- Email: [email protected]
Role of neocortex in binaural hearing in the cat. III. Binaural masking-level differences
Brain Research, 151 (1978) 381-385 O Elsevier/North-Holland Biomedical Press
381
Role of neocortex in binaural hearing in the cat. III. Binaural masking-level differences
JERRY L. CRANFORD, JAMES STRAMLER and MAKOTO IGARASHI Institute of Otorhinolaryngology and Communicative Disorders, The Neurosensory Center qf Houston, Houston, Texas 77030 (U.S.A.)
(Accepted February 23rd, 1978)
In man, monaural hearing loss produces two major impairments. In addition to a pronounced difficulty in locating the source of unexpected brief sounds, such individuals also discover that they have lost their normal ability, in a room crowded with people talking, of being able to easily suppress the background noise and focus attention on individual speakers. Sometimes referred to as the 'cocktail party' problem, this latter function of the normal human brain has been, in recent years, the subject of an extensive amount of psychophysical research with normal human listeners 4. The laboratory version of this binaural phenomenon, which is commonly labeled the 'binaural masking-level difference' (BMLD), refers to the observation that the detectability of an auditory signal presented in noise may be improved by appropriate changes in the interaural relations between either the signal or the noise. Two recent experiments, one involving differences in interaural intensity relations 1, and the other differences in tonal phase-angle relations 5, have demonstrated the occurrence of BMLD's in normal cats. Cranford's experiment 1 involved measuring the effects of noise at one ear on the detection thresholds for tones embedded in noise at the opposite ear. He found that normal cats exhibit significantly lower detection thresholds for monaural tones when noise is present in the non-signal as well as the signal ear. Wakeford and Robinson 5 measured the relative detectability of in-phase (diotic) vs. 180° out-of-phase (dichotic) binaural tones in the presence of continuous diotic noise. These investigators observed improved detectability of tones when they were out- of-phase relative to the noise. The purpose of the present experiment was to examine the effects of unilateral and bilateral ablation of auditory neocortex on these two 'intensity' and 'temporal' forms of BMLD tests. Nine adult cats were tested in the present experiments. The auditory stimuli were presented directly to the cats' ears by means of small hearing aid phones mounted in flexible leather helmets (Fig. 1). The earphones were Danavox model 3600-56 transducers. An analysis of the output characteristics revealed a fairly fiat response curve between 0.5 kHz and 5 kHz. Above and below these limits the output levels dropped significantly. Between 0.5 kHz and 2 kHz the maximum deviation from that observed at the test frequency of I kHz was less than 5 dB. Matched pairs of these phones
382
B
D
A
A. Audio transducer ~'~-&~ B. Electrical leads from audio transducer H to coupler mounted on back of helmet C. Coupler which connects leads from transducer to telephone cord D. Flexible telephone cord attached to coupler E. Removable cap for sealing top of cone F. Soft leather harness which holds cones in place G. Soft rubber molding fits directly against side of head H. Funnel-shaped cones which fit over pinnae
G
Fig. 1. The design of the stereo headset used to test cats in the present BMLD experiments.
