responses were fitted to a 5-parameter polynomial and a 95 % confidence band was established. F r o m 187 tone sequences in 11 preparations, the mean width of the confidence band from the center to either the upper or lower 95 %
564 confidence limit was 9.7 ~ 4.5 ~ of the control response. To quantify the m a g n i t u d e o f response modification, the average of the responses to the first 5 c o n t r o l test tones delivered before the tone sequence was defined as the control response. The average o f the response to the last 5 of the 25 tones was defined as the final response. The q u a n t i t y (final/control) was calculated. To determine the statistical significance o f the decrements, K a n d e l l r a n k correlations were carried out for each tone sequence between the n u m b e r of trials (e.g. 1st, 2nd, 3rd . . . . 10th, etc.) a n d the magnitude of response. In Table I, the (final/control) values in the CN a n d the A N , the n u m b e r of tone series carried out, a n d the n u m b e r of tone series with significant response decrements from the K e n d a l l correlation are tabulated with the stimulus parameters. These data were listed in the order of increasing stimulus duty cycle values defined as [(tone d u r a t i o n ) / (tone d u r a t i o n + inter-tone interval)]. A n e x a m i n a t i o n of Table I shows that :(1) in the CN, the p r o p o r t i o n s of runs with significant response decrements increased with stimulus duty cycle whereas no such trend was evident in the A N ; a n d (2) the (final/ control) values decreased with increasing stimulus duty cycle values in the CN, but not in the A N . We next c o m p a r e d the response decrement in different parts of the CN. F o r a given stimulus paradigm, no significant difference could be f o u n d between data from
TABLE I Response decrement in the acoustic nerve and the cochlear nucleus during repetitive tonal stimulation Acoustic nerve
Cochlear nucleus
Tone duration (see)
Intertone- Duty interval cycle (see) (%)
Final/Initial (%)
No. runs
ns*
Final~Initial (%)
No. runs
ns*
1.5 1.5 1.5 1.0 1.5 1.5 0.5 1.5 0.5 1.5 1.5 1.5 2.5 3.5 1.5 4.5 6.5 8.5 25.0
8.5 7.5 6.5 4.0 5.5 4.5 1.5 3.5 1.0 2.5 1.5 1.0 1.5 1.5 0.5 1.5 1.5 1.5 0
104.8 ± 11.6 100.0 100.0 108.0 ± 7.6 100.0 100.0 100.0 100.1 ± 7.0 100.0 96.7 ± 5.6 99.3 i 3.6 100.0 100.0 104.7 ± 8.2 101.2 d- 15.3 100.0 100.0 98.0 ± 6.5 103.7 ± 8.1
28 1 1 3 1 I 1 7 1 6 7 1 1 3 8 1 1 12 11
2 0 0 0 0 0 0 1 0 0 0 0
94.4 k 8.1 98.5 100.1 90.5 ~ 9.0 95.9 95.2 102.1 93.6 :~ 8.6 89.1 91.7 ~ 13.4 84.5 ~ 8.2 82.6 85.5 ± 5.2 82.5 ~ 13.4 75.4 ~ 12.4 85.2 82.9 78.8 £ 16.7 60.0 ~ 19.0
15 1 I 16 1 1 1 7 I 5 6 1 3 3 4 1 1 8 16
4 0 0 8 1 1 0 3 1 4 6 1 3 3 4 1 1 8 16
15 17 19 20 21 25 25 30 33 37.5 50 60 62.5 70 75 75 81 85 100
0 0 0 0 0 0
* Number of runs with significant response decrement from Kendall rank correlation test.
565 its 3 principal subdivisions mentioned earlier. In other words, it is not possible to distinguish the 3 C N subdivisions based on the response decrement data. It appears that response decrements in the cochlear nucleus under repetitive tonal stimulation is a function of the stimulus paradigm and may occur in the absence of decrement in the acoustic nerve. Since the present experiments were carried out on decerebrate preparations, projections from cortex or thalamus could not have influenced the cochlear nucleus response. In the cochlear nucleus which was surgically isolated from the brain stem, similar response decrements developedL Thus, the process causing response decrement may not require influences more central to the cochlear nucleus. The lack of difference in the 3 subdivisions of cochlear nucleus is surprising since different divisions contain cells which differ appreciably in morphology and electrophysiology6,is. Previous work showed that the response decrement of acoustic nerve and cochlear nucleus units due to repetitive acoustic stimulation was a function of the sound intensityT,15,19. We did not study the effect of sound intensity since the inherent averaging nature of the multiple unit recording may not be suitable for the work. Unlike the earlier results, no significant decrement was observed in the acoustic nerve responses, although decrement was observed in the spontaneous discharge rates (Fig. 1), in agreement with the others10,19. While decrements in the cochlear nucleus response may not always have importance to acoustic habituation in the intact, behaving individual, the possibility of a significant contribution exists whenever acoustic stimulation produces decrements in the cochlear nucleus. Such a conceptualization of acoustic habituation presents the behavioral phenomenon against a neural background of temporal hierarchies. As the temporal configurations of the habituating stimulus change, so do the participating neural elements. By experimentally determining the response plasticity for the different neural elements, predictions can be made as to the behavior of specific neuronal pools to habituating stimuli with particular temporal configurations. This was supported in part by N I H Grant HD-04612 and in part by a grant award from the College of Medicine, University of South Alabama.
