Brain Research, 176 (1979) 375-379 © Elsevier/North-Holland Biomedical Press
375
Auditory cortex lesions and auditory-visual associative learning in cats
JERRY L. CRANFORD Department of Otolaryngology, University of Texas Medical Branch, Galveston, Texas 77550 (U.S.A.)
(Accepted July 12th, 1979)
Early concepts of neocortical function were dominated by the notion that the cortical receiving areas of the auditory nervous system were necessary for the conscious sensation of sounds, whereas unlearned reflexive or overtrained automatic habits were mediated at a subcortical level. The evidence up to 1930 suggested that destruction of auditory cortex might produce total deafness for all sounds3,9,10. Although the extreme cortical deafness hypothesis was soon refuted by controlled laboratory investigations135, subsequent research has been dominated by attempts to identify possible physical or perceptual attributes of sounds for which animals without auditory cortex are functionally 'deaf'. It now appears that the search for primary sensory roles for auditory cortex in normal hearing has reached an impasse. Current evidence strongly suggests that destruction of auditory cortex has no permanent effect on the ability to discriminate the basic physical parameters (frequency, intensity) of sounds 7A1,16. In addition, the notion that auditory cortex might have a critical sensory role in discriminating the temporal aspects of sounds has also been questioned by more recent research 6,8,1~. In view of this state of affairs, the present investigator recently began a program of research designed to investigate the possibility that auditory cortex might be involved in allowing animals to form learned associations between auditory and visual aspects of their environment. In the past, such 'higher order' intermodal integrative functions were assumed to be the property of the so-called associative areas of the cortex. However, in recent years, there has been a growing amount of anatomical, electrophysiological, and behavioral data2,4,5, a4 indicating that auditory cortex may be less exclusively auditory in function than previously assumed. The present report constitutes a progress report on this new line of research. It is felt that a preliminary report is worthwhile at this time inasmuch as the initial results do indicate the possibility of an associative role for auditory cortex which should be of interest to other workers in the field. Three cats were trained in each of 3 experiments before and after one-stage bilateral ablations of auditory cortex situated between the suprasylvian sulcus and the rhinal fissure (auditory fields AI, AlI, Ep, SII, l-T). Because of the visual requirements of the present tasks, care was taken in surgery to minimize under-cutting of the supra-
376 sylvian and lateral gyrii (visual cortex). The success of this effort was indicated by the presence of only sparse amounts of retrograde degeneration in the LP-pulvinar complex and in the lateral geniculate nucleus. The small amount of variation in amount of degeneration seen in individual cases was not correlated with differences in behavioral performance. In Experiment [ cats were first trained to cross to the opposite compartment of a shuttle box to avoid shock whenever 10 sec trains of I kHz tone pulses were presented from overhead free-field speakers. The tone pulses were I sec in duration with I sec inter-pulse intervals and measured 65 dB SPL at the normal location of the cat's head in the apparatus. Cats received 10 trials per day with inter-trial intervals randomized between 30 and 90 sec. Next, the cats were further trained to respond to tones in the absence of pulsing lights. The pulsing light stimulation was provided by alternately lowering the room illumination level inside the IAC chamber from 180 to 160 foot-candles (measured 6 in. below the ceiling light fixture) by means of a Triac AC power supply. One second periods of reduced illumination levels were alternated with one second periods of normal ambient levels. When presented, the periods of reduced illumination levels were timed to coincide with the occurrence of the tone pulses. In each daily training session, the pulsing light stimuli were present only during a random half (5) of the tone trials, being absent during the