were selected for use in the present study. The tonal stimuli consisted of trains of 1 kHz tone pulses delivered at a rate of 1/sec. Each pulse had a duration of 0.5 sec. with linear rise and fall times of 100 msec. The gaussian masking noise (which was ungated and presented continuously throughout each test session) was band limited only by the characteristics of the audio transducers. As measured through a 6 cc coupler, the spectrum level of the 1 kHz component of the noise was found to be 47 dB SPL re 0.0002 dyne/sq.cm. The experimental audiometer used in the present study was similar to that previously described 1,2. The cats were first trained to avoid shock by crossing to the opposite compartment of a double-grill box when positive trials consisting of 10 sec. long trains of I kHz tone pulses were presented from a free-field loudspeaker. Following this initial avoidance training, the cats were adapted to wearing helmets and trained to respond when the avoidance signals were delivered with earphones rather than from the loudspeaker. After the animals had learned to respond consistently to the warning signals at either ear, the monaural thresholds for the detection of the tones in the absence of noise was determined by a modified method of limits1, ~. After determining monaural sensitivity levels, the cats were tested with four basic experiment conditions. These were (a) condition SmNm in which signal and noise are presented to one ear with no input to the opposite ear; (b) condition SmNo in which signals are presented to one ear only and equal intensity in-phase noise is presented to both ears; (c) condition SoNo in which signal and noise are both presented binaurally and in-phase; and (d) condition S~No in which the signal is presented binaurally but 180 ° out-of-phase at the two ears while the noise is in-phase. The tests in (a) and (b) were counterbalanced with respect to which ear received the signals thus effectively making
383 TABLE I The mean amount of 'release from masking' observed with each of 9 cats on the 'temporal' and 'intensity' forms of BMLD test. See the text for details. Since the reconstructed cortical lesions and resulting patterns of thalamic degeneration observed with the present cats was virtually identical to that reported for the cats of the first two binaural experiments of the present series2,z, a detailed description of the histological findings was considered unnecessary for the present report. In all 9 cats the minimum extent of the cortical lesions included auditory sub-divisions AI, AII, Ep, SII, and I-T. The slight individual variability observed in lesion placement was not correlated in any systematic fashion with differences in behavioral results. SnNo vs. SoNo Pre-Op
Two-stage Operation Cat 4075 7.8 dB Cat 3608 5.2 dB Cat 4264 6.3 dB Cat 4074 7.2 dB Cat 3620 7.8 dB Cat 3501 6.0 dB Cat 4984 4.4 dB One-stage operation Cat 7261 7.2 dB Cat 7263 8.4 dB Means 6.7 dB
SmNo vs. SmN,,~
Unilateral
Bilateral
Pre-Op
Unilateral
Bilateral
7.6 dB 8.8 dB 5.3 dB 6.2 dB 9.0 dB 7.8 dB 5.1 dB
4.5 dB 4.8 dB 5.0 dB 4.3 dB 8.5 dB 6.7 dB 2.8 dB
4.8 dB 6.7 dB 2.9 dB 5.7 dB 5.9 dB 3.3 dB *
4.7 dB 7.9 dB 2.9 dB 4.0 dB 7.9 dB 5.1 dB *
0 4.0 0 4.5 * 2.1 0
* * 7.1 dB
2.0 dB 2.9 dB 4.6 dB
* * 4.9 dB
* * 5.4 dB
* * 1.8 dB
dB dB dB dB dB dB
* Cats not tested. a total of 6 separate test conditions. Tests were administered with each of the 6 conditions in a r a n d o m i z e d b u t balanced fashion (i.e., within a given 6 day block, each c o n d i t i o n was tested only once b u t the order of p r e s e n t a t i o n of the tests was r a n d o m i z e d between consecutive blocks). I n each phase of the experiment, testing was c o n t i n u e d until a m i n i m u m of l0 separate thresholds had been d e t e r m i n e d with each of the different test c o n d i t i o n s or until threshold levels had stabilized. The m a j o r findings of the present investigation are s u m m a r i z e d in Table I. Prior to the first o p e r a t i o n the m e a n B M L D observed with the S~Novs. SoNo phase test was significantly higher (Sandler's A-statistic P < 0.01) t h a n that observed with the SmNo vs. SmNm intensity test. After unilateral operations (areas AI, AII, Ep, SII, I-T) there was a small non-significant (P > 0.05) increase in the m e a n B M L D s observed with b o t h tests. I n the two previous b i n a u r a l hearing experiments of the present series2, 3, cats with unilateral lesions of the a u d i t o r y cortex exhibited selective deficits in discrimi n a t i n g sounds at ears contralateral to the d a m a g e d hemisphere whenever c o m p e t i n g sounds were present at b o t h ears. I n order to determine whether a similar ' d i r e c t i o n a l ' lesion effect m i g h t have occurred in the present SmNo vs. SmNm intensity test, we compared the relative m a g n i t u d e s of the B M L D s observed when the m o n a u r a l tones were delivered to ears located either ipsilateral or contralateral to the side o f the d a m a g e d hemisphere. A l t h o u g h , for the six cats, the m e a n a m o u n t of release from m a s k i n g was greater when m o n a u r a l tones were presented to ears located opposite the d a m a g e d hemisphere, this difference was n o t statistically significant (P > 0.05). The only cat