1 Britt, R. and Starr, A., Synaptic events and discharge patterns of cochlear nucleus cells. I. Steadyfrequency tone bursts, J. Neurophysiol. 39 (1976) 162-178. 2 Brown, K. A. and Buchwald, J. S., Response decrements during repetitive tone stimulation in the surgically isolated cochlear nucleus, Exp. Neurol., 53 (1976) 663-669. 3 Buchwald, J. S. and Humphrey, G. L., Response plasticity in the cochlear nucleus of decerebrate cats during acoustic habituation, J. Neurophysiol., 35 (1972) 864-878. 4 Buchwald, J. S., Holstein, S. B. and Weber, D. S., Technique, interpretation and experimental applications. In R. F. Thompson and M. M. Patterson (Eds.), Bioelectric Recording Techniques. Cellular Processes and Brain Potentials, Academic Press, New York, 1973, pp. 202-242. 5 Buchwald, J. S. and Humphrey, G. L., An analysis of habituation in the specific sensory systems. In E. Stellar and J. Sprague (Eds.), Progress in Physiological Psychology, Vol. 5., Academic Press, New York, 1973, pp. 1-75. 6 Evans, E. F. and Nelson, P. G., The responses of single neurons in the cochlear nucleus of the cat as a function of their location and the anesthetic state, Exp. Brain Res., 17 (1973) 426-427. 7 Goldberg, J. M. and Greenwood, D. D., Response of neurons of the dorsal and posteroventral
566
8 9 10 11 12
13 14 15 16 17 18 19
cochlear nuclei of the cat to acoustic stimulation of long duration, J. Neurophysiol., 29 (1966) 72-93. Goldberg, J. M., Adrian, H. O. and Smith, F. D., Response of neurons of the superior olvary complex of the cat to acoustic stimuli of long duration, J. NeurophysioL, 27 (1964) 706-749. Humphrey, G., The Nature of Learning, Harcourt, New York, 1963. Kiang, N., Discharge patterns of single fibers in the cat's auditory nerve. In Research Monograph No. 35, MIT Press, Cambridge, Mass., 1965, pp. 68-83. Peake, W. T., Goldstein, M. H. and Kiang, N. Y., Responses of the auditory nerve to repetitive acoustic stimuli, J. Acoust. Soc. Amer., 34 (1962) 562-570. Rose, J. E., Brugge, J. F., Anderson, D. J. and Hind, J. G., Phase locked response to low-frequency tones in single auditory nerve fibers of the squirrel monkey, J. Neurophysiol., 30 (1967) 769-793. Rupert, A., Moushegian, G. and Galambos, R., Unit responses to sound from auditory nerve of the cat, J. NeurophysioL, 26 (1963) 449-465. Simmons, F. B. and Linehan, J. A., Observations on a single auditory nerve fiber over a six-week period, J. NeurophysioL, 31 (1968) 799-805. Smith, R. L., Short-term adaptation in single auditory nerve fibers: some post-stimulatory effects, J. Neurophysiol., 40 (1977) 1098-1112. Walsh, B. T., Miller, J. B., Gacek, R. R. and Kiang, N. Y. S., Spontaneous activity in the eighth cranial nerve of the cat, Int. J. Neurosci., 3 (1972) 221-236. Wickelgren, W. O., Effect of acoustic habituation on click evoked responses in cats, J. Neurophysiol., 31 (1968) 777-782. Young, E. D. and Brownell, W. E., Responses to tones and noise of single ceils in dorsal cochlear nucleus of unanesthetized cats, J. Neurophysiol., 39 (1976) 282-300. Young, E. and Sachs, M. B., Recovery from sound exposure in auditory nerve fibers, J. Acoust. Soc..4mer., 48 (1970) 966-977.
