Effect of Auditory Neocortex Ablation on Pitch Perception in the Cat JERRY
L. CRANFORD,
MAKOTO
IGARASHI,
AND
Department of Otorhinolaryngology and Communicative Baylor College of Medicine, Houston, Texas 77025 REVIEW (9) Of the experimental literature related to the behavioral effects of auditory cortex lesions concluded that discriminations involving the “recognition” of soundssuffer more than do tasks requiring only the “detection” of new signals. Recognition tasks are ones in which animals are required to discriminate more than one type of change in the auditory environment by responding to certain changes and withholding response to other changes or, alternately, making discriminably different responsesto each of the changes.Detection tasks, in contrast, only require a single responseto a unitary changein the characteristics of the background signals. Although this procedural distinction hasbeen quite successful in accounting for the outcome of numerous ablation studies, a number of experimental exceptions do exist. For example, detection tasks involving changesin either the duration of individual tone pulsesor the temporal patterning of a seriesof tones are severely disrupted by large bilateral ablation of auditory cortex (6, 21). More recently, Brown et al. (3) found that cats with bilateral lesions of auditory cortex could perform a recognition task which involved the discrimination of increasesfrom decreasesin the frequency of ongoing tone pulses.Theselatter investigators, however, reported that several of the lesionswere smaller than intended, thus raising the possibility that the successfui postoperative performance may have been the result of sparingof critical amountsof auditory cortex, In view of the relatively large degree of theoretical importance (11, 16, 17, 23) that has been attached to the distinction between recognition and detection tasks in terms of neocortical function, we felt that further investigation of the role of neocortex in these two forms of discrimination would be worthwhile. One research area which we consideredto be in need of additional investigation concerns the role of neocortex in frequency discrimination. Prior to the report of Brown et al., investigators had conA RECENT
Receivedfor publication
June
27, 1975.
JAMES I-I. STRAMLER Sciences,
eluded that, while auditory decorticate cats could successfully detect changes in the frequency of ongoingtonal signals(4, 11, 23), they could not perform recognition tasks which required the discrimination of tones of different frequency against a silent background (1, 23). The first goal of the experiments to be described in the present report, therefore, was to test the basic Brown et al. experimental design to determine whether, in fact, cats in which all neocortical targets of the medial geniculate nucleus and posterior group of the thalamus are bilaterally ablated can perform a recognition task. A secondobjective was to administer, to any cats which were retrainable postoperatively, a series of special discrimination transfer or stimulus equivalence tests to determine whether operated cats use different cues to solve the basic discrimination problem than do unoperated cats; i.e., whether the cat’s “perception” of auditory frequency is changed in any way by the presenceof the cortical lesion METHODS
Subjects A total of I2 adult cats were tested in the present experiment. The cats were selected on the basisof general health and temperamentas well asthe presenceof clean external ear canals and normal appearing tympanic membranes. Four cats (B-3504, B-3572, B-3577, and B-3984) served as unoperated controls for the present seriesof tests. Of the remaining eight cats, half (B-1349, B-2616, B-2618, and B-2787) were tested before and after one-stage bilateral auditory cortex ablations, whereasthe other four cats (B-1347, B-2303, B-2502, and B-2789) received two-stage ablations with retraining given between the first and second operations. Apparatus All cats were trained with a shock-avoidance procedure in a two-way shuttle box. Auditory stimuli were presented from Lansing LE-85 speakersmounted at the top of the grill box 48 143
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144
CRANFORD,
IGARASHI,
inches directly above the center of the floor of each compartment. The speakers and training apparatus were located inside an IAC model 1202 sound-treated chamber which had a background sound level of approximately 36 dB re 0.0002 dyn/cm 2* The l.O- and 1.GkHz neutral frequencies used in the present experiment were generated by a Hewlett-Packard 200 CD wide-range audio oscillator, whereas the O.8-, 1.2-, and 2.0-kHz comparison signals were generated by a Krohn-Hite 4100 push-button oscillator. The outputs of the nectral and comparison oscillator were switched by a relay into an Iconix model 6837 electronic switch. The risefall time for all tone pulses was 100 ms. The after being fed successively gated tones, through an Iconix model 6836 programmable attenuator and a McIntosh MC-75 amplifier, were sent in a synchronous fashion to the two audio transducers. The relative onset times and signal durations were controlled by an Iconix model 6255 interval timer.
Stimulus presentation and test procedures In the first phase of the experiment nine cats were trained to cross to the opposite compartment of the grill box when an ongoing series of neutral LO-kHz tone pulses were made to alternate with tone pulses of 1.2 kHz. The remaining three cats (B-2787, B-2789, and B-3572) were trained to cross when neutral l.O-kHz tones alternated with O.8-kHz tones. The tone pulses were of 1 s duration with l-s silent intervals between successive pulses. If the cat had not initiated a cross to the opposite compartment by the beginning of the fourth consecutive warning tone (0.8 or 1.2 kHz, respectively), electric shock (paired with a loud buzzer) was intermittently applied to the pads of the cat’s feet through the grid floor of the training apparatus until the cat responded. The intertrial intervals (ITIs) ranged from 30 to 90 s, with a mean of 60 s. In order to prevent cats from using loudness differences as possible cues for responding, the intensity levels of the signals were randomly varied in 4-dB steps over a, 28-dB range. The sound pressure level of the O-8-, 1 .O-, 1.2-, 1.6-, and 2.0-kHz tones used in the present experiment was approximately 70 dB re 0.0002 dyn/cm2 at the midpoint of the 28-dB range of intensities used. The cats were trained 5-6 daysiwk with 12 trials each day until they achieved a minimum criterion of 3 consecutive days of 1 l/ 12 correct. The second phase of the experiment involved further training in which the cats were required to inhibit crosses to a frequency change oppo-
AND
STRAMLER
site in direction to that with which they had been previously trained. Thus, nine of the cats were trained to withhold crosses when the neutral LO-kHz tones alternated with 0.8-kHz tones (“negative trials”) but to continue crossing, as before, in response to changes involving 1.2-kHz tones (“positive trials”). Cats B-2787, B-2789, and B-3572 were trained with the converse condition requiring crosses to 0.8-kHz and noncrosses to 1.2-kHz signals. In order to avoid shock on negative trials, the cats had to inhibit crosses during a minimum of five alternations of the neutral and negative tones. Each cat received six positive and six negative trials each day. The order of daily presentation of the two types of trials was randomized with the restriction that not more than four consecutive trials could be of the same type. All other procedures were the same as described for the first phase of the experiment except that all cats, after they attained the original 3-day learning criterion, were routinely given 4 days of overtraining before proceeding to the next part of the experiment. The third phase of the experiment involved the presentation of a series of retention and discrimination transfer tests. What follows next is a description of these tests in the order of their presentation and the special procedures used to administer them. a )
POSTOPERATIVE
DISCRIMINATION-RETENTION
All bilaterally operated cats received in all respects to 3 days of tests, identical the last three training sessions given prior to the last operation. The score on these tests constituted a measure of retention for the preoperative problem. If the retention score was above chance, the cats were continued with the same procedures in an attempt to retrain to the preoperative criterion. If the score was not above chance, then the cats were retrained on the first phase of the present experiment prior to attempting retraining with the second-phase problem.