remaining trials. It is important to note that, whenever pulsing lights were present during a given tone trial, pulsing lights were also continually present during the preceding inter-trial interval. Likewise, for trials containing no pulsing light stimuli, the preceding inter-trial intervals contained steady ambient levels. Thus, changes from one conditional cue condition to the other occurred only at the conclusion of a given trial. The design of Experiment ll was the exact opposite of Experiment I. Cats were first trained to respond to trials consisting of 10 sec periods of pulsing light stimuli. Next, the cats were further trained to respond to pulsing lights only when continual pulsing tones were present in the background and to inhibit responses in the absence of tonal signals. Except for the important difference that cats were required to use the presence or absence of tonal signals as conditional cues for responding or withholding responses to pulsing light trials, the procedures used in Experiment I I were identical to those of Experiment I. In Experiment III cats were first trained to respond to 10 sec trials involving the simultaneous presentation of pulsing light and tone stimuli. After learning to respond to compound stimuli, cats were further trained to inhibit responses during trials in which either tone or light signals were presented alone. Cats received 30 trials per day, 10 of which were with compound light-tone stimuli, and 10 each with light alone or tone alone. A constant 30 sec inter-trial interval was combined with a procedure of randomizing the order of the 3 types of trials. Fig. 1 presents the findings obtained with one representative cat from each of the three experiments. The results from Experiment I indicate that normal cats have difficulty consistently using visual stimuli as conditional cues for respondi~lg to sounds. Before surgery, the 3 cats required a mean of 400 trials (range: 320-490 trials) to reach a training criterion of two consecutive days of 90 ~ correct or better. Auditory cortex lesions, while producing temporary amnesia, did not appear to significantly alter the
377
EXPERIMENT I PREOPERATIVE
~
50
POSTOPERATIVE
. . . . . . . . . . . . . . . . . . .
m O-
O
t
I
t
[
I
1
10
20
30
40
I I
49 1
I
I
f
I
10
20
30
39
DAYS OF TESTING
EXPERIMENT PREOPERATIVI
II
EXPERIMENT
POSTOPERATIVE
5
PREOPERATIVE
III
POSTOPERATIVE
-
~ o. DAYS OF TESTING
9,9q
0 .~2~._o 1
J 10
,, 22
. = TO.E + UG.T ~ 10
+ 22
DAYS OF TESTING
Fig. 1. Presents typical behavioral findings obtained in each of the 3 auditory-visual associative experiments. The graphs only depict performance during sessions in which cats were required to learn the significance of the presence or absence of conditional light or tone cues (Experiments I, 11) or to discriminate compound light and tone stimuli from trials in which light or tone signals were presented alone (Experiment III). The Experiment II[ graph does not depict performance on the light-alone trials since none of the cats made any errors during these trials. See the text for details. diffÉculty level of the task. After surgery, the cats required a mean of 357 trials (range: 180-500 trials) to reattain the preoperative criterion. The results of Experiment II, in contrast, show that while normal cats have considerably less difficulty using sounds as conditional cues for responding to visual stimuli (mean of 133 trials; range of 120-150 trials), there is evidence for a temporary postoperative impairment. After surgery, the 3 cats required a mean of 330 trials (range: 260-390 trials) to relearn the task to preoperative levels. A possible clue to the nature of the postoperative difficulties exhibited by cats in Experiment II was provided by an analysis of the types of training errors which cats made before and after surgery. The results of this error analysis are presented in Fig. 2. Before surgery, the nature of the errors made by cats in Experiments I and I1 were quite different. In Experiment I, the greatest proportion of errors resulted from cats failing to respond to tones when pulsing lights were present in the background, rather than responding in the absence of conditional light stimuli. In marked contrast, cats in Experiment l! made proportionately fewer errors during trials in which conditional tone cues were present. After surgery, cats in both experiments made proportionately more errors in the presence of the respective pulsing conditional cues than in their absence. These results suggest that, for both normal and operated cats, pulsing lights exert little control over the cats' responses to tones. The results of Experiment II, however, suggest that tones become less efficacious in controlling the cats' response to visual stimuli only after cortical operations. It is unlikely that this latter effect can be