Brain Research, 173 (1979) 562-566 © Elsevier/North-Holland Biomedical Press
A comparison of acoustic nerve and cochlear nucleus responses during acoustic habituation
CHI-MING HUANG and J. S. BUCHWALD Department of Physiology, University of South Alabama, Mobile, Ala. 36688 and Department of Physiology, Mental Retardation Center and Brain Research Institute, UCLA Medical Center, Los Angeles, Calif. 90024 (U.S.A.)
(Accepted May 24th, 1979)
Even though habituation has been viewed as learning in its simplest form 9, the behavioral responses are many and complex and their neurophysiological mechanisms vary not only with the form of the behavior but also with the temporal parameters of the repetitive stimulus. Although many electrophysiological analyses of acoustic habituation have been carried out, general statements are not possible 5. The results obtained with unit vs evoked potential recordings further complicated the interpretation. For example, unit response decrements occur as peripherally as the cochlear nucleus 3, while evoked potential changes do not occur below the thalamic level 17; such data have made conceptualization of the neural substrates relevant to habituation difficult. Other studies on the responses of the acoustic nerve fibers 1°,11,15,19 and neurons in the cochlear nucleus v and superior olive 8 either employed tonal repetition rates exceeding 10/sec, not those typically used in acoustic habituation, or were done under the effect of anesthesia 12-14,18. The use of widely different combinations of stimulus duration and inter-tone interval has further complicated the resolution of these data into a coherent whole. In this report we present multiple unit data on the response decrement of the acoustic nerve (AN) and cochlear nucleus (CN) in unanesthetized cats over temporal parameters for the repetitive acoustic stimulus typically used in acoustic habituation studies. Recordings were carried out on 11 cats. The surgical and recording procedures have been detailed elsewhere 3. Briefly, the cats were initially anesthetized with a mixture of N20, 02 and methoxyflurane. Anesthesia was terminated after a mid-collicular decerebration. The preparation was then paralyzed with Flaxedil 3,4. Recordings of multiple unit activity were made with concentric or bipolar electrodes (15-30 K f~ at 1000 Hz)3,L A silver ball electrode was implanted on the round window to monitor the stability of the cochlear microphonic potentiaP. The entire amplification and recording system had a frequency response range from 30-5000 Hz. Acoustic stimuli were pure tones between 500-5000 Hz. Sound intensities of 70 or 80 dB spl (re 0.0002 dyne/sq. cm) at the central end of the earbar were used. Data analysis of the multiple unit activity was done by a special-purpose integrator circuit described previously 4. The
563
Acoustic Nerve 123
rain
5 I
, ~ ' ~ J ~ '~"~
rain
'
Cochleor Nucleus
i
,
50 sec
'!r,
w
i
control
1.5 sec tones
recovery
3 rain lone recovery
Fig. 1. Typical pattern of multiple unit responses to repetitive tones (1.5 sec tone every 5 sec) and continuous tones (3 min) in the acoustic nerve and the cochlear nucleus. The data were taken from 4 different preparations which showed variations in the signal-to-noise ratio. The acoustic nerve data showed no response decrement during repetitive stimulation, but the spontaneous activity dropped below control level at the end of the continuous tone. In the cochlear nucleus, response decrement could also be seen during repetitive tone stimulation.
