Discrimination of intermittent noise by macaques following lesions of the temporal lobe

EXPERIMENTAL

NEUROLOGY

Discrimination following

16, 201-214

(1966)

of intermittent Lesions of the DAVID

Department

of Physiology,

Yale University Received

Noise by Temporal

Macaques Lobe

SYMMES’ School June

of Medicine,

*Vew Haven,

Connecticut

1, 1966

The effects of cortical ablations in the temporal lobe of monkeys were assessed on a test involving discrimination of intermittent from steady white noise and on several control tests. Lesions which removed inferotemporal areas produced no losses, whereas ablation of primary auditory cortex produced severe and lasting impairment. The lesions had to be complete within the auditory “focal zone” for permanent losses to occur. Cell counts in the medial geniculate bodies confirmed the known projection of the auditory pathway in monkey, but correlated only in a general way with the severity of behavioral impairment. Introduction

The nature and severity of behavioral impairments following lesions of the auditory cortex of primates are largely unknown. The relatively few reports which have attempted to characterize the changes in auditory function in monkeys with such lesions have often been brief, lacking anatomical documentation, and with little or no control data to support the conclusion that the deficits seen were in fact primarily of an auditory nature (reviews: 1, 19). Only the studies by Evarts (7) include adequate histological material and lead to the conclusion that large frequency differences can be discriminated by monkeys with complete or nearly complete removal of the primary auditory area. A more recent study using differential conditioned avoidance techniques (10) found essentially similar results, but severe impairments were reported for more difficult tonal discriminations after apparently large lesions. The matter of anatomical verification of lesions, always important, assumes a particularly crucial role in investigation of auditory cortex in primates. Lesions which appear extensive on surface drawings may miss more than 5~07~of the auditory focal zone,‘) which of course lies entirely 1 This research has been supported by National Institutes of Health grant NB-02681. The collaboration of J. G. Wegener in early phases of the study, and the consultation of Jerome Sutin on the histological aspects, are gratefully acknowledged. 2 The term auditory “focal zone” will be used throughout to indicate the projection field of the anterior parvocellular medial geniculate. The term apparently originated with Polyak (12, p. 59) and has been extended and related to later findings by Wegener (19). 201

LUL

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within the Sylvian fissure. More important, the auditory cortex of primates appears to be organized differently from that in carnivores in several respects, and past attempts at defining its functional limits have raised important questions about the relationships between the three sources of data available for such definitions-anatomical, electrophysiological, and behavioral. The cortical areas surrounding the focal zone from which evoked responses to auditory stimuli have been recorded in monkeys include insula, superior temporal gyrus, and parietal operculum ( 13). Ablation of these areas in addition to the focal zone was reported by Wegener (lo) not to increase severity of deficits beyond that seen after smaller lesions intended to remove the focal zone only. In cat, it is usually necessary to remove all cortical areas responsive to click stimulation for lasting impairment of auditory function to occur ( 11). The apparent inconsistency of these findings may be due to the specific tasks or training procedures, or to a change in the significance of evoked potential data in brains with much greater ratios of association to koniocortex. An important first step in understanding the functional contribution of auditory cortex, both primary and “fringe,” to hearing capacity in primates is the identification of auditory tasks which cannot be performed by animals in which these regions have been selectively destroyed. If severe and lasting impairment in auditory function follows ablations restricted to part of the evoked potential field (the anatomically defined part), with no additional impairment when the remainder is also ablated, new insights into the significance of the ever-expanding electrophysiological maps of sensory cortex would be obtained. The present experiment was designed to find out whether such severe and lasting impairments can be demonstrated in monkeys. The evidence available suggests that cortically-ablated monkeys, like cats, do not permanently fail discriminations which are based on large differences in the frequency of pure tone stimuli unless the test conditions are made extremely difficult. Tasks requiring discriminations of temporal and spatial cues, however, reveal reliable impairments in cats over lengthy postoperative training periods (11). Discrimination of intermittence in a chopped noise signal is a task which explicitly depends on temporal cues, and permits, as well, rather direct comparison with other modalities, since many forms of sensory input may be presented intermittently. Comparisons have been made in man between responses to intermittent noise and to visual flicker, and some of the factors which enhance or disrupt the capacity to detect intermittence are common to both modalities (6). The evidence from neurophysiological studies in animals clearly indicates that the periodicity aspect of intermittent noise is detectable in evoked cortical activity at high chopping rates (8)) and that the auditory system analyzes such signals as though they did not contain enhanced frequency bands corresponding to the chopping rate (14).