TEST.
h)
FREQUENCY-GENERALIZATION
TEST,
This
test involved presenting special sessions in which the ITIs contained tonal pulses of 1.6 kHz frequency rather than 1.0 kHz. Two types of test trials were presented, the first being ones in which the ongoing 1.6-kHz tones alternated with tones of 2.0 kHz, and the second where the 1.6-kHz signals alternated with 1.2-kHz tones. Each cat received four such sessions, each containing 6 positive and 6 negative frequency changes, interspersed over days among regular retraining sessions on the original discrimination. Each cat had to achieve a criterion level of performance on the preceding days regular ses-
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CORTICAL
LESIONS
sion before receiving a stimulus-generalization session. On the generalization trials cats received occasional mild shock for failing to generalize their responses appropriately (i.e., failing to cross to the opposite compartment when the new frequency change was in the same direction as the original positive trials and failing to inhibit crosses when the new change was the same direction as previous negative trials). This was necessitated by the observation that some cats tended to “freeze” rather than cross to the opposite compartment when first presented with a positive trial containing a “novel” frequency value. C) ABSOLUTE-DISCRIMINATION TEST. After the cats were retrained to the original 3-day criterion level on regular sessions involving neutral LO-kHz signals, the LO-kHz tones were eliminated (i.e., the ITIs now contained no tones) and the cats were presented with an absolute discrimination between 1.2- versus 0.8kHz tone pulses. Four consecutive sessions, each containing six positive and six negative trials, were given. As with the generalization test, occasional mild shock was administered for inappropriate responding. In the generalization- and absolute-discrimination tests, all other procedures were the same as in the first two phases of the experiment (i.e., scrambling of tonal intensities, duration and rate of presentation of tone pulses, lengths of positive and negative trials, lengths of ITIs, etc.). d)
FREQUENCY-DISCRIMINATlON
This
THRESHOLD
test involved first retraining the bilaterally operated cats to criterion levels of performance with the original discrimination containing LO-kHz neutral tones and then decreasing the differences between positive and negative frequency values in lo-Hz steps over trials and sessions in an attempt to determine the thresholds for discriminating directional frequency changes. A modified method of limits was used to determine these values. During each session the differences between neutral and positive frequencies were reduced by decreasing (or increasing) the latter signal in lo-Hz steps until the cat failed to cross on a minimum of two of three trials. The differences were then increased in IO-Hz steps until the cat again responded on two or more consecutive trials. Shock was given for all incorrect responses. During each test session the differences between neutral and negative stimuli were also successively decreased and increased in a similar manner. Thus, two independent thresholds were measured, one for positive and one for negative frequency changes. All other procedures were the same as used in the original disTEST.
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145
crimination training except that scrambling of tonal intensities was eliminated whenever the frequency differences appeared to be in the region of the cat’s threshold. All four of the preceding tests were not given to every cat in the present experiment. The four unoperated control cats received the frequency-generalization and absolute-discrimination tests, but not the retention- or frequencydiscrimination threshold tests. The eight operated cats did receive all four tests, but only after bilateral cortical lesions. Prior to surgery and after unilateral operations, these cats were only trained to criterion with the fist two phases of the present experiment.
Surgical and histological procedures The auditory cortex was removed from the two hemispheres in either one or two stages by subpial aspiration under pentobarbital sodium anesthesia. Strict aseptic precautions were maintained throughout. Animals were allowed a minimum of 14 days of recovery from each operation before testing was resumed. At the end of the experiment, each animal was perfused with normal saline and 10% formalin. Prior to removing the brain, the ears were examined for any signs of abnormality. After a minimum storage period of 30 days in 10% formalin, the brain was embedded in egg yolk (8) and cut on a freezing microtome in the frontal plane at 25 pm. Every ninth section was stained with cresyl violet. The cortical lesions were reconstructed by systematic projection of frontal sections to a standard lateral plane. Retrograde degeneration in the dorsal thalamus was studied and drawn with the aid of a microprojector. RESULTS
Anatomical Figure 1 shows the reconstructed surface lesions in the eight cats translated to standardized lateral views of the cerebral hemisphere. On the basis of surface extent of cortical ablations and severity of retrograde degenerative changes in the dorsal thalamus, the present cases can be divided into three categories according to overa11 lesion size. Cats B-1347 and B-2789 had the largest lesions. In both cases severe degeneration was present bilaterally throughout the rostral-caudal extent of the principal and magnocellular divisions of the medial geniculate nucleus (GM) as well as the posterior group (PO). Extensive undercutting of the suprasylvian and lateral gyri occurred as evidenced by the presence of severe degeneration throughout the entire extent of the lateral geniculate nucleus (GL) as well as the lateral posterior-
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CRANFORD,
IGARASHI,
TWO-STAGE
AND
CORTICAL
STRAMLER
ABLATION B-2789
B-2303
B-2502
ONE-STAGE
FIG. 1 . Reconstructed ce re bra1 hemispheres.
cortical
CORTICAL
ABLATION
B-2787
I3- 2616
B- 1349
B-26t8
lesions
in eight operated
pulvinar (LP-PUL) complex. Degeneration was also present more anteriorly in the region of the lateral dorsal nucleus (LD). In B-1347 the degeneration anteriorly in LP and the lateral parts of LD was severe bilaterally, whereas in B-2789 it was, while extensive, more moderate in degree as evidenced by the presence of less severe gliosis plus occasional healthy-appearing cells. In both cases severe degeneration extended bilaterally into the ventrobasal complex, notably the lateral division of the ventroposterior nucleus (VPL). A second group of cats (B-2303, B-2502, B-2787, and B-261 6) also had severe retrograde degeneration present bilaterally throughout the entire extent of the principal and magnocellular divisions of GM. Degeneration in PO was severe bilaterally except, however, for the extreme caudal regions which had occasional
cats translated
to standardized
lateral
views
of the
normal-appearing cells present. Although moderate to severe amounts of degeneration were present throughout most of GL, LP, and PUL bilaterally, very little evidence for degeneration was found in the anterior regions of LP or in LD. Some degeneration was found bilaterally in the lateral aspects of the ventrobasal complex, although it was not as severe or extensive as in B-1347 and B-2789. Thalamic degeneration in the remaining two cats (B-1349 and B-2618) was similar to that of the intermediate group except that normalappearing cells were present bilaterally in the more caudal portions of the principal and magnocellular divisions of GM as well as PO. Also, overall, less severe degeneration was seen in LP, PUL, and GL than in the other cases. To illustrate the range of thalamic degeneration observed in the present cases we have
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CORTICAL
LESIONS
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147
6-2618
6
5
4
2
3
2. Thalamic degeneration in cats B-2618 and B-1347. Severe degeneration is depicted in solid black and slight degeneration is shown by stippling. Abbreviations are: CL, n. central lateral; CM, n. centromedian; GL, lateral geniculate body; GM, medial geniculate body, principal division; Ha, n. habenular; LD, n. laterodorsal; LP, n. lateroposterior; MC, medial geniculate body, magnocellular division; MD, n. mediodorsal; Pf, n. parafascicular; PO, posterior group; Pul, n. pulvinar; R, n. reticular; TO, optic tract; VGL, ventral lateral geniculate; VL, n. ventrolateral; VM, n. ventromedial; VP, n. ventroposterior; VPL, n, ventroposterior, lateral division; VPM, n. ventroposterior, medial division. FIG.
elected to depict, in Fig. 2, the degenerative tions of the present cases, each required more changes in the smallestlesion case(B-2618j as than twice the number of trials for retraining well as the largest (B-1347). (672 and 612 trials, respectively) than any of the other six operated cats.
Behavioral
1. Mean number of total trials to criterion on Jirst two phases ING. Table 1 summarizesthe number of total of discrimination task trials and mean errors per sessionrequired, be- _ TABLE
PHASE
ONE
AND
TWO
DTSCRIMINAT1ON
TR4IN-
fore and after the different cortical operations, for each of the three groups of cats to complete training with the first two phasesof the present experiment. Before surgery all three groups were reasonably equated in terms of speed of mastery of the basic discrimination task. The unilateral operation produced little disruption of the discrimination, with cats achieving criterion levels of performance in lessthan one-third the number of trials required before surgery. After bilateral lesionsthe two-stage cats, as a group, required more training than did one-stagecats to relearn the discrimination. However, this difference is the result of the fact that cats B-1347 and B-2789, which had the largest cortical abla-
Normal Cats
Beforesurgery
One-Stage Two-Stage Cats Cats
T: 411 T: 417 T: 393 E: 1.31(+) E: 1.78(+) E: OX(+) 0.96( - )
0.51(-)
After unilateral operation
O&6(-)
T: 114 E: 1.24(+)
OSO(--) After bilateral operation
T: 372 E: 1.44(+) 0.31(-)
T: 426 E: 1.89(+) O.%(-)
Also shown are the mean number of errors per session made on positive (+ ) and negative (- ) trials during phase-two training. T: trials; E: errors.
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IGARASHI,
With respect to the mean number of errors per session on positive and negative trials, 10 of the 12 cats consistently made more errors on positive than on negative trials throughout all phases of testing. However, one unoperated cat (B-3577) had a mean of 1.07 errors on positive and 1.67 errors on negative trials. Prior to the first operation only, cat B-2789 also made more errors on negative than on positive trials (means of 0.69 and 0.46 errors, respectively).