384 which exhibited an interaural BMLD difference greater than 2dB was 3620. Although this cat, like the other five cats, exhibited no significant interaural differences in the absolute thresholds for the 1 kHz tones in the absence of noise, it did exhibit an interaural difference in the magnitude of the signal-to-noise ratio when tested with condition SmNm. Noise mixed with tones at the ear contralateral to the operated hemisphere produced an average of 8 dB more masking than when tones and noise were presented together at the ipsilateral ear. Histological examination of the cortical lesion of cat 3620 revealed no obvious basis for this asymmetrical hearing effect. None of the other cats exhibited any significant interaural differences in the signal-to-noise ratios. The findings obtained following bilateral lesions are also summarized in Table I. Compared with the preoperative levels, the mean magnitude of the BM LDs observed with both tests were significantly reduced (P < 0.001) in magnitude following the second operation. The BMLDs found with the phase test were reduced by 31 whereas the BMLDs in the intensity test were reduced by 63 %. Although all cats exhibited BMLDs with the phase test, three of the six cats which were tested with the intensity test following bilateral lesions exhibited no evidence o f a BMLD. Histological examination of cortical lesions and thalamic degeneration revealed no obvious anatomical basis for the unique findings with these three cats. All six cats had similar lesions which included complete ablation of auditory subdivisions AI, All, Ep, SII, and I-T. The extent of under-cutting of non-auditory cortical regions also did not differentiate the two groups. Prior to beginning the present experiment, and again after its completion, we measured the analogous human BMLDs using the same stimulus presentation procedures, experimental audiometer, and earphones (mounted in a human stereo headset) as used for the cats. With three normal hearing subjects the mean human BMLD with the phase test was found to be 7.5 dB whereas with the intensity test the mean BMLD was 5.2 dB. These findings confirm the present and previous results with cats2, 5 and humans 4 which indicated that significantly larger BMLDs occur in experimental situations involving interaural differences in the phase relationships of signals and noise as compared to differences in intensity relations. The present experimental findings suggest that BMLDs, instead of being exclusively a cortically dependent binaural hearing phenomenon, are mediated at least in part by a subcortical analyzing system possibly localized in the superior olivary complex. This hypothesis is further reinforced by the additional finding obtained in the present experiment indicating that the BMLD is an unlearned phenomenon. Before the first cortical operation, no learning was necessary for the occurrence of BMLDs other than that related to learning to wear helmets and responding to low intensity sounds. At the first opportunity for the occurrence o f a BMLD, i.e., upon first receiving tests with S~No or SmNo following a series of prior threshold tests with the respective homophasic conditions, the cats exhibited BMLDs. Similar findings were obtained following unilateral and bilateral cortical operations. When we first completed the present experiment, we interpreted the finding of decreased BMLDs following bilateral cortical operations to be a secondary result of the increased emotionality (as reflected in increased spontaneous activity and less consistent day-to-day performance) which
385 is observed, at least to some degree, in most cats following bilateral lesions. However, the findings from an experiment completed subsequent to the B M L D study suggests that the reduction in the size of the BMLDs may actually reflect the disturbance of a normal cortical role. In brief, two of the present cats (3608, 7263), which had reduced BMLDs, have subsequently been found to have normal thresholds for detecting interaural reversals in the intensity and phase relationships of binaural 1 K H z tones. This research was supported by N I N C D S grants NS 11812 and NS 10940.
1 Cranford, J. L., Auditory masking level differences in the cat, J. comp. physioL PsychoL, 89 (1975) 219-223. 2 Cranford, J. L., Role of neocortex in binaural hearing in the cat. I. Contralateral masking, Brain Research, 100 (1975) 395-406. 3 Cranford, J. L. and Oberholtzer, M., Role of neocortex in binaural hearing in the cat. II. The 'precedence effect' in sound localization, Brain Research, 111 (1976) 225-239. 4 Green, D. M. and Henning, G. B., Audition, Ann. Rev. Psychol., 20 (1969) 105-128. 5 Wakeford, O. S. and Robinson, D. E., Detection of binaurally masked tones by the cat, J. acoust. Soc. Amer., 56 (1974) 952-956.