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Methods Thirteen monkeys were trained, operated, and retested on a discrimination test based on chopped white noise. They were from a group of twenty-nine trained by essentially similar methods, of which seven failed to reach the criterion set for accurate discrimination, and nine were used in other experiments or died before completing the planned experimental program. Reference will be made to the performance of the larger group in discussion of the results and will be more completely described elsewhere. The thirteen animals comprising the primary experimental group in this report included three Macaca speciosa and ten Macaca mulatta, weighing between 2.5 and 4.0 kg at operation. Three animals had earlier received extensive training on a visual flicker discrimination, and the rest were experimentally naive. The general plan of the experiment involved (i) training on the basic chopped noise discrimination, (ii) testing the discrimination at higher (more difficult) rates of interruption, (iii) training on one of several control tests, (iv) testing both learned tasks for preoperative retention, (v) surgery, (vi) initial postoperative testing on the basic chopped noise discrimination and control tests, (vii) further testing for 500 trials on the basic chopped noise discrimination, (viii) reconstruction of cortical lesions and examination in detail of retrograde degeneration in the posterior thalamus. Procedural details will be described under the above headings. Basic Chopped Noise Discrimination. The stimuli used consisted of speech band white noise presented via a high fidelity speaker mounted in the wall of a test box 70 X 70 X 70 cm located in a sound isolated test room. The intensity of the stimuli was about 80 db (ref. 0.0002 dynes/cm”) as determined by placing a sound level meter in the box at the point in front of the speaker usually occupied by a monkey. Background noise fluctuated between 45 and 60 db, concentrated at frequencies below 200 cycle/set. The intermittent stimulus was produced by passing noise through an electronic gate modulated 10 times per second (ips) with a duty cycle of 0.80. The steady noise stimulus consisted of noise passed through the same gate and interrupted at 300 ips, a rate which was indistinguishable from continuous noise for human observers at the specified conditions of loudnessand soundtime fraction (16). Half the animals were trained to pressa 76-mm diameter panel just below the speaker within 5 set on intermittent noise presentations, and not to press the panel for 5 set on steady noise presentations. The other half of the group was trained on the reverse contingencies. All correct responseswere rewarded by automatic delivery of a Ciba banana-flavored food pellet (symmetrical reward go no-go procedure), and all incorrect responseswere followed by repeating the missedtrial until the correct responsewas made. Forty trials a day were run plus as many correction trials as were needed.

204

SYMMES

Trials were balanced in order and separated by unpredictable intervals averaging fifteen seconds. Training was continued until 90 correct responses were obtained in a consecutive block of 100, and the number of trials up to the beginning of that block was recorded as the learning score. Testing at Higher Chopping Rates. All animals were given blocks of trials at higher rates of chopping according to a simplified method of ascending limits. Performance of SOY0 correct was required at each level of difficulty before presenting the next, and animals were given as many as 100 trials per session. Although some animals were tested quite extensively in this phase of the study, no systematic attempt to obtain stable thresholds was made. It is known that extended testing is required to achieve such stability ( 17). The primary purpose rather was to verify that rate of intermittence was the cue being discriminated. Control Tests. A discrimination of flickering from steady light was taught prior to auditory training in three animals and following it in three others.3 The methods have been described elsewhere (17). This group of six comprised a visual retention control group when tested postoperatively. Two different animals were trained on a “tone vs noise” discrimination preoperatively just after reaching criterion on the intermittent noise problem. The negative stimulus in the go no-go procedure was a 1000 cycle/set tone, and the positive or approach stimulus was the same as that which the animals had been trained to approach earlier (a procedure which greatly favored learning of the new discrimination). The tone vs noise problem was included to provide an auditory retention control of a strict sort since it is a difficult auditory task not dependent on periodicity cues. Preoperative Retention. All animals were retested for retention of both the basic intermittent noise discrimination and control tests after a 3-week rest period. Criteria and scoring were as for initial learning, and the degree of retention expressed by the conventional savings score. Surgery. Under surgical anesthesia, bilateral one stage aseptic ablations of focal zone auditory cortex were made in eight animals, and in two others the ablation was enlarged to include the entire supratemporal plane. Three animals were subjected to bilateral one-stage ablations of inferotemporal cortex, forming an operated control group. Postoperative Testing. All animals were retested on the basic noise discrimination beginning 3-4 weeks after surgery. After reaching criterion, or after training for original trials plus 100, the visual retention control group was retested on the flicker discrimination. The auditory retention control group (tone vs noise) was tested on alternate days from the beginning of 3 Learning on the second task was not faster than subgroup. These observations confirm those of Burton intermodal transfer in monkeys (4).