2. Mean individual uver 4 days of testing --
perj’urmances
All 4 days Normal
FREQUENCY-GENERALIZATION TEST. The left part of Table 2 summarizes the findings obtained on the generalization test with each of the three groups of cats. Presented separately are percentages “correct” on positive and negative trials. Positive and negative generalization trials are defined as ones which have frequency changes of the same direction as the trials with which each animal was originally trained. The percentages correct, therefore, reflect the degree to which cats respond in the same manner on the new positive and negative trials as they did on the original trials. All 12 cats performed significantly worse on generalization sessions than on the original discrimination (nonoverlapping distributions). Of the four unoperated cats, only two (B-3572 and B-3984) demonstrated above chance levels of performance, B-3577 and B-3504 both performed at chance levels. The former cat exhibited a high (and equal) probability of crossing on both positive and negative trials, whereas the latter cat, while crossing on fewer overall trials, was equally deficient at performing the transfer task. By comparison, three of the four two-stage cats demonstrated above chance levels of performance on the generalization test. Only cat B-1347 seemed unable to discriminate the new frequency changes, making as many crosses on negative as on positive trials.
Two-stage
trials
Absolute Test
Pos and neg, day 1 vs. day 4
Avg
B-3572 B-3577 B-3504 B-3984
50 80 49 63 61
97 20 54 87 65
74 50 52 75 63
50 58 33 50 48
vs. vs. vs. vs. vs.
B-1347 B-2303 B-,3502 B-2789
44 53 63 65 56
56 73 84 94 77
50 63 74 80 67
67 47 75 83 68
B-I349 B-2787 B-2616 B-2618
17 42 31 32 31
58 42 52 23 44
38 42 42 28 38
25 25 42 17 27
Aw
and negative
Test
Neg
A%
One-stage
on positive
Pos
A&
and 56
-Generalization
Cats
STRAMLER
B-2789, 26 and 96% correct for B-2303, and 100% correct for B-2502.
RETENTION TEST. The degree of retention exhibited by each of the eight cats after the bilateral lesion appears closely related to both the extent and severity of degenerative changes found in the dorsal thalamus as well as the type of surgical procedure received. Thus, the only one-stage cat which exhibited any signs of postoperative retention was B-2618, the cat with the smallest bilateral lesion. B-2618’s score over the 3 days of retention testing was 44% correct on positive trials and 100% correct on negative trials. (All scores reported on this and subsequent tests have been corrected for each cat’s rate of spontaneous crosses during ITIs according to the method described by Masterton and Diamond (14); individual rates of spontaneous activity in the present experiment were 10% or less.) The only two-stage cat which failed to show signs of postoperative retention was B-1347, the cat with the largest lesion. The retention scores for the remaining two-stage cats on positive and negative trials, were 15 and 96% correct for respectively,
TABLE
AND
AI1 4 days
Pos and neg, day. 1 vs. day 4
Pos
Neg
Avg
83 50 67 75 69
87 82 76 80 82
100 97 72 100 93
94 90 74 90 88
92 83 84 75 84
vs. 100 vs. 92 vs, 57 vs. 92 vs. 85
vs. vs. vs. vs. vs.
50 75 50 59 59
79 96 90 63 82
67 100 100 79 87
73 98 95 71 85
42 100 92 83 79
vs. 83 vs. 92 vs. 100 vs. 58 vs. 83
vs. vs. vs. vs. vs.
50 42 34 16 36
88 94 78 88 87
100 100 94 100 99
94 97 86 94 93
92 100 84 100 94
vs. 92 vs. 100 vs. 92 vs. 92 vs. 94
Values are percentages.
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CORTICAL
LESIONS
AND PITCH PERCEPTION
Relative to the findings with the unoperated and two-stage cats, those obtained with the one-stage animals were unexpected. All four of these cats made significantly (f = 2.506, df = 3, P < 0.05) more crosses on negative than on positive trials. Note that cat B-2787, which had been originally trained to cross to 0.8-kHz and inhibit crosses to 1.2-k& signals, also crossed less (inhibition?) on positive than on negative trials
TABLE 3. Smallest positive and negative frequency changes (in steps of IO Hz) which could be correctly discriminated on a minimum uf 5 of 10 trials
FREQUENCY-DISCRIMINATION TEST. Table 3 summarizes
THRESHOLD
for each of the eight bilaterally operated cats the smallest frequency differences which could be correctly discriminated at least 50% of the time. Each score represents the cat’s average performance on a minimum of 10 separate trials. Again, overall size of the cortical lesions appears to be a critical variable in determining the test results. Efforts to test the two cats with the largest bilateral lesions, B-1347 and B-2789, on this part of the experiment were unsuccessful. In response to attempts to reduce differences in positive and negative frequency values, these two cats quickly developed and maintained a pattern of either crossing to both types of frequency change or not responding to either. In contrast, the two cats with the smallest overall lesions, B-1349 and B-2618, demonstrated a discrimination threshold which appeared to be close to 10 Hz. When tones of 1,010 Hz were made to alternate with the neutral 1,000 Hz signals, both cats responded well above chance. However, when signals of 990 Hz were presented, the cats did not cross to the opposite compartment. This latter observation suggests that the 10 Hz-threshold involves being able to
- Positive Hz %
Operated Cats One-stage
B-1349 B-261 6 B-2618 B-2787
Two-stage
B-1347 B-2303 B-2502 B-2789
l
ABSOLUTE-DISCRIMINATION TEST. The right half of Table 2 summarizes the results obtained during the 4 days of absolute-discrimination testing. With the exception of cat B-2789, all animals performed significantly (t = 7.03, df = 11, P < 0.01) better on the absolute tests than they did on the generalization tests. Differences between the three groups of cats were small, although the mean score for the onestage cats was slightly higher than that of the other two groups. In order to determine the extent to which learning occurred over the 4 days of generalization and absolute testing, individual performances on the first and fourth test sessions were compared (Table 2). Although some cats in all three groups exhibited evidence of improvement over days of testing, only with the unoperated cats on the generalization test did this involve a majority (three of four cats) of the respective members.
149
1,010 1,020 1,010 980
84 50 91 73
Not testable 1,020 1,020
100 61
Not testable
Negative Hz % 990 980 990 1,060
83 64 80 62
Not testable 990 100 990 100 Not testable
recognize the nature of the frequency changes rather than simply detecting that a change has occurred.