381
Role of neocortex in binaural hearing in the cat. III. Binaural masking-level differences
JERRY L. CRANFORD, JAMES STRAMLER and MAKOTO IGARASHI Institute of Otorhinolaryngology and Communicative Disorders, The Neurosensory Center qf Houston, Houston, Texas 77030 (U.S.A.)
(Accepted February 23rd, 1978)
In man, monaural hearing loss produces two major impairments. In addition to a pronounced difficulty in locating the source of unexpected brief sounds, such individuals also discover that they have lost their normal ability, in a room crowded with people talking, of being able to easily suppress the background noise and focus attention on individual speakers. Sometimes referred to as the 'cocktail party' problem, this latter function of the normal human brain has been, in recent years, the subject of an extensive amount of psychophysical research with normal human listeners 4. The laboratory version of this binaural phenomenon, which is commonly labeled the 'binaural masking-level difference' (BMLD), refers to the observation that the detectability of an auditory signal presented in noise may be improved by appropriate changes in the interaural relations between either the signal or the noise. Two recent experiments, one involving differences in interaural intensity relations 1, and the other differences in tonal phase-angle relations 5, have demonstrated the occurrence of BMLD's in normal cats. Cranford's experiment 1 involved measuring the effects of noise at one ear on the detection thresholds for tones embedded in noise at the opposite ear. He found that normal cats exhibit significantly lower detection thresholds for monaural tones when noise is present in the non-signal as well as the signal ear. Wakeford and Robinson 5 measured the relative detectability of in-phase (diotic) vs. 180° out-of-phase (dichotic) binaural tones in the presence of continuous diotic noise. These investigators observed improved detectability of tones when they were out- of-phase relative to the noise. The purpose of the present experiment was to examine the effects of unilateral and bilateral ablation of auditory neocortex on these two 'intensity' and 'temporal' forms of BMLD tests. Nine adult cats were tested in the present experiments. The auditory stimuli were presented directly to the cats' ears by means of small hearing aid phones mounted in flexible leather helmets (Fig. 1). The earphones were Danavox model 3600-56 transducers. An analysis of the output characteristics revealed a fairly fiat response curve between 0.5 kHz and 5 kHz. Above and below these limits the output levels dropped significantly. Between 0.5 kHz and 2 kHz the maximum deviation from that observed at the test frequency of I kHz was less than 5 dB. Matched pairs of these phones
382
B
D
A
A. Audio transducer ~'~-&~ B. Electrical leads from audio transducer H to coupler mounted on back of helmet C. Coupler which connects leads from transducer to telephone cord D. Flexible telephone cord attached to coupler E. Removable cap for sealing top of cone F. Soft leather harness which holds cones in place G. Soft rubber molding fits directly against side of head H. Funnel-shaped cones which fit over pinnae
G
Fig. 1. The design of the stereo headset used to test cats in the present BMLD experiments.