that for naive and Ettlinger

animals for either on the absence of

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postoperative training, and when the two animals reached criterion on it the basic noise discrimination was continued in daily sessions until criterion was finally reached, (Ag) or until original trials plus 600 had been run (A,). A third control group was made up of two animals which demonstrated severe auditory impairments. These two were taught the visual flicker discrimination postoperatively to form a visual learning control group. Second Postoperative Session. The animals which had failed to reach criterion during the first postoperative session were again placed on the basic intermittent noise discrimination and run for an additional 500 trials. The performance level during this period was taken as a measure of the permanence and severity of losses in capacity to discriminate. Anatomical Reconstructions and Cell Count. After survival times of from 60 to 220 days all animals were killed and the brains prepared for celloidin imbedding. Sections of 50-p thickness were cut and every tenth stained with cresylech violet under regulated pH. Reconstruction of the cortical lesions were prepared using every fortieth section. Retrograde changes in the medial geniculate nucleus were evaluated as follows. Four sections were selected for each hemisphere to correspond as closely as possible to the plates A 4.5, A 3.5, A 2.5 and A 1.5 of the Snider and Lee atlas (15). Cells were counted under 562 >( magnification in square sample areas 0.05 mm on a side. For each section eight such samples were taken extending in a systematic way over the extent of the parvocellular sample counts were portion of the medial geniculate nucleus. Thirty-two thus obtained for each hemisphere. From these data the number of neurons in a cube 0.05 mm on a side was calculated. Neurons were counted on the basis of having visible nucleoli, and half the cases with nucleoli lying on a boundary were excluded. Glial nuclei were not counted, and were not densely stained in most cases due to the staining methods. A similar counting procedure was used to obtain a normal cell count in six hemispheres from unilaterally operated and unoperated monkeys. Behavioral

Results

The rate of acquisition of the basic intermittent noise discrimination is given by the mean learning score of 1721 trials (range 670-3240) for the thirteen animals in the present experiment. This compares with a median score of 1980 for the larger group of twenty-nine, including seven animals which failed to reach criterion over extended training and were dropped from the study. The introduction of mild foot-shock to reduce over-responding shortened the learning time to less than half these values in another experiment. All animals immediately generalized the discrimination learned at 10 ips to higher rates, and many demonstrated good discrimination at rates between 50 and 80 ips. Several human observers tested under as

206

SYMMES

nearly as possible identical free field conditions discriminated at better than chance levels when chopping rate was 100 ips. The conclusion is therefore suggestedfrom very limited data that human listeners are superior in this task to monkeys. However, it is probable that prolonged testing would reveal improving sensitivity in the monkeys. In the present experiment the purpose of including testing at higher chopping rates was to verify the absenceof extraneous cues in the test situation. This purpose was fulfilled since discrimination performance deteriorated to chance levels as rate increased in all animals.

A5 A6 A7 A Al

FIG. 1. Savings IT = inferotemporal

A3 A2 A9

scores on chopped noise ablation; A = auditory

u

discrimination in thirteen cortex ablation.

operated

monkeys.

Retention of the basic discrimination (which was of course strengthened by the training at higher rates which followed) was measured at the end of a 3-week rest period and found to be excellent. The lined area in Fig. 1 indicates the entire range of savings scoresobtained in unoperated animals, arrived at by dividing the difference between initial and retention scores by their sum. Retention following surgery is also shown in Fig. 1 and grossly reveals the profound impairment observed in the animals with larger auditory cortex lesions and the absence of any impairment in the three operated control animals with inferotemporal removals. The latter finding confirms the report of Weiskrantz and Mishkin (21). A more detailed presentation of the results of the auditory cortex seriesis given in Table 1, in which the animals were ranked from top to bottom by increasing severity of deficit.

loss loss

Behavioral change

ANATOMICAL

DATA

loss

capacity

operculum;

loss loss

capacity capacity

ON

ORDER

ANIMALS

not applic.

62%

= superior

63

78%

; STG

52% 77

77 77

78%

temporal

SO%

67%

94%

86%

82%

74%

82%

?

76

48 65

765%

Over-responding Pre Post

75

69% 61%

1 AIMED

gyrus

SEVERITY

TABLE LESIONS

OF INCREASING

WITH

> 90% 90%

> 90% > 90% > 90%

Final performance

TEN

PS = prestriate

retention loss severe retention loss (failed first postop session) severe retention loss (was improving) capacity loss

no loss retention retention

AND

0 PO = Parietal

Al0

A6

A5

A?