The primary question of the present investigation of whether cats which have auditory cortical subdivisions AI, AII, Ep, I-T, and SII bilaterally ablated can discriminate increases from decreases in the frequency of ongoing tonal signals was answered in the affirmative. All eight operated cats were able to relearn the basic discrimination. The secondary question of whether cats with bilateral auditory cortex ablations use different cues than unoperated cats in solving the present type of discrimination problem was relatively easy to answer but difficult to interpret. This resulted from a dramatic difference in the performance of the one- and two-stage operated cats on the frequency generalization test. The fact that both unoperated and operated cats performed significantly better on the absolutediscrimination test than on the generalization test suggests that the animals solved the original problem more on the basis of the absolute frequency values of positive and negative tones than the directionality of the frequency changes. If one only compares the performance of the unoperated and two-stage cats, then the conclusion that operated and unoperated cats solve the discrimination problem in the same manner seems justified. However, the performance of the one-stage cats on the frequencygeneralization test appears qualitatively different from that of the other two groups. Rather than simply failing to correctly discriminate new positive from negative frequency changes, all four of these cats exhibited a marked tendency to continue responding on trials containing 1.2-kHz tones in the same manner as they
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had responded in original training. This suggeststhe paradoxical hypothesis that onestage operated cats are even more likely than either unoperated or two-stage operated cats to solve the present type of discrimination problem on the basis of absolute frequency cues. Although not intended as an explanation, one way to account for the present difference in the findings with one- and two-stage surgical procedures centers on the relationship between neural plasticity and a phenomenon known as the “serial lesion effect” (10). Clinical and experimental evidence is available (ref 10contains
a comprehensive review of this literature) which indicates that considerable sparing of function may occur in the nervous systemif the target region is ablated serially with time allowed for recovery between successiveoperations. A similar effect appearsto have occurred in the present investigation. The performance of the cats which received successiveunilateral operations with retraining given between operations did not differ from that of unoperated cats. The performance of the one-stage cats suggestsa functional deficit which may consist of either decreasedbehavioral flexibility (i.e., inability to perform successfully in situations which require both relative and absolute discriminations) or, alternately, a primary sensory deficit somehow involving stimulus generalization (5, 19, 24). The findings of the present investigation are of considerable significance in relation to two formal hypotheses regarding the functional capacities of auditory decorticate cats. Thompson (23), on the basis of published experiments (1, 23) which obtained evidence that cats (and dogs) with large bilateral auditory cortex lesions could not be trained to perform auditory tasks that required an absolute discrimination against a silent background, developed the hypothesis that the primary effects of auditory cortex ablations are to disrupt an animal’sability to inhibit responsesto “no-go” stimuli. The fact that all eight operated cats in the present experiment retained this latter behavioral capacity provides further evidence against Thompson’s hypothesis (2, 3, 12, 20). Neff (11, 16, 17), in reviewing the differences between auditory discriminations which can or cannot be acquired by cats with bilateral ablations of auditory cortex, developed a neural model from which a number of predictions concerning the auditory capacitiesof cortically ablated animals can be derived. Neff noted that auditory discriminations which had been previously found to survive cortical ablations have two features in common. The first is that the animal is required to detect a change in an on-
AND
STRAMLER
going auditory signal and the secondis that the change always involves either the introduction of a new frequency or an increase in the intensity of the ongoing signal (4, 11, 13, 18, 23). According to Neff, these two features are accompanied by two significant neural events which provide a basisfor solution. First, neural habituation occurs to the continuous presentation of the ongoing neutral signal and, second, the change in frequency or increasein intensity activates previously unactivated neural units. Changesin frequency are assumedto trigger a different group of units, whereas increasesin intensity evoke additional units over and above those already firing. Combined with the prior habituation to the ongoing signal, both of these changeseffectively result in an increase in the total amount of evoked neural activity. The animal’s task becomessimply one of detecting this increasedactivity and attaching appropriate behavioral responses. Changes in duration or pattern, on the other hand, involve temporal rearrangement of stimuli which are already present in the ongoing neutral signals and do not stimulatenew units to fire. Accordingly, animals with large bilateral auditory cortex lesions almost invariably fail on the latter type of discrimination task (6, 7, 21). Thus, Neff s model contains two basic propositions, one related to neural habituation and one to excitation of new neural units. The present finding that cats with complete bilateral removal of the neocortical targets of GM and PO can perform absolutefrequency discriminations againsta silent background would seemto question the universality of the first proposition, However, the relative validity of the second proposition is somewhat more difficult to determine. In postulating that a “larger neural event” is the basis on which auditory decorticate cats perform auditory discriminations, Neff did not specify whether the event was a simple “dimensionless” changeor whether discriminably different events might be correlated with certain stimulus parameters such as frequency. The results of the present experiment suggestthe latter alternative, In order to perform the present type of discrimination, cats have to make a differential responseto two different frequency changes.A successfulsolution requires recognition rather than a simple detection of increased neural activity. The results of the present investigation are, therefore, at variance with current concepts of the effects of auditory neocortex ablations in normal hearing processes.They also bring into sharpfocus the profound effect that differences in experimental procedure have on the outcome of different investigations. Whereas Thompson
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CORTICAL
LESIONS
(22, 23) had great difficulty training even unoperated cats to perform absolute discriminations, the procedures used in the present project appear to have facilitated equally quick solutions to this type of problem by both operated and unoperated cats. This suggests that the degree of difficulty previously assumed to be inherent in absolute discriminations may be more related to the method of training used than to any underlying sensory or learning factors (12). Although procedural variations have often been alluded to as possible underlying causes for apparent discrepancies in the results of different investigations, such variations, with few exceptions (12, 20, 22, 23, 25), have not been included as significant features of experimental designs in auditory research. It would seem that the inclusion of such procedural variables as specific independent measures in future experimental designs would provide valuable new insights into the neural mechanisms of normal hearing. SUMMARY
Cats which received one- or two-stage bilateral ablations of auditory cortex were compared to unoperated cats on a test involving the discrimination of increases (1.2 kHz) from decreases (0.8 kHz) in the frequency of ongoing 1.O-kHz tone pulses. Whereas two-stage cats exhibited more evidence of postoperative retention for the original task than did one-stage cats, both groups relearned the discrimination in approximately the same number of trials as
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normal cats Individual differences in difficulty of relearning apparently reflected the degree of undercutting of the polysensory association areas of the suprasylvian and lateral gyri. Following retraining, all cats received two discrimination transfer tests. The first test was identical to the original discrimination problem in all respects except that different frequency values were substituted for the original set (Le., 1.6-kHz tones alternating with either 2.0- or 1.2-kHz signals). Whereas both unoperated and two-stage cats had difficulty discriminating the new positive from negative trials, the one-stage cats exhibited a significant tendency to continue responding to changes involving I.2-kHz tones in the same manner as in the original discrimination task. In the second test the cats were asked to discriminate the original 1.2- and 0.8kHz tones against a silent background. Both operated and unoperated cats performed significantly above chance on this test. These results suggest that the cats solved the original discrimination on the basis of absolute frequency cues rather than the directionality of frequency changes. The significance of these findings are discussed in relation to current concepts of the functional capacity of auditory decorticate animals. l
ACKNOWLEDGMENTS This research was supported in part by The Deafness Research Foundation, and
Institute of Neurological PO1 NS 10940.
a grant from by National Diseases and Stroke Grant
REFERENCES W. F. Effect of destroying three 1ocaIized cerebral cortical areas for sound on correct conditioned differential responses of the dog’s foreleg. Am. J. Physiol. 18: 415-428, 1945. 2, AXELROD, S. AND DIAMOND, I. T. Effects of auditory cortex ablation on ability to discriminate between stimuli presented to the two ears. J. Camp. Physiul. Psychol. 59: 79-89, 1965. 3. BROWN, T. S., GODVILAS, G. R., AND MARCO, L. A. Effect of auditory cortical lesions on a test of frequency discrimination in the cat. Proc, Ann, Conv. Am. Psychul. Assoc., 75th, 1967, p. 101-102. 4. BUTLER, R.A., DIAMOND, I.T., ANDNEFF, W, D. Role of auditory cortex in discrimination of changes in frequency. J. iVeurophysio1. 20: 1, ALLEN,
108-120,
7.
8.
9.
10.
1957.
5. DIAMOND, I. T. The sensory neocortex. In: Contributions to Sensory Physiology, edited by W. D. Neff. New York: Academic, 1967, p. 51-100. 6. DIAMOND, I. T. AND NEFF, W. D. Ablation of temporal cortex and discrimination of auditory patterns. J. Neurophysiol. 20: 300-315, 1957.
11. 12.
1. T., GOLDBERG, J. M., AND NEFF, W. D. Tonal discrimination after ablation of auditory cortex. J. Neurophysiol. 25: 223-235, 1962. EBBESSON, S. 0. E. The selective silverimpregnation of degenerating axons and their synaptic endings in nonmammalian species. In: Con temporary Research Methods = Neuroanatomy, edited by W. J. H. Nauta and F 0. E. Ebbesson, New York: Springer, 1970, p. 132-161. ELLIOTT, D, N. AND TRAHIOTIS, C. Corticallesions and auditory discrimination. Psychol. Bull. 77: 198-222, 1972. FINGER, S., WALBRAN, B., AND STEIN, D. G. Brain damage and behavioral recovery: serial lesion phenomena. Bruin Res. 63: I-18, 1973. GOLDBERG, J. M. AND NEFF, W. D. Frequency discrimination after ablation of cortical auditory areas. J. Neurophysiol. 24: 119-128, 1961. HEFFNER, H. E. The Ejfect of Auditory Cortex Ablation on Sound Localization in the Monkey (Macaca mulatta) (Ph.D. dissertation). Tallahassee: Florida State University, 1973. DIAMOND,
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KR~TER, K. D. AN~D ADES, H. W. Studies on the function of higher acoustic nervous centers in the cat. Am. J. Psychol. 56: 501-536, 1943. 14. MASTERTON, R. B. AND DIAMOND, I. T. Effects of auditory cortex ablation on discrimination of small binaural time differences. J. Neu rophysiol.