were selected for use in the present study. The tonal stimuli consisted of trains of 1 kHz tone pulses delivered at a rate of 1/sec. Each pulse had a duration of 0.5 sec. with linear rise and fall times of 100 msec. The gaussian masking noise (which was ungated and presented continuously throughout each test session) was band limited only by the characteristics of the audio transducers. As measured through a 6 cc coupler, the spectrum level of the 1 kHz component of the noise was found to be 47 dB SPL re 0.0002 dyne/sq.cm. The experimental audiometer used in the present study was similar to that previously described 1,2. The cats were first trained to avoid shock by crossing to the opposite compartment of a double-grill box when positive trials consisting of 10 sec. long trains of I kHz tone pulses were presented from a free-field loudspeaker. Following this initial avoidance training, the cats were adapted to wearing helmets and trained to respond when the avoidance signals were delivered with earphones rather than from the loudspeaker. After the animals had learned to respond consistently to the warning signals at either ear, the monaural thresholds for the detection of the tones in the absence of noise was determined by a modified method of limits1, ~. After determining monaural sensitivity levels, the cats were tested with four basic experiment conditions. These were (a) condition SmNm in which signal and noise are presented to one ear with no input to the opposite ear; (b) condition SmNo in which signals are presented to one ear only and equal intensity in-phase noise is presented to both ears; (c) condition SoNo in which signal and noise are both presented binaurally and in-phase; and (d) condition S~No in which the signal is presented binaurally but 180 ° out-of-phase at the two ears while the noise is in-phase. The tests in (a) and (b) were counterbalanced with respect to which ear received the signals thus effectively making
383 TABLE I The mean amount of 'release from masking' observed with each of 9 cats on the 'temporal' and 'intensity' forms of BMLD test. See the text for details. Since the reconstructed cortical lesions and resulting patterns of thalamic degeneration observed with the present cats was virtually identical to that reported for the cats of the first two binaural experiments of the present series2,z, a detailed description of the histological findings was considered unnecessary for the present report. In all 9 cats the minimum extent of the cortical lesions included auditory sub-divisions AI, AII, Ep, SII, and I-T. The slight individual variability observed in lesion placement was not correlated in any systematic fashion with differences in behavioral results. SnNo vs. SoNo Pre-Op
Two-stage Operation Cat 4075 7.8 dB Cat 3608 5.2 dB Cat 4264 6.3 dB Cat 4074 7.2 dB Cat 3620 7.8 dB Cat 3501 6.0 dB Cat 4984 4.4 dB One-stage operation Cat 7261 7.2 dB Cat 7263 8.4 dB Means 6.7 dB
SmNo vs. SmN,,~
Unilateral
Bilateral
Pre-Op
Unilateral
Bilateral
7.6 dB 8.8 dB 5.3 dB 6.2 dB 9.0 dB 7.8 dB 5.1 dB
4.5 dB 4.8 dB 5.0 dB 4.3 dB 8.5 dB 6.7 dB 2.8 dB
4.8 dB 6.7 dB 2.9 dB 5.7 dB 5.9 dB 3.3 dB *
4.7 dB 7.9 dB 2.9 dB 4.0 dB 7.9 dB 5.1 dB *
0 4.0 0 4.5 * 2.1 0
* * 7.1 dB
2.0 dB 2.9 dB 4.6 dB
* * 4.9 dB
* * 5.4 dB
* * 1.8 dB
dB dB dB dB dB dB
* Cats not tested. a total of 6 separate test conditions. Tests were administered with each of the 6 conditions in a r a n d o m i z e d b u t balanced fashion (i.e., within a given 6 day block, each c o n d i t i o n was tested only once b u t the order of p r e s e n t a t i o n of the tests was r a n d o m i z e d between consecutive blocks). I n each phase of the experiment, testing was c o n t i n u e d until a m i n i m u m of l0 separate thresholds had been d e t e r m i n e d with each of the different test c o n d i t i o n s or until threshold levels had stabilized. The m a j o r findings of the present investigation are s u m m a r i z e d in Table I. Prior to the first o p e r a t i o n the m e a n B M L D observed with the S~Novs. SoNo phase test was significantly higher (Sandler's A-statistic P < 0.01) t h a n that observed with the SmNo vs. SmNm intensity test. After unilateral operations (areas AI, AII, Ep, SII, I-T) there was a small non-significant (P > 0.05) increase in the m e a n B M L D s observed with b o t h tests. I n the two previous b i n a u r a l hearing experiments of the present series2, 3, cats with unilateral lesions of the a u d i t o r y cortex exhibited selective deficits in discrimi n a t i n g sounds at ears contralateral to the d a m a g e d hemisphere whenever c o m p e t i n g sounds were present at b o t h ears. I n order to determine whether a similar ' d i r e c t i o n a l ' lesion effect m i g h t have occurred in the present SmNo vs. SmNm intensity test, we compared the relative m a g n i t u d e s of the B M L D s observed when the m o n a u r a l tones were delivered to ears located either ipsilateral or contralateral to the side o f the d a m a g e d hemisphere. A l t h o u g h , for the six cats, the m e a n a m o u n t of release from m a s k i n g was greater when m o n a u r a l tones were presented to ears located opposite the d a m a g e d hemisphere, this difference was n o t statistically significant (P > 0.05). The only cat