A0 A,

A2

Al A.3

BEHAVIORAL

AT

AUDITORY

Focal zone sparing

CORTEX,

RANKED

sparing

on R

; I = insula;

ASP = anterior

minimal complete lesion complete lesion ASP also removed minor medial sparing on L ASP also removed

minor

90% spared ext. medial sparing on R Post. medial sparing on both sides Post. medial sparing on R Post. medial sparing on both sides minor medial sparing on L

OF DEFICIT

TOP

TO

supratemporal

STG

both

plane.

sides

extensive STG sides both sides, I on R PO, I on L on L

very both STG minor minor STG

sides

little both

very STG

on

damagea

BOTTOM

PO, PS both sides very little massive PO, STG,

Unintentional

FROM

R

IN

208

SYMMES

The four most impaired animals achieved scores in the final 500 trial block which did not differ from chance. (The empirically determined chance score was found to have an average value of 57% in these and other animals.) These monkeys had received a total number of trials following surgery equal to their initial learning score plus 600. Absence of discrimination during this period of training is interpreted as a permanent loss of the capacity to discriminate intermittent from steady noise. There is little support in the present data for the belief that. a major factor in the observed impairments is a reduced ability to inhibit response to the negative stimulus in the go no-go situation. While most animals PERFORMANCE

Visual

A10 A4 A8 A2 A3 a F = fail;

TABLE 2 ON CONTROL TESTS FOLLOWING AUDITORY ALL SCORES ARE TRIALS TO CRITERION”

retention VR

CN

200 80 80 40 40

F F 1040 880 720

CN = chopped

Visual

A5 A6

noise

learning VL

CN

580 1240

F F

CORTEX

ABLATION.

Control auditory retention

A7 A9

CAR

CN

440 280

F 2050

discrimination.

increased the proportion of commission errors in their total errors (column headed “over-responding” in Table 1) there is no correlation between the severity of deficit and increase in this “disinhibition.” In fact one of the most severely impaired animals (A,) was trained not on the go no-go methods used for most subjects, but on a procedure requiring positional responses to two levers. Correct performance on positional problems does not depend on inhibiting a response to one class of stimuli, and yet A4 never regained any sign of discrimination capacity. Results of the control testing are shown in Table 2. Retention of the visual flicker discrimination was entirely unimpaired in animals with severe auditory losses, and the same is true of new visual learning. These findings provide clear evidence that the capacity for learning and performing difficult discriminations was not generally impaired in the present animals. A more significant finding is that performance on an auditory task involving stimuli which differ in frequency components rather than periodicity was unimpaired. The retention scores shown for the tone vs noise task are not greater than preoperative retention scores in the same and other animals. Successful performance on tone vs noise coupled with severely impaired probably cannot be performance on intermittent noise discriminations

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attributed to greater difficulty of the latter, although direct evidence is lacking in the present experiment. Two recent studies have reported that learning of an identical tone vs noise discrimination requires about as many trials as the intermittent noise discrimination used here (3, 9). Emphatically, none of the animals in this study displayed any abnormality of response to common auditory stimuli presented informally in the home cages beyond the first postoperative week. Both detection and response to other monkey vocalizations, for example, appeared entirely normal after this initial period. Anatomical

Results

A close correlation exists between the behavioral impairments seen and the extent of auditory focal-zone damage in the present series. Unfortunately, clean ablation of just the desired area sparing surrounding tissue is virtually impossible, and the ideal ablation was approximated in only one animal (AZ). In two animals, as mentioned above, a larger lesion was deliberately made, including most of the supratemporal plane rostrally to the temporal tip. Those portions of the focal zone spared are briefly indicated in Table 1, together with short descriptions of the principal cortical areas damaged outside of the focal zone. The data all point to the necessary and sufficient character of the auditory focal zone as neural substrate for the capacity to discriminate intermittent from steady noise. It is not completely clear from the present data, however, that substantial damage to surrounding areas of the electrophysiologically defined auditory cortex contributes nothing to the postoperative picture, as reported by 1Vegener (19). Both animals A7 and As had substantial bilateral damage to the lateral aspect of the superior temporal gyrus. These animals were the most severely impaired of the group which demonstrated any postoperative capacity for the discrimination tested, a correlation which appears to favor the view that the lateral temporal region contributes to auditory function. However, such an interpretation rests on the assumption (or, if possible, demonstration) that equal damage was done to the focal zone in Ar and A, on one hand and in less severely impaired animals on the other. It is not possible to establish this point beyond doubt from the present data, although some inferences may be made. Animal As had a greater degree of focal zone sparing than A+ for example, but much more damage outside of the focal zone. Greater impairment in Ax then could be attributed to the peripheral damage. However, the medial geniculate of A8 contained more healthy cells, particularly in anterior sections, than AZ, suggesting that the superior temporal gyrus does not have a sustaining projection from medial geniculate and that cell density in thalamus is not an unfailing correlate of behavioral status. The anatomical