AND
13.
27: 15-36, MEYER,
127-136, 19.
RANDALL,
with
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1946.
W. L. Generalization to tones in cats central nervous system lesions. In:
Generalization, edited by D. J, Mostofsky Stanford: Stanford Univ. Press, 1965, p. 134-153. RAVIZZA. R. J. AND MASTERTON, R. B. Contribution of neocortex to sound localization in opossum (Didelphis virginiana). J. Neu rophysiStimulus
20.
1964,
R. AND WOOLSEY, C. N. Effects of localized cortical destruction upon auditory discriminative conditioning in cat. J. Neurophysiol. 15: 149-162, 1952. 16. NEFF, W. D. Role of auditory cortex in sound discrimination. In: Neural Mechanisms of’ the Auditovy and Vestibular Systems, edited by G. L. Rasmussen and W. F. Windle. Springfield: Thomas, 1960, p. 211-216. 17. NEFF, W. D. Neural mechanisms of auditory discrimination. In: Savory Communication, edited by W. Rosenblith. New York: Wiley, 1961, p. 259-278. 18. RAAB, D. W. AND ADES, H. W. Cortical and midbrain mediation of a conditioned discrimination of acoustic intensities. Am. J. Psychol. 59: 15.
STRAMLER
01. 35: 344-356, 21.
22.
1972.
D. P., NEFF, W. D., AND N. L. Discrimination of tone duration after bilateral ablation of cortical auditory areas. J. Neurophysiol. 28: 673-681, 1965. THOMPSON, R. F. The effect of training procedure upon auditory frequency discrimination in the cat. J. Crimp. Physiol. Psychol. 52: 186-190, SCHARLOCK, STROMINGER,
1959. 23,
R. F. Function of auditory cortex of cat in frequency discrimination. J, Neurophys-
24.
THOMPSON,
THOMPSON,
iol.
23: 321-334,
stimulus Psycho/. 25.
1960.
R. F. Role of the cerebral cortex in Physiol. generalization. J. Csmp. 55: 279-287, 1962. C. AND ELLIOTT,
D. N. Extension of the Neff neural model to situations demanding discrimination among complex stimuli. J. TRAHIOTIS,
Acoust.
Sot.
Am.
47: 1116-l
127, 1970.
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L. CRANFORD,
MAKOTO
IGARASHI,
AND
Department of Otorhinolaryngology and Communicative Baylor College of Medicine, Houston, Texas 77025 REVIEW (9) Of the experimental literature related to the behavioral effects of auditory cortex lesions concluded that discriminations involving the “recognition” of soundssuffer more than do tasks requiring only the “detection” of new signals. Recognition tasks are ones in which animals are required to discriminate more than one type of change in the auditory environment by responding to certain changes and withholding response to other changes or, alternately, making discriminably different responsesto each of the changes.Detection tasks, in contrast, only require a single responseto a unitary changein the characteristics of the background signals. Although this procedural distinction hasbeen quite successful in accounting for the outcome of numerous ablation studies, a number of experimental exceptions do exist. For example, detection tasks involving changesin either the duration of individual tone pulsesor the temporal patterning of a seriesof tones are severely disrupted by large bilateral ablation of auditory cortex (6, 21). More recently, Brown et al. (3) found that cats with bilateral lesions of auditory cortex could perform a recognition task which involved the discrimination of increasesfrom decreasesin the frequency of ongoing tone pulses.Theselatter investigators, however, reported that several of the lesionswere smaller than intended, thus raising the possibility that the successfui postoperative performance may have been the result of sparingof critical amountsof auditory cortex, In view of the relatively large degree of theoretical importance (11, 16, 17, 23) that has been attached to the distinction between recognition and detection tasks in terms of neocortical function, we felt that further investigation of the role of neocortex in these two forms of discrimination would be worthwhile. One research area which we consideredto be in need of additional investigation concerns the role of neocortex in frequency discrimination. Prior to the report of Brown et al., investigators had conA RECENT
Receivedfor publication
June
27, 1975.
JAMES I-I. STRAMLER Sciences,
eluded that, while auditory decorticate cats could successfully detect changes in the frequency of ongoingtonal signals(4, 11, 23), they could not perform recognition tasks which required the discrimination of tones of different frequency against a silent background (1, 23). The first goal of the experiments to be described in the present report, therefore, was to test the basic Brown et al. experimental design to determine whether, in fact, cats in which all neocortical targets of the medial geniculate nucleus and posterior group of the thalamus are bilaterally ablated can perform a recognition task. A secondobjective was to administer, to any cats which were retrainable postoperatively, a series of special discrimination transfer or stimulus equivalence tests to determine whether operated cats use different cues to solve the basic discrimination problem than do unoperated cats; i.e., whether the cat’s “perception” of auditory frequency is changed in any way by the presenceof the cortical lesion METHODS
Subjects A total of I2 adult cats were tested in the present experiment. The cats were selected on the basisof general health and temperamentas well asthe presenceof clean external ear canals and normal appearing tympanic membranes. Four cats (B-3504, B-3572, B-3577, and B-3984) served as unoperated controls for the present seriesof tests. Of the remaining eight cats, half (B-1349, B-2616, B-2618, and B-2787) were tested before and after one-stage bilateral auditory cortex ablations, whereasthe other four cats (B-1347, B-2303, B-2502, and B-2789) received two-stage ablations with retraining given between the first and second operations. Apparatus All cats were trained with a shock-avoidance procedure in a two-way shuttle box. Auditory stimuli were presented from Lansing LE-85 speakersmounted at the top of the grill box 48 143
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144
CRANFORD,
IGARASHI,
inches directly above the center of the floor of each compartment. The speakers and training apparatus were located inside an IAC model 1202 sound-treated chamber which had a background sound level of approximately 36 dB re 0.0002 dyn/cm 2* The l.O- and 1.GkHz neutral frequencies used in the present experiment were generated by a Hewlett-Packard 200 CD wide-range audio oscillator, whereas the O.8-, 1.2-, and 2.0-kHz comparison signals were generated by a Krohn-Hite 4100 push-button oscillator. The outputs of the nectral and comparison oscillator were switched by a relay into an Iconix model 6837 electronic switch. The risefall time for all tone pulses was 100 ms. The after being fed successively gated tones, through an Iconix model 6836 programmable attenuator and a McIntosh MC-75 amplifier, were sent in a synchronous fashion to the two audio transducers. The relative onset times and signal durations were controlled by an Iconix model 6255 interval timer.
Stimulus presentation and test procedures In the first phase of the experiment nine cats were trained to cross to the opposite compartment of the grill box when an ongoing series of neutral LO-kHz tone pulses were made to alternate with tone pulses of 1.2 kHz. The remaining three cats (B-2787, B-2789, and B-3572) were trained to cross when neutral l.O-kHz tones alternated with O.8-kHz tones. The tone pulses were of 1 s duration with l-s silent intervals between successive pulses. If the cat had not initiated a cross to the opposite compartment by the beginning of the fourth consecutive warning tone (0.8 or 1.2 kHz, respectively), electric shock (paired with a loud buzzer) was intermittently applied to the pads of the cat’s feet through the grid floor of the training apparatus until the cat responded. The intertrial intervals (ITIs) ranged from 30 to 90 s, with a mean of 60 s. In order to prevent cats from using loudness differences as possible cues for responding, the intensity levels of the signals were randomly varied in 4-dB steps over a, 28-dB range. The sound pressure level of the O-8-, 1 .O-, 1.2-, 1.6-, and 2.0-kHz tones used in the present experiment was approximately 70 dB re 0.0002 dyn/cm2 at the midpoint of the 28-dB range of intensities used. The cats were trained 5-6 daysiwk with 12 trials each day until they achieved a minimum criterion of 3 consecutive days of 1 l/ 12 correct. The second phase of the experiment involved further training in which the cats were required to inhibit crosses to a frequency change oppo-
AND
STRAMLER
site in direction to that with which they had been previously trained. Thus, nine of the cats were trained to withhold crosses when the neutral LO-kHz tones alternated with 0.8-kHz tones (“negative trials”) but to continue crossing, as before, in response to changes involving 1.2-kHz tones (“positive trials”). Cats B-2787, B-2789, and B-3572 were trained with the converse condition requiring crosses to 0.8-kHz and noncrosses to 1.2-kHz signals. In order to avoid shock on negative trials, the cats had to inhibit crosses during a minimum of five alternations of the neutral and negative tones. Each cat received six positive and six negative trials each day. The order of daily presentation of the two types of trials was randomized with the restriction that not more than four consecutive trials could be of the same type. All other procedures were the same as described for the first phase of the experiment except that all cats, after they attained the original 3-day learning criterion, were routinely given 4 days of overtraining before proceeding to the next part of the experiment. The third phase of the experiment involved the presentation of a series of retention and discrimination transfer tests. What follows next is a description of these tests in the order of their presentation and the special procedures used to administer them. a )
POSTOPERATIVE
DISCRIMINATION-RETENTION
All bilaterally operated cats received in all respects to 3 days of tests, identical the last three training sessions given prior to the last operation. The score on these tests constituted a measure of retention for the preoperative problem. If the retention score was above chance, the cats were continued with the same procedures in an attempt to retrain to the preoperative criterion. If the score was not above chance, then the cats were retrained on the first phase of the present experiment prior to attempting retraining with the second-phase problem.