378 completely accounted for in terms of a shift in the relative perceptual saliency of the auditory and visual stimuli since previous experiments ~3 failed to show a change in the normal dominance of hearing over vision in cats following auditory cortex lesions. Also, the results of Experiment 111, to be described next, further contra-indicates any simple change in normal auditory-visual dominance relationships. The results of Experiment ili provide a second possible clue to the nature of the deficit observed in Experiment 11. In this experiment, after cats had learned to respond to compound pulsing light and tone trials, they were further trained to inhibit responses when pulsing lights or pulsing tones were presented alone. That all 3 cats solved the initial compound cue task on the basis of the tones was evidenced by the fact that subsequent training was entirely devoted to conditioning the cats to inhibit responses to tones alone. In fact, before as well as after surgery, none of the cats made any errors during trials in which pulsing lights were presented alone. These results suggest that the postoperative difficulties exhibited by the cats of Experiment I! may have been at least partly due to an attention problem. The lack of any deficit in Experiment 111, other than temporary amnesia, may have been due to the fact that, during compound cue trials, the onset of the light and tone signals was a simultaneous event. In Experiment 1I, the tones were turned on anywhere from 30 to 90 sec prior to the occurrence of pulsing light trials. This may have allowed the operated animals to habituate or become
EXPERIMENT I
E X P E R I M E N T II
I
I TQN,E : CONDITIONAL STIMULUS
LIGHT : CONDITIONAL STIMULUS I TONE = RESPONSE STIMULUS I
1.0-
BEFORE SURGERY
AFTER SURGERY
O0 er
0
er tr LU .J
I
LIG,.HT = RESPONSE STIMULUS 1,0
BEFORE SURGERY
AFTER SURGERY
S+ S-
S+ S-
o.8
.8-
~< .60pZ 0
.4-
m0
~- . 2 o
Z 0
.4
0~
"2
0-
rr 0_
S+ S-
S+ SCONDITIONAL CUES
Fig. 2. Depicts the relative proportion of discrimination errors which cats in Experiments I and II made during trials containing conditional cues (S-+) as compared to trials in which conditional cues were absent (S--). The graphs show the mean performance Of all 3 cats in each experiment averaged over all training sessions. The performance of individual cats in both experiments conformed to the group trend.
379 s o m e h o w less attentive to the presence o f the tones p r i o r to the occurrence o f pulsing lights. It must be emphasized, however, t h a t the deficit exhibited by the operated cats in E x p e r i m e n t II was n o t p e r m a n e n t . All 3 cats eventually relearned to p r e o p e r a t i v e levels. Therefore, the present findings indicate the occurrence o f a t e m p o r a r y neural i m p a i r m e n t due to loss o f a n o r m a l cortical function (or to the removal o f n o r m a l cortical influences o n o t h e r parts o f the a u d i t o r y nervous system) from which eventual recovery or c o m p e n s a t i o n is possible. Thus, in a d d i t i o n to investigating possible nonsensory roles for cortex in hearing, this kind o f evidence strongly indicates the need to also take a systematic l o o k at recovery p h e n o m e n a and changing effects after lesions. This line o f research is c o n t i n u i n g in the a u t h o r ' s University of Texas Medical Branch l a b o r a t o r y . W e are c u r r e n t l y i m p l e m e n t i n g some new o p e r a n t c o n d i t i o n i n g techniques in an a t t e m p t to e x p a n d the scope a n d b r e a d t h o f future studies. This research was s u p p o r t e d by a g r a n t from the Deafness Research F o u n d a t i o n a n d was p e r f o r m e d while the a u t h o r was at Baylor College o f Medicine, H o u s t o n , Texas.