removal of the microphonics from the acoustic nerve activities was accomplished through a sharp notch filter (24 dB/octave). The cochlear nucleus responses were free from microphonic contamination and were analyzed without filtering. In a few cases where the filter was used, the results were unchanged. Each experiment involved only one C N and one A N recording site. At the end of the experiment, the recording sites were marked with current and the brain perfused with 10 % formalin. Verification of electrode placement confirmed all 11 A N recording sites. Three C N recording sites were found in anteroventral CN, two in posteroventral CN, and 4 in dorsal CN, two more recording sites were in the border area between anteroventral and posteroventral CN. A typical protocol contained 3 steps. First, five 1.5 sec control test tones were given once every 10 sec. Following a silent period of 30 sec, the second step consisted of 25 tones with a predetermined combination of tone duration and inter-tone interval. In the CN, responses to individual tones generally decreased and reached a steadystate level (Fig. 1). In the AN, the response decrement was less obvious, but the spontaneous activity level was often seen decreased, particularly following prolonged sound stimulation. In the third step, test tones of 1.5 sec duration were given once every 10 sec to monitor the recovery which was exponential or near exponential. Longer periods were necessary for recovery from larger amounts of response decrements. In general, response recovery was complete within 1 min. Each series of 25 responses were fitted to a 5-parameter polynomial and a 95 % confidence band was established. F r o m 187 tone sequences in 11 preparations, the mean width of the confidence band from the center to either the upper or lower 95 %
564 confidence limit was 9.7 ~ 4.5 ~ of the control response. To quantify the m a g n i t u d e o f response modification, the average of the responses to the first 5 c o n t r o l test tones delivered before the tone sequence was defined as the control response. The average o f the response to the last 5 of the 25 tones was defined as the final response. The q u a n t i t y (final/control) was calculated. To determine the statistical significance o f the decrements, K a n d e l l r a n k correlations were carried out for each tone sequence between the n u m b e r of trials (e.g. 1st, 2nd, 3rd . . . . 10th, etc.) a n d the magnitude of response. In Table I, the (final/control) values in the CN a n d the A N , the n u m b e r of tone series carried out, a n d the n u m b e r of tone series with significant response decrements from the K e n d a l l correlation are tabulated with the stimulus parameters. These data were listed in the order of increasing stimulus duty cycle values defined as [(tone d u r a t i o n ) / (tone d u r a t i o n + inter-tone interval)]. A n e x a m i n a t i o n of Table I shows that :(1) in the CN, the p r o p o r t i o n s of runs with significant response decrements increased with stimulus duty cycle whereas no such trend was evident in the A N ; a n d (2) the (final/ control) values decreased with increasing stimulus duty cycle values in the CN, but not in the A N . We next c o m p a r e d the response decrement in different parts of the CN. F o r a given stimulus paradigm, no significant difference could be f o u n d between data from
TABLE I Response decrement in the acoustic nerve and the cochlear nucleus during repetitive tonal stimulation Acoustic nerve
Cochlear nucleus
Tone duration (see)
Intertone- Duty interval cycle (see) (%)
Final/Initial (%)
No. runs
ns*
Final~Initial (%)
No. runs
ns*
1.5 1.5 1.5 1.0 1.5 1.5 0.5 1.5 0.5 1.5 1.5 1.5 2.5 3.5 1.5 4.5 6.5 8.5 25.0
8.5 7.5 6.5 4.0 5.5 4.5 1.5 3.5 1.0 2.5 1.5 1.0 1.5 1.5 0.5 1.5 1.5 1.5 0
104.8 ± 11.6 100.0 100.0 108.0 ± 7.6 100.0 100.0 100.0 100.1 ± 7.0 100.0 96.7 ± 5.6 99.3 i 3.6 100.0 100.0 104.7 ± 8.2 101.2 d- 15.3 100.0 100.0 98.0 ± 6.5 103.7 ± 8.1
28 1 1 3 1 I 1 7 1 6 7 1 1 3 8 1 1 12 11
2 0 0 0 0 0 0 1 0 0 0 0
94.4 k 8.1 98.5 100.1 90.5 ~ 9.0 95.9 95.2 102.1 93.6 :~ 8.6 89.1 91.7 ~ 13.4 84.5 ~ 8.2 82.6 85.5 ± 5.2 82.5 ~ 13.4 75.4 ~ 12.4 85.2 82.9 78.8 £ 16.7 60.0 ~ 19.0
15 1 I 16 1 1 1 7 I 5 6 1 3 3 4 1 1 8 16
4 0 0 8 1 1 0 3 1 4 6 1 3 3 4 1 1 8 16
15 17 19 20 21 25 25 30 33 37.5 50 60 62.5 70 75 75 81 85 100
0 0 0 0 0 0
* Number of runs with significant response decrement from Kendall rank correlation test.
565 its 3 principal subdivisions mentioned earlier. In other words, it is not possible to distinguish the 3 C N subdivisions based on the response decrement data. It appears that response decrements in the cochlear nucleus under repetitive tonal stimulation is a function of the stimulus paradigm and may occur in the absence of decrement in the acoustic nerve. Since the present experiments were carried out on decerebrate preparations, projections from cortex or thalamus could not have influenced the cochlear nucleus response. In the cochlear nucleus which was surgically isolated from the brain stem, similar response decrements developedL Thus, the process causing response decrement may not require influences more central to the cochlear nucleus. The lack of difference in the 3 subdivisions of cochlear nucleus is surprising since different divisions contain cells which differ appreciably in morphology and electrophysiology6,is. Previous work showed that the response decrement of acoustic nerve and cochlear nucleus units due to repetitive acoustic stimulation was a function of the sound intensityT,15,19. We did not study the effect of sound intensity since the inherent averaging nature of the multiple unit recording may not be suitable for the work. Unlike the earlier results, no significant decrement was observed in the acoustic nerve responses, although decrement was observed in the spontaneous discharge rates (Fig. 1), in agreement with the others10,19. While decrements in the cochlear nucleus response may not always have importance to acoustic habituation in the intact, behaving individual, the possibility of a significant contribution exists whenever acoustic stimulation produces decrements in the cochlear nucleus. Such a conceptualization of acoustic habituation presents the behavioral phenomenon against a neural background of temporal hierarchies. As the temporal configurations of the habituating stimulus change, so do the participating neural elements. By experimentally determining the response plasticity for the different neural elements, predictions can be made as to the behavior of specific neuronal pools to habituating stimuli with particular temporal configurations. This was supported in part by N I H Grant HD-04612 and in part by a grant award from the College of Medicine, University of South Alabama.