TEST.
h)
FREQUENCY-GENERALIZATION
TEST,
This
test involved presenting special sessions in which the ITIs contained tonal pulses of 1.6 kHz frequency rather than 1.0 kHz. Two types of test trials were presented, the first being ones in which the ongoing 1.6-kHz tones alternated with tones of 2.0 kHz, and the second where the 1.6-kHz signals alternated with 1.2-kHz tones. Each cat received four such sessions, each containing 6 positive and 6 negative frequency changes, interspersed over days among regular retraining sessions on the original discrimination. Each cat had to achieve a criterion level of performance on the preceding days regular ses-
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CORTICAL
LESIONS
sion before receiving a stimulus-generalization session. On the generalization trials cats received occasional mild shock for failing to generalize their responses appropriately (i.e., failing to cross to the opposite compartment when the new frequency change was in the same direction as the original positive trials and failing to inhibit crosses when the new change was the same direction as previous negative trials). This was necessitated by the observation that some cats tended to “freeze” rather than cross to the opposite compartment when first presented with a positive trial containing a “novel” frequency value. C) ABSOLUTE-DISCRIMINATION TEST. After the cats were retrained to the original 3-day criterion level on regular sessions involving neutral LO-kHz signals, the LO-kHz tones were eliminated (i.e., the ITIs now contained no tones) and the cats were presented with an absolute discrimination between 1.2- versus 0.8kHz tone pulses. Four consecutive sessions, each containing six positive and six negative trials, were given. As with the generalization test, occasional mild shock was administered for inappropriate responding. In the generalization- and absolute-discrimination tests, all other procedures were the same as in the first two phases of the experiment (i.e., scrambling of tonal intensities, duration and rate of presentation of tone pulses, lengths of positive and negative trials, lengths of ITIs, etc.). d)
FREQUENCY-DISCRIMINATlON
This
THRESHOLD
test involved first retraining the bilaterally operated cats to criterion levels of performance with the original discrimination containing LO-kHz neutral tones and then decreasing the differences between positive and negative frequency values in lo-Hz steps over trials and sessions in an attempt to determine the thresholds for discriminating directional frequency changes. A modified method of limits was used to determine these values. During each session the differences between neutral and positive frequencies were reduced by decreasing (or increasing) the latter signal in lo-Hz steps until the cat failed to cross on a minimum of two of three trials. The differences were then increased in IO-Hz steps until the cat again responded on two or more consecutive trials. Shock was given for all incorrect responses. During each test session the differences between neutral and negative stimuli were also successively decreased and increased in a similar manner. Thus, two independent thresholds were measured, one for positive and one for negative frequency changes. All other procedures were the same as used in the original disTEST.
AND PITCH PERCEPTION
145
crimination training except that scrambling of tonal intensities was eliminated whenever the frequency differences appeared to be in the region of the cat’s threshold. All four of the preceding tests were not given to every cat in the present experiment. The four unoperated control cats received the frequency-generalization and absolute-discrimination tests, but not the retention- or frequencydiscrimination threshold tests. The eight operated cats did receive all four tests, but only after bilateral cortical lesions. Prior to surgery and after unilateral operations, these cats were only trained to criterion with the fist two phases of the present experiment.
Surgical and histological procedures The auditory cortex was removed from the two hemispheres in either one or two stages by subpial aspiration under pentobarbital sodium anesthesia. Strict aseptic precautions were maintained throughout. Animals were allowed a minimum of 14 days of recovery from each operation before testing was resumed. At the end of the experiment, each animal was perfused with normal saline and 10% formalin. Prior to removing the brain, the ears were examined for any signs of abnormality. After a minimum storage period of 30 days in 10% formalin, the brain was embedded in egg yolk (8) and cut on a freezing microtome in the frontal plane at 25 pm. Every ninth section was stained with cresyl violet. The cortical lesions were reconstructed by systematic projection of frontal sections to a standard lateral plane. Retrograde degeneration in the dorsal thalamus was studied and drawn with the aid of a microprojector. RESULTS
Anatomical Figure 1 shows the reconstructed surface lesions in the eight cats translated to standardized lateral views of the cerebral hemisphere. On the basis of surface extent of cortical ablations and severity of retrograde degenerative changes in the dorsal thalamus, the present cases can be divided into three categories according to overa11 lesion size. Cats B-1347 and B-2789 had the largest lesions. In both cases severe degeneration was present bilaterally throughout the rostral-caudal extent of the principal and magnocellular divisions of the medial geniculate nucleus (GM) as well as the posterior group (PO). Extensive undercutting of the suprasylvian and lateral gyri occurred as evidenced by the presence of severe degeneration throughout the entire extent of the lateral geniculate nucleus (GL) as well as the lateral posterior-
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146
CRANFORD,
IGARASHI,
TWO-STAGE
AND
CORTICAL
STRAMLER
ABLATION B-2789
B-2303
B-2502
ONE-STAGE
FIG. 1 . Reconstructed ce re bra1 hemispheres.
cortical
CORTICAL
ABLATION
B-2787
I3- 2616
B- 1349
B-26t8
lesions
in eight operated
pulvinar (LP-PUL) complex. Degeneration was also present more anteriorly in the region of the lateral dorsal nucleus (LD). In B-1347 the degeneration anteriorly in LP and the lateral parts of LD was severe bilaterally, whereas in B-2789 it was, while extensive, more moderate in degree as evidenced by the presence of less severe gliosis plus occasional healthy-appearing cells. In both cases severe degeneration extended bilaterally into the ventrobasal complex, notably the lateral division of the ventroposterior nucleus (VPL). A second group of cats (B-2303, B-2502, B-2787, and B-261 6) also had severe retrograde degeneration present bilaterally throughout the entire extent of the principal and magnocellular divisions of GM. Degeneration in PO was severe bilaterally except, however, for the extreme caudal regions which had occasional
cats translated
to standardized
lateral
views
of the
normal-appearing cells present. Although moderate to severe amounts of degeneration were present throughout most of GL, LP, and PUL bilaterally, very little evidence for degeneration was found in the anterior regions of LP or in LD. Some degeneration was found bilaterally in the lateral aspects of the ventrobasal complex, although it was not as severe or extensive as in B-1347 and B-2789. Thalamic degeneration in the remaining two cats (B-1349 and B-2618) was similar to that of the intermediate group except that normalappearing cells were present bilaterally in the more caudal portions of the principal and magnocellular divisions of GM as well as PO. Also, overall, less severe degeneration was seen in LP, PUL, and GL than in the other cases. To illustrate the range of thalamic degeneration observed in the present cases we have
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CORTICAL
LESIONS
AND PITCH PERCEPTION
147
6-2618
6
5
4
2
3
2. Thalamic degeneration in cats B-2618 and B-1347. Severe degeneration is depicted in solid black and slight degeneration is shown by stippling. Abbreviations are: CL, n. central lateral; CM, n. centromedian; GL, lateral geniculate body; GM, medial geniculate body, principal division; Ha, n. habenular; LD, n. laterodorsal; LP, n. lateroposterior; MC, medial geniculate body, magnocellular division; MD, n. mediodorsal; Pf, n. parafascicular; PO, posterior group; Pul, n. pulvinar; R, n. reticular; TO, optic tract; VGL, ventral lateral geniculate; VL, n. ventrolateral; VM, n. ventromedial; VP, n. ventroposterior; VPL, n, ventroposterior, lateral division; VPM, n. ventroposterior, medial division. FIG.
elected to depict, in Fig. 2, the degenerative tions of the present cases, each required more changes in the smallestlesion case(B-2618j as than twice the number of trials for retraining well as the largest (B-1347). (672 and 612 trials, respectively) than any of the other six operated cats.