1 Bard, P. and Rioch, D. M., A study of four cats deprived of neocortex and additional portions of the forebrain, Bull. Johns Hopk. Hosp., 60 (1937) 75-147. 2 Bignall, K. E., lmbert, M. and Buser, P., Optic projections to non-visual cortex of the cat, J. Neurophysiol., 29 (1966) 396-409, 3 Bramwell, E., A case of cortical deafness, Brain, 50 (1927) 579-580. 4 Colavita, F. B., Auditory cortical lesions and visual pattern discrimination in cat, Brain Research, 39 (1972) 437-447. 5 Colavita, F. B., Insular-temporal lesions and vibrotactile temporal pattern discrimination in cats, Physiol. Behav., 12 (1974) 215-218. Cranford, J. L., lgarashi, M. and Stramler, J. H., Effect of auditory neocortex ablation on identification of click rates in cats, Brain Research, 116 (1976) 69-81. 7 Cranford, J. L., lgarashi, M. and Stramler, J. H., Effect of auditory neocortex ablation on pitch perception in the cat, J. NeurophysioL, 39 (1976) 143-152. 8 Cranford, J. L., lgarashi, M. and DeWitt, R., Role of neocortex in interaural intensity and phaseangle discrimination: detection vs. identification, Neurosci. Abstr,, 3 (1977) 5. 9 Ferrier, D., The Function of the Brain, 2nd Ed., Smith, Elder, London, 1886. 10 Ferrier, D., The Croonian Lectures on Cerebral Localization, Smith, Elder, London, 1890. 11 Goldberg, J. M. and Neff, W. D., Frequency discrimination after ablation of cortical auditory areas, J. Neurophysiol., 24 (1961) 119-128. 12 Heffner, H. and Masterton, B., Contribution of auditory cortex to sound localization in the monkey (Macaea mulatta), J. Neurophysiol., 38 (1975) 1340-1358. 13 Jane, J. A., Masterton, R. B. and Diamond, I. T., The function of the tectum for attention to auditory stimuli in the cat, J. comp. NeuroL, 125 (1965) 165-192. 14 Marty, R., Etude topographique et stratigraphique des projection du corps genoville lateral sur le cortex cerebral, Arch. itaL BioL, 107 (1969) 723-742. 15 Mettler, F. A., Finch, G., Girden, E. and Culler, E. A., Acoustic value of the several components of the auditory pathway, Brain, 57 (1934) 475-483. 16 Raab, D. W. and Ades, H. W., Cortical and midbrain mediation of a conditioned discrimination of acoustic intensities, Amer. J. PsychoL, 59 (1946) 127-136.
375
Auditory cortex lesions and auditory-visual associative learning in cats
JERRY L. CRANFORD Department of Otolaryngology, University of Texas Medical Branch, Galveston, Texas 77550 (U.S.A.)
(Accepted July 12th, 1979)
Early concepts of neocortical function were dominated by the notion that the cortical receiving areas of the auditory nervous system were necessary for the conscious sensation of sounds, whereas unlearned reflexive or overtrained automatic habits were mediated at a subcortical level. The evidence up to 1930 suggested that destruction of auditory cortex might produce total deafness for all sounds3,9,10. Although the extreme cortical deafness hypothesis was soon refuted by controlled laboratory investigations135, subsequent research has been dominated by attempts to identify possible physical or perceptual attributes of sounds for which animals without auditory cortex are functionally 'deaf'. It now appears that the search for primary sensory roles for auditory cortex in normal hearing has reached an impasse. Current evidence strongly suggests that destruction of auditory cortex has no permanent effect on the ability to discriminate the basic physical parameters (frequency, intensity) of sounds 7A1,16. In addition, the notion that auditory cortex might have a critical sensory role in discriminating the temporal aspects of sounds has also been questioned by more recent research 6,8,1~. In view of this state of affairs, the present investigator recently began a program of research designed to investigate the possibility that auditory cortex might be involved in allowing animals to form learned associations between auditory and visual aspects of their environment. In the past, such 'higher order' intermodal integrative functions were assumed to be the property of the so-called associative areas of the cortex. However, in recent years, there has been a growing amount of anatomical, electrophysiological, and behavioral data2,4,5, a4 indicating that auditory cortex may be less exclusively auditory in function than previously assumed. The present report constitutes a progress report on this new line of research. It is felt that a preliminary report is worthwhile at this time inasmuch as the initial results do indicate the possibility of an associative role for auditory cortex which should be of interest to other workers in the field. Three cats were trained in each of 3 experiments before and after one-stage bilateral ablations of auditory cortex situated between the suprasylvian sulcus and the rhinal fissure (auditory fields AI, AlI, Ep, SII, l-T). Because of the visual requirements of the present tasks, care was taken in surgery to minimize under-cutting of the supra-