1 Britt, R. and Starr, A., Synaptic events and discharge patterns of cochlear nucleus cells. I. Steadyfrequency tone bursts, J. Neurophysiol. 39 (1976) 162-178. 2 Brown, K. A. and Buchwald, J. S., Response decrements during repetitive tone stimulation in the surgically isolated cochlear nucleus, Exp. Neurol., 53 (1976) 663-669. 3 Buchwald, J. S. and Humphrey, G. L., Response plasticity in the cochlear nucleus of decerebrate cats during acoustic habituation, J. Neurophysiol., 35 (1972) 864-878. 4 Buchwald, J. S., Holstein, S. B. and Weber, D. S., Technique, interpretation and experimental applications. In R. F. Thompson and M. M. Patterson (Eds.), Bioelectric Recording Techniques. Cellular Processes and Brain Potentials, Academic Press, New York, 1973, pp. 202-242. 5 Buchwald, J. S. and Humphrey, G. L., An analysis of habituation in the specific sensory systems. In E. Stellar and J. Sprague (Eds.), Progress in Physiological Psychology, Vol. 5., Academic Press, New York, 1973, pp. 1-75. 6 Evans, E. F. and Nelson, P. G., The responses of single neurons in the cochlear nucleus of the cat as a function of their location and the anesthetic state, Exp. Brain Res., 17 (1973) 426-427. 7 Goldberg, J. M. and Greenwood, D. D., Response of neurons of the dorsal and posteroventral
566
8 9 10 11 12
13 14 15 16 17 18 19
cochlear nuclei of the cat to acoustic stimulation of long duration, J. Neurophysiol., 29 (1966) 72-93. Goldberg, J. M., Adrian, H. O. and Smith, F. D., Response of neurons of the superior olvary complex of the cat to acoustic stimuli of long duration, J. NeurophysioL, 27 (1964) 706-749. Humphrey, G., The Nature of Learning, Harcourt, New York, 1963. Kiang, N., Discharge patterns of single fibers in the cat's auditory nerve. In Research Monograph No. 35, MIT Press, Cambridge, Mass., 1965, pp. 68-83. Peake, W. T., Goldstein, M. H. and Kiang, N. Y., Responses of the auditory nerve to repetitive acoustic stimuli, J. Acoust. Soc. Amer., 34 (1962) 562-570. Rose, J. E., Brugge, J. F., Anderson, D. J. and Hind, J. G., Phase locked response to low-frequency tones in single auditory nerve fibers of the squirrel monkey, J. Neurophysiol., 30 (1967) 769-793. Rupert, A., Moushegian, G. and Galambos, R., Unit responses to sound from auditory nerve of the cat, J. NeurophysioL, 26 (1963) 449-465. Simmons, F. B. and Linehan, J. A., Observations on a single auditory nerve fiber over a six-week period, J. NeurophysioL, 31 (1968) 799-805. Smith, R. L., Short-term adaptation in single auditory nerve fibers: some post-stimulatory effects, J. Neurophysiol., 40 (1977) 1098-1112. Walsh, B. T., Miller, J. B., Gacek, R. R. and Kiang, N. Y. S., Spontaneous activity in the eighth cranial nerve of the cat, Int. J. Neurosci., 3 (1972) 221-236. Wickelgren, W. O., Effect of acoustic habituation on click evoked responses in cats, J. Neurophysiol., 31 (1968) 777-782. Young, E. D. and Brownell, W. E., Responses to tones and noise of single ceils in dorsal cochlear nucleus of unanesthetized cats, J. Neurophysiol., 39 (1976) 282-300. Young, E. and Sachs, M. B., Recovery from sound exposure in auditory nerve fibers, J. Acoust. Soc..4mer., 48 (1970) 966-977.