Behavioral
1. Mean number of total trials to criterion on Jirst two phases ING. Table 1 summarizesthe number of total of discrimination task trials and mean errors per sessionrequired, be- _ TABLE
PHASE
ONE
AND
TWO
DTSCRIMINAT1ON
TR4IN-
fore and after the different cortical operations, for each of the three groups of cats to complete training with the first two phasesof the present experiment. Before surgery all three groups were reasonably equated in terms of speed of mastery of the basic discrimination task. The unilateral operation produced little disruption of the discrimination, with cats achieving criterion levels of performance in lessthan one-third the number of trials required before surgery. After bilateral lesionsthe two-stage cats, as a group, required more training than did one-stagecats to relearn the discrimination. However, this difference is the result of the fact that cats B-1347 and B-2789, which had the largest cortical abla-
Normal Cats
Beforesurgery
One-Stage Two-Stage Cats Cats
T: 411 T: 417 T: 393 E: 1.31(+) E: 1.78(+) E: OX(+) 0.96( - )
0.51(-)
After unilateral operation
O&6(-)
T: 114 E: 1.24(+)
OSO(--) After bilateral operation
T: 372 E: 1.44(+) 0.31(-)
T: 426 E: 1.89(+) O.%(-)
Also shown are the mean number of errors per session made on positive (+ ) and negative (- ) trials during phase-two training. T: trials; E: errors.
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148
CRANFORD,
IGARASHI,
With respect to the mean number of errors per session on positive and negative trials, 10 of the 12 cats consistently made more errors on positive than on negative trials throughout all phases of testing. However, one unoperated cat (B-3577) had a mean of 1.07 errors on positive and 1.67 errors on negative trials. Prior to the first operation only, cat B-2789 also made more errors on negative than on positive trials (means of 0.69 and 0.46 errors, respectively).
2. Mean individual uver 4 days of testing --
perj’urmances
All 4 days Normal
FREQUENCY-GENERALIZATION TEST. The left part of Table 2 summarizes the findings obtained on the generalization test with each of the three groups of cats. Presented separately are percentages “correct” on positive and negative trials. Positive and negative generalization trials are defined as ones which have frequency changes of the same direction as the trials with which each animal was originally trained. The percentages correct, therefore, reflect the degree to which cats respond in the same manner on the new positive and negative trials as they did on the original trials. All 12 cats performed significantly worse on generalization sessions than on the original discrimination (nonoverlapping distributions). Of the four unoperated cats, only two (B-3572 and B-3984) demonstrated above chance levels of performance, B-3577 and B-3504 both performed at chance levels. The former cat exhibited a high (and equal) probability of crossing on both positive and negative trials, whereas the latter cat, while crossing on fewer overall trials, was equally deficient at performing the transfer task. By comparison, three of the four two-stage cats demonstrated above chance levels of performance on the generalization test. Only cat B-1347 seemed unable to discriminate the new frequency changes, making as many crosses on negative as on positive trials.
Two-stage
trials
Absolute Test
Pos and neg, day 1 vs. day 4
Avg
B-3572 B-3577 B-3504 B-3984
50 80 49 63 61
97 20 54 87 65
74 50 52 75 63
50 58 33 50 48
vs. vs. vs. vs. vs.
B-1347 B-2303 B-,3502 B-2789
44 53 63 65 56
56 73 84 94 77
50 63 74 80 67
67 47 75 83 68
B-I349 B-2787 B-2616 B-2618
17 42 31 32 31
58 42 52 23 44
38 42 42 28 38
25 25 42 17 27
Aw
and negative
Test
Neg
A%
One-stage
on positive
Pos
A&
and 56
-Generalization
Cats
STRAMLER
B-2789, 26 and 96% correct for B-2303, and 100% correct for B-2502.
RETENTION TEST. The degree of retention exhibited by each of the eight cats after the bilateral lesion appears closely related to both the extent and severity of degenerative changes found in the dorsal thalamus as well as the type of surgical procedure received. Thus, the only one-stage cat which exhibited any signs of postoperative retention was B-2618, the cat with the smallest bilateral lesion. B-2618’s score over the 3 days of retention testing was 44% correct on positive trials and 100% correct on negative trials. (All scores reported on this and subsequent tests have been corrected for each cat’s rate of spontaneous crosses during ITIs according to the method described by Masterton and Diamond (14); individual rates of spontaneous activity in the present experiment were 10% or less.) The only two-stage cat which failed to show signs of postoperative retention was B-1347, the cat with the largest lesion. The retention scores for the remaining two-stage cats on positive and negative trials, were 15 and 96% correct for respectively,
TABLE
AND
AI1 4 days
Pos and neg, day. 1 vs. day 4
Pos
Neg
Avg
83 50 67 75 69
87 82 76 80 82
100 97 72 100 93
94 90 74 90 88
92 83 84 75 84
vs. 100 vs. 92 vs, 57 vs. 92 vs. 85
vs. vs. vs. vs. vs.
50 75 50 59 59
79 96 90 63 82
67 100 100 79 87
73 98 95 71 85
42 100 92 83 79
vs. 83 vs. 92 vs. 100 vs. 58 vs. 83
vs. vs. vs. vs. vs.
50 42 34 16 36
88 94 78 88 87
100 100 94 100 99
94 97 86 94 93
92 100 84 100 94
vs. 92 vs. 100 vs. 92 vs. 92 vs. 94
Values are percentages.
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CORTICAL
LESIONS
AND PITCH PERCEPTION
Relative to the findings with the unoperated and two-stage cats, those obtained with the one-stage animals were unexpected. All four of these cats made significantly (f = 2.506, df = 3, P < 0.05) more crosses on negative than on positive trials. Note that cat B-2787, which had been originally trained to cross to 0.8-kHz and inhibit crosses to 1.2-k& signals, also crossed less (inhibition?) on positive than on negative trials
TABLE 3. Smallest positive and negative frequency changes (in steps of IO Hz) which could be correctly discriminated on a minimum uf 5 of 10 trials
FREQUENCY-DISCRIMINATION TEST. Table 3 summarizes
THRESHOLD
for each of the eight bilaterally operated cats the smallest frequency differences which could be correctly discriminated at least 50% of the time. Each score represents the cat’s average performance on a minimum of 10 separate trials. Again, overall size of the cortical lesions appears to be a critical variable in determining the test results. Efforts to test the two cats with the largest bilateral lesions, B-1347 and B-2789, on this part of the experiment were unsuccessful. In response to attempts to reduce differences in positive and negative frequency values, these two cats quickly developed and maintained a pattern of either crossing to both types of frequency change or not responding to either. In contrast, the two cats with the smallest overall lesions, B-1349 and B-2618, demonstrated a discrimination threshold which appeared to be close to 10 Hz. When tones of 1,010 Hz were made to alternate with the neutral 1,000 Hz signals, both cats responded well above chance. However, when signals of 990 Hz were presented, the cats did not cross to the opposite compartment. This latter observation suggests that the 10 Hz-threshold involves being able to
- Positive Hz %
Operated Cats One-stage
B-1349 B-261 6 B-2618 B-2787
Two-stage
B-1347 B-2303 B-2502 B-2789
l
ABSOLUTE-DISCRIMINATION TEST. The right half of Table 2 summarizes the results obtained during the 4 days of absolute-discrimination testing. With the exception of cat B-2789, all animals performed significantly (t = 7.03, df = 11, P < 0.01) better on the absolute tests than they did on the generalization tests. Differences between the three groups of cats were small, although the mean score for the onestage cats was slightly higher than that of the other two groups. In order to determine the extent to which learning occurred over the 4 days of generalization and absolute testing, individual performances on the first and fourth test sessions were compared (Table 2). Although some cats in all three groups exhibited evidence of improvement over days of testing, only with the unoperated cats on the generalization test did this involve a majority (three of four cats) of the respective members.