376 sylvian and lateral gyrii (visual cortex). The success of this effort was indicated by the presence of only sparse amounts of retrograde degeneration in the LP-pulvinar complex and in the lateral geniculate nucleus. The small amount of variation in amount of degeneration seen in individual cases was not correlated with differences in behavioral performance. In Experiment [ cats were first trained to cross to the opposite compartment of a shuttle box to avoid shock whenever 10 sec trains of I kHz tone pulses were presented from overhead free-field speakers. The tone pulses were I sec in duration with I sec inter-pulse intervals and measured 65 dB SPL at the normal location of the cat's head in the apparatus. Cats received 10 trials per day with inter-trial intervals randomized between 30 and 90 sec. Next, the cats were further trained to respond to tones in the absence of pulsing lights. The pulsing light stimulation was provided by alternately lowering the room illumination level inside the IAC chamber from 180 to 160 foot-candles (measured 6 in. below the ceiling light fixture) by means of a Triac AC power supply. One second periods of reduced illumination levels were alternated with one second periods of normal ambient levels. When presented, the periods of reduced illumination levels were timed to coincide with the occurrence of the tone pulses. In each daily training session, the pulsing light stimuli were present only during a random half (5) of the tone trials, being absent during the remaining trials. It is important to note that, whenever pulsing lights were present during a given tone trial, pulsing lights were also continually present during the preceding inter-trial interval. Likewise, for trials containing no pulsing light stimuli, the preceding inter-trial intervals contained steady ambient levels. Thus, changes from one conditional cue condition to the other occurred only at the conclusion of a given trial. The design of Experiment ll was the exact opposite of Experiment I. Cats were first trained to respond to trials consisting of 10 sec periods of pulsing light stimuli. Next, the cats were further trained to respond to pulsing lights only when continual pulsing tones were present in the background and to inhibit responses in the absence of tonal signals. Except for the important difference that cats were required to use the presence or absence of tonal signals as conditional cues for responding or withholding responses to pulsing light trials, the procedures used in Experiment I I were identical to those of Experiment I. In Experiment III cats were first trained to respond to 10 sec trials involving the simultaneous presentation of pulsing light and tone stimuli. After learning to respond to compound stimuli, cats were further trained to inhibit responses during trials in which either tone or light signals were presented alone. Cats received 30 trials per day, 10 of which were with compound light-tone stimuli, and 10 each with light alone or tone alone. A constant 30 sec inter-trial interval was combined with a procedure of randomizing the order of the 3 types of trials. Fig. 1 presents the findings obtained with one representative cat from each of the three experiments. The results from Experiment I indicate that normal cats have difficulty consistently using visual stimuli as conditional cues for respondi~lg to sounds. Before surgery, the 3 cats required a mean of 400 trials (range: 320-490 trials) to reach a training criterion of two consecutive days of 90 ~ correct or better. Auditory cortex lesions, while producing temporary amnesia, did not appear to significantly alter the
377
EXPERIMENT I PREOPERATIVE
~
50
POSTOPERATIVE
. . . . . . . . . . . . . . . . . . .