384 which exhibited an interaural BMLD difference greater than 2dB was 3620. Although this cat, like the other five cats, exhibited no significant interaural differences in the absolute thresholds for the 1 kHz tones in the absence of noise, it did exhibit an interaural difference in the magnitude of the signal-to-noise ratio when tested with condition SmNm. Noise mixed with tones at the ear contralateral to the operated hemisphere produced an average of 8 dB more masking than when tones and noise were presented together at the ipsilateral ear. Histological examination of the cortical lesion of cat 3620 revealed no obvious basis for this asymmetrical hearing effect. None of the other cats exhibited any significant interaural differences in the signal-to-noise ratios. The findings obtained following bilateral lesions are also summarized in Table I. Compared with the preoperative levels, the mean magnitude of the BM LDs observed with both tests were significantly reduced (P < 0.001) in magnitude following the second operation. The BMLDs found with the phase test were reduced by 31 whereas the BMLDs in the intensity test were reduced by 63 %. Although all cats exhibited BMLDs with the phase test, three of the six cats which were tested with the intensity test following bilateral lesions exhibited no evidence o f a BMLD. Histological examination of cortical lesions and thalamic degeneration revealed no obvious anatomical basis for the unique findings with these three cats. All six cats had similar lesions which included complete ablation of auditory subdivisions AI, All, Ep, SII, and I-T. The extent of under-cutting of non-auditory cortical regions also did not differentiate the two groups. Prior to beginning the present experiment, and again after its completion, we measured the analogous human BMLDs using the same stimulus presentation procedures, experimental audiometer, and earphones (mounted in a human stereo headset) as used for the cats. With three normal hearing subjects the mean human BMLD with the phase test was found to be 7.5 dB whereas with the intensity test the mean BMLD was 5.2 dB. These findings confirm the present and previous results with cats2, 5 and humans 4 which indicated that significantly larger BMLDs occur in experimental situations involving interaural differences in the phase relationships of signals and noise as compared to differences in intensity relations. The present experimental findings suggest that BMLDs, instead of being exclusively a cortically dependent binaural hearing phenomenon, are mediated at least in part by a subcortical analyzing system possibly localized in the superior olivary complex. This hypothesis is further reinforced by the additional finding obtained in the present experiment indicating that the BMLD is an unlearned phenomenon. Before the first cortical operation, no learning was necessary for the occurrence of BMLDs other than that related to learning to wear helmets and responding to low intensity sounds. At the first opportunity for the occurrence o f a BMLD, i.e., upon first receiving tests with S~No or SmNo following a series of prior threshold tests with the respective homophasic conditions, the cats exhibited BMLDs. Similar findings were obtained following unilateral and bilateral cortical operations. When we first completed the present experiment, we interpreted the finding of decreased BMLDs following bilateral cortical operations to be a secondary result of the increased emotionality (as reflected in increased spontaneous activity and less consistent day-to-day performance) which
385 is observed, at least to some degree, in most cats following bilateral lesions. However, the findings from an experiment completed subsequent to the B M L D study suggests that the reduction in the size of the BMLDs may actually reflect the disturbance of a normal cortical role. In brief, two of the present cats (3608, 7263), which had reduced BMLDs, have subsequently been found to have normal thresholds for detecting interaural reversals in the intensity and phase relationships of binaural 1 K H z tones. This research was supported by N I N C D S grants NS 11812 and NS 10940.
1 Cranford, J. L., Auditory masking level differences in the cat, J. comp. physioL PsychoL, 89 (1975) 219-223. 2 Cranford, J. L., Role of neocortex in binaural hearing in the cat. I. Contralateral masking, Brain Research, 100 (1975) 395-406. 3 Cranford, J. L. and Oberholtzer, M., Role of neocortex in binaural hearing in the cat. II. The 'precedence effect' in sound localization, Brain Research, 111 (1976) 225-239. 4 Green, D. M. and Henning, G. B., Audition, Ann. Rev. Psychol., 20 (1969) 105-128. 5 Wakeford, O. S. and Robinson, D. E., Detection of binaurally masked tones by the cat, J. acoust. Soc. Amer., 56 (1974) 952-956.