149
1,010 1,020 1,010 980
84 50 91 73
Not testable 1,020 1,020
100 61
Not testable
Negative Hz % 990 980 990 1,060
83 64 80 62
Not testable 990 100 990 100 Not testable
recognize the nature of the frequency changes rather than simply detecting that a change has occurred.
The primary question of the present investigation of whether cats which have auditory cortical subdivisions AI, AII, Ep, I-T, and SII bilaterally ablated can discriminate increases from decreases in the frequency of ongoing tonal signals was answered in the affirmative. All eight operated cats were able to relearn the basic discrimination. The secondary question of whether cats with bilateral auditory cortex ablations use different cues than unoperated cats in solving the present type of discrimination problem was relatively easy to answer but difficult to interpret. This resulted from a dramatic difference in the performance of the one- and two-stage operated cats on the frequency generalization test. The fact that both unoperated and operated cats performed significantly better on the absolutediscrimination test than on the generalization test suggests that the animals solved the original problem more on the basis of the absolute frequency values of positive and negative tones than the directionality of the frequency changes. If one only compares the performance of the unoperated and two-stage cats, then the conclusion that operated and unoperated cats solve the discrimination problem in the same manner seems justified. However, the performance of the one-stage cats on the frequencygeneralization test appears qualitatively different from that of the other two groups. Rather than simply failing to correctly discriminate new positive from negative frequency changes, all four of these cats exhibited a marked tendency to continue responding on trials containing 1.2-kHz tones in the same manner as they
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had responded in original training. This suggeststhe paradoxical hypothesis that onestage operated cats are even more likely than either unoperated or two-stage operated cats to solve the present type of discrimination problem on the basis of absolute frequency cues. Although not intended as an explanation, one way to account for the present difference in the findings with one- and two-stage surgical procedures centers on the relationship between neural plasticity and a phenomenon known as the “serial lesion effect” (10). Clinical and experimental evidence is available (ref 10contains
a comprehensive review of this literature) which indicates that considerable sparing of function may occur in the nervous systemif the target region is ablated serially with time allowed for recovery between successiveoperations. A similar effect appearsto have occurred in the present investigation. The performance of the cats which received successiveunilateral operations with retraining given between operations did not differ from that of unoperated cats. The performance of the one-stage cats suggestsa functional deficit which may consist of either decreasedbehavioral flexibility (i.e., inability to perform successfully in situations which require both relative and absolute discriminations) or, alternately, a primary sensory deficit somehow involving stimulus generalization (5, 19, 24). The findings of the present investigation are of considerable significance in relation to two formal hypotheses regarding the functional capacities of auditory decorticate cats. Thompson (23), on the basis of published experiments (1, 23) which obtained evidence that cats (and dogs) with large bilateral auditory cortex lesions could not be trained to perform auditory tasks that required an absolute discrimination against a silent background, developed the hypothesis that the primary effects of auditory cortex ablations are to disrupt an animal’sability to inhibit responsesto “no-go” stimuli. The fact that all eight operated cats in the present experiment retained this latter behavioral capacity provides further evidence against Thompson’s hypothesis (2, 3, 12, 20). Neff (11, 16, 17), in reviewing the differences between auditory discriminations which can or cannot be acquired by cats with bilateral ablations of auditory cortex, developed a neural model from which a number of predictions concerning the auditory capacitiesof cortically ablated animals can be derived. Neff noted that auditory discriminations which had been previously found to survive cortical ablations have two features in common. The first is that the animal is required to detect a change in an on-
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going auditory signal and the secondis that the change always involves either the introduction of a new frequency or an increase in the intensity of the ongoing signal (4, 11, 13, 18, 23). According to Neff, these two features are accompanied by two significant neural events which provide a basisfor solution. First, neural habituation occurs to the continuous presentation of the ongoing neutral signal and, second, the change in frequency or increasein intensity activates previously unactivated neural units. Changesin frequency are assumedto trigger a different group of units, whereas increasesin intensity evoke additional units over and above those already firing. Combined with the prior habituation to the ongoing signal, both of these changeseffectively result in an increase in the total amount of evoked neural activity. The animal’s task becomessimply one of detecting this increasedactivity and attaching appropriate behavioral responses. Changes in duration or pattern, on the other hand, involve temporal rearrangement of stimuli which are already present in the ongoing neutral signals and do not stimulatenew units to fire. Accordingly, animals with large bilateral auditory cortex lesions almost invariably fail on the latter type of discrimination task (6, 7, 21). Thus, Neff s model contains two basic propositions, one related to neural habituation and one to excitation of new neural units. The present finding that cats with complete bilateral removal of the neocortical targets of GM and PO can perform absolutefrequency discriminations againsta silent background would seemto question the universality of the first proposition, However, the relative validity of the second proposition is somewhat more difficult to determine. In postulating that a “larger neural event” is the basis on which auditory decorticate cats perform auditory discriminations, Neff did not specify whether the event was a simple “dimensionless” changeor whether discriminably different events might be correlated with certain stimulus parameters such as frequency. The results of the present experiment suggestthe latter alternative, In order to perform the present type of discrimination, cats have to make a differential responseto two different frequency changes.A successfulsolution requires recognition rather than a simple detection of increased neural activity. The results of the present investigation are, therefore, at variance with current concepts of the effects of auditory neocortex ablations in normal hearing processes.They also bring into sharpfocus the profound effect that differences in experimental procedure have on the outcome of different investigations. Whereas Thompson
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CORTICAL
LESIONS
(22, 23) had great difficulty training even unoperated cats to perform absolute discriminations, the procedures used in the present project appear to have facilitated equally quick solutions to this type of problem by both operated and unoperated cats. This suggests that the degree of difficulty previously assumed to be inherent in absolute discriminations may be more related to the method of training used than to any underlying sensory or learning factors (12). Although procedural variations have often been alluded to as possible underlying causes for apparent discrepancies in the results of different investigations, such variations, with few exceptions (12, 20, 22, 23, 25), have not been included as significant features of experimental designs in auditory research. It would seem that the inclusion of such procedural variables as specific independent measures in future experimental designs would provide valuable new insights into the neural mechanisms of normal hearing. SUMMARY
Cats which received one- or two-stage bilateral ablations of auditory cortex were compared to unoperated cats on a test involving the discrimination of increases (1.2 kHz) from decreases (0.8 kHz) in the frequency of ongoing 1.O-kHz tone pulses. Whereas two-stage cats exhibited more evidence of postoperative retention for the original task than did one-stage cats, both groups relearned the discrimination in approximately the same number of trials as
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normal cats Individual differences in difficulty of relearning apparently reflected the degree of undercutting of the polysensory association areas of the suprasylvian and lateral gyri. Following retraining, all cats received two discrimination transfer tests. The first test was identical to the original discrimination problem in all respects except that different frequency values were substituted for the original set (Le., 1.6-kHz tones alternating with either 2.0- or 1.2-kHz signals). Whereas both unoperated and two-stage cats had difficulty discriminating the new positive from negative trials, the one-stage cats exhibited a significant tendency to continue responding to changes involving I.2-kHz tones in the same manner as in the original discrimination task. In the second test the cats were asked to discriminate the original 1.2- and 0.8kHz tones against a silent background. Both operated and unoperated cats performed significantly above chance on this test. These results suggest that the cats solved the original discrimination on the basis of absolute frequency cues rather than the directionality of frequency changes. The significance of these findings are discussed in relation to current concepts of the functional capacity of auditory decorticate animals. l
ACKNOWLEDGMENTS This research was supported in part by The Deafness Research Foundation, and
Institute of Neurological PO1 NS 10940.
a grant from by National Diseases and Stroke Grant
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