m O-
O
t
I
t
[
I
1
10
20
30
40
I I
49 1
I
I
f
I
10
20
30
39
DAYS OF TESTING
EXPERIMENT PREOPERATIVI
II
EXPERIMENT
POSTOPERATIVE
5
PREOPERATIVE
III
POSTOPERATIVE
-
~ o. DAYS OF TESTING
9,9q
0 .~2~._o 1
J 10
,, 22
. = TO.E + UG.T ~ 10
+ 22
DAYS OF TESTING
Fig. 1. Presents typical behavioral findings obtained in each of the 3 auditory-visual associative experiments. The graphs only depict performance during sessions in which cats were required to learn the significance of the presence or absence of conditional light or tone cues (Experiments I, 11) or to discriminate compound light and tone stimuli from trials in which light or tone signals were presented alone (Experiment III). The Experiment II[ graph does not depict performance on the light-alone trials since none of the cats made any errors during these trials. See the text for details. diffÉculty level of the task. After surgery, the cats required a mean of 357 trials (range: 180-500 trials) to reattain the preoperative criterion. The results of Experiment II, in contrast, show that while normal cats have considerably less difficulty using sounds as conditional cues for responding to visual stimuli (mean of 133 trials; range of 120-150 trials), there is evidence for a temporary postoperative impairment. After surgery, the 3 cats required a mean of 330 trials (range: 260-390 trials) to relearn the task to preoperative levels. A possible clue to the nature of the postoperative difficulties exhibited by cats in Experiment II was provided by an analysis of the types of training errors which cats made before and after surgery. The results of this error analysis are presented in Fig. 2. Before surgery, the nature of the errors made by cats in Experiments I and I1 were quite different. In Experiment I, the greatest proportion of errors resulted from cats failing to respond to tones when pulsing lights were present in the background, rather than responding in the absence of conditional light stimuli. In marked contrast, cats in Experiment l! made proportionately fewer errors during trials in which conditional tone cues were present. After surgery, cats in both experiments made proportionately more errors in the presence of the respective pulsing conditional cues than in their absence. These results suggest that, for both normal and operated cats, pulsing lights exert little control over the cats' responses to tones. The results of Experiment II, however, suggest that tones become less efficacious in controlling the cats' response to visual stimuli only after cortical operations. It is unlikely that this latter effect can be
378 completely accounted for in terms of a shift in the relative perceptual saliency of the auditory and visual stimuli since previous experiments ~3 failed to show a change in the normal dominance of hearing over vision in cats following auditory cortex lesions. Also, the results of Experiment 111, to be described next, further contra-indicates any simple change in normal auditory-visual dominance relationships. The results of Experiment ili provide a second possible clue to the nature of the deficit observed in Experiment 11. In this experiment, after cats had learned to respond to compound pulsing light and tone trials, they were further trained to inhibit responses when pulsing lights or pulsing tones were presented alone. That all 3 cats solved the initial compound cue task on the basis of the tones was evidenced by the fact that subsequent training was entirely devoted to conditioning the cats to inhibit responses to tones alone. In fact, before as well as after surgery, none of the cats made any errors during trials in which pulsing lights were presented alone. These results suggest that the postoperative difficulties exhibited by the cats of Experiment I! may have been at least partly due to an attention problem. The lack of any deficit in Experiment 111, other than temporary amnesia, may have been due to the fact that, during compound cue trials, the onset of the light and tone signals was a simultaneous event. In Experiment 1I, the tones were turned on anywhere from 30 to 90 sec prior to the occurrence of pulsing light trials. This may have allowed the operated animals to habituate or become
EXPERIMENT I
E X P E R I M E N T II
I
I TQN,E : CONDITIONAL STIMULUS
LIGHT : CONDITIONAL STIMULUS I TONE = RESPONSE STIMULUS I
1.0-
BEFORE SURGERY
AFTER SURGERY
O0 er
0
er tr LU .J
I
LIG,.HT = RESPONSE STIMULUS 1,0
BEFORE SURGERY
AFTER SURGERY
S+ S-
S+ S-
o.8
.8-
~< .60pZ 0
.4-
m0
~- . 2 o
Z 0
.4
0~
"2
0-
rr 0_
S+ S-
S+ SCONDITIONAL CUES
Fig. 2. Depicts the relative proportion of discrimination errors which cats in Experiments I and II made during trials containing conditional cues (S-+) as compared to trials in which conditional cues were absent (S--). The graphs show the mean performance Of all 3 cats in each experiment averaged over all training sessions. The performance of individual cats in both experiments conformed to the group trend.
379 s o m e h o w less attentive to the presence o f the tones p r i o r to the occurrence o f pulsing lights. It must be emphasized, however, t h a t the deficit exhibited by the operated cats in E x p e r i m e n t II was n o t p e r m a n e n t . All 3 cats eventually relearned to p r e o p e r a t i v e levels. Therefore, the present findings indicate the occurrence o f a t e m p o r a r y neural i m p a i r m e n t due to loss o f a n o r m a l cortical function (or to the removal o f n o r m a l cortical influences o n o t h e r parts o f the a u d i t o r y nervous system) from which eventual recovery or c o m p e n s a t i o n is possible. Thus, in a d d i t i o n to investigating possible nonsensory roles for cortex in hearing, this kind o f evidence strongly indicates the need to also take a systematic l o o k at recovery p h e n o m e n a and changing effects after lesions. This line o f research is c o n t i n u i n g in the a u t h o r ' s University of Texas Medical Branch l a b o r a t o r y . W e are c u r r e n t l y i m p l e m e n t i n g some new o p e r a n t c o n d i t i o n i n g techniques in an a t t e m p t to e x p a n d the scope a n d b r e a d t h o f future studies. This research was s u p p o r t e d by a g r a n t from the Deafness Research F o u n d a t i o n a n d was p e r f o r m e d while the a u t h o r was at Baylor College o f Medicine, H o u s t o n , Texas.
1 Bard, P. and Rioch, D. M., A study of four cats deprived of neocortex and additional portions of the forebrain, Bull. Johns Hopk. Hosp., 60 (1937) 75-147. 2 Bignall, K. E., lmbert, M. and Buser, P., Optic projections to non-visual cortex of the cat, J. Neurophysiol., 29 (1966) 396-409, 3 Bramwell, E., A case of cortical deafness, Brain, 50 (1927) 579-580. 4 Colavita, F. B., Auditory cortical lesions and visual pattern discrimination in cat, Brain Research, 39 (1972) 437-447. 5 Colavita, F. B., Insular-temporal lesions and vibrotactile temporal pattern discrimination in cats, Physiol. Behav., 12 (1974) 215-218. Cranford, J. L., lgarashi, M. and Stramler, J. H., Effect of auditory neocortex ablation on identification of click rates in cats, Brain Research, 116 (1976) 69-81. 7 Cranford, J. L., lgarashi, M. and Stramler, J. H., Effect of auditory neocortex ablation on pitch perception in the cat, J. NeurophysioL, 39 (1976) 143-152. 8 Cranford, J. L., lgarashi, M. and DeWitt, R., Role of neocortex in interaural intensity and phaseangle discrimination: detection vs. identification, Neurosci. Abstr,, 3 (1977) 5. 9 Ferrier, D., The Function of the Brain, 2nd Ed., Smith, Elder, London, 1886. 10 Ferrier, D., The Croonian Lectures on Cerebral Localization, Smith, Elder, London, 1890. 11 Goldberg, J. M. and Neff, W. D., Frequency discrimination after ablation of cortical auditory areas, J. Neurophysiol., 24 (1961) 119-128. 12 Heffner, H. and Masterton, B., Contribution of auditory cortex to sound localization in the monkey (Macaea mulatta), J. Neurophysiol., 38 (1975) 1340-1358. 13 Jane, J. A., Masterton, R. B. and Diamond, I. T., The function of the tectum for attention to auditory stimuli in the cat, J. comp. NeuroL, 125 (1965) 165-192. 14 Marty, R., Etude topographique et stratigraphique des projection du corps genoville lateral sur le cortex cerebral, Arch. itaL BioL, 107 (1969) 723-742. 15 Mettler, F. A., Finch, G., Girden, E. and Culler, E. A., Acoustic value of the several components of the auditory pathway, Brain, 57 (1934) 475-483. 16 Raab, D. W. and Ades, H. W., Cortical and midbrain mediation of a conditioned discrimination of acoustic intensities, Amer. J. PsychoL, 59 (1946) 127-136.