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SYMMES

data from A7 do not contribute to this argument substantively because the amount of focal zone sparing was slight and unilateral. A more detailed presentation of selected anatomical findings is given in Figs. 2 and 3. Three brains from the auditory cortex series were chosen

FIG. cortex

2. Reconstruction series. See text.

of

cortical

lesions

in

three

selected

animals

from

auditory

to illustrate the more significant points, and because the lesions are among the most symmetrical. Reconstructions of the cortical lesions and cell counts at four levels in the parvocellular medial geniculate body are presented for: As, the largest lesion in the group able to attain postoperative criterion; AB, the smallest lesion in the group with permanent capacity loss; AG,

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the largest lesion in the study, which is included primarily for anatomical interest since the behavioral deficit could not have been increased over that seen in A4 and As. The cortical reconstructions shown in Fig. 2 are based on sections 2 mm apart. Particular emphasis was placed on displaying the more rostra1 areas of damage; all three lesions extended very slightly farther than the most caudal section shown. The cell densities shown in Fig. 3 are the combined averages for both hemispheres, and normal values (mean and range) from six control hemispheres are also plotted. The upper horizontal

4x10*

. +4.5

+3.5 STEREOTAXIC

FIG. 3. Fig. 2.

Cell

densities

in medial

geniculate

. t1.5

+25 PLANE

bodies

of animals

with

lesions

shown

in

line indicates the average density in the parvocellular medial geniculate found by Chow in four normal hemispheres without a breakdown on the rostrocaudal axis (5). The lower horizontal line indicates the cell density which could not be distinguished from zero by the present sampling methods. It is clear that ablation of auditory focal zone alone (A,) produces retrograde degeneration throughout the parvo-cellular medial geniculate nucleus, but that substantial sparing of neurons occurs in the more posterior sections. Additional removal of the anterior supratemporal plane results in almost total degeneration of the nucleus (A6 and Alo, the latter not shown, had identical cell counts). Since isolated ablations of anterior supratemporal plane were not made in this series it is not possible to tell whether the projection of the posterior pole of parvocellular medial geniculate is sustaining or essential. These results are in agreement with those of others, however,

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SYMMES

which have led to the conclusion that the projection is an essential one (2, 18). The cell densities in Aa are clearly greater than in any of the four most severely impaired animals, but significantly so only in the most anterior section. Unfortunately, the conclusion that the critical neural subzone is the cortical projection of the most anterior one fourth of the medial geniculate is not supported by evidence from other animals in the series; A7 and Aa both had nearly complete cell loss in this region yet were capable of relearning the discrimination (A7 with great difficulty). Correlation of extent of focal zone sparing with test performance is made much more difficult when the sparing is not symmetrical in the hemispheres, as was the case in the four least impaired animals. Anatomically, the data support earlier descriptions of the projection of the medial geniculate body; behaviorally, the correlation between cell density in thalamus and performance is only a general one. Discussion

Proving the presence of capacity for auditory discrimination in monkeys is difficult in some cases, proving the absence of it is impossible. The former point, that for some reason auditory problems are particularly difficult for monkeys as compared, for example, to cats, has been discussed recently by Wegener (20) and is borne out in the present findings. The possibility is raised by the lengthy training required for such learning that auditory cues lack strong arousal value for monkeys, and that deficits obtained following ablations are primarily the result of nonspecific interference with the capacity to detect and respond to weak or indistinct sensory events. It is for this reason that extensive behavioral controls were included in the present study, and the complete absence of deficits on the tasks sampled certainly makes an interpretation along these lines unlikely. The use of a counter-shock procedure to punish errors of commission both by loss of food reward and by painful stimuli to the feet greatly improves the initial learning rate on a chopped noise discrimination but has little effect on predicted deficits following auditory cortex removal .4 The deleterious effect of repeated footshock in long postoperative training precludes a definitive test of the question as to whether permanent losses still follow focal zone removal when the arousal value of the cues has been enhanced, presumably, by fear of painful shock and the learning period shortened to roughly that needed for similar visual problems. The second point made at the outset of this section concerns the impossibility of proving the absence of sensory capacity. The degree to which a deficit may be regarded as permanent depends obviously on the duration and thoroughness of postoperative assessment. The former factor must be weighed 4 Unpublished

observations.

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against the desire for histological verification of the lesion and other factors. In the present study the animals showing the major deficits were tested for at least 2000 trials postoperatively and in several cases considerably more. Their performance did not improve during this period, and none showed even temporary periods of consistent discrimination. The term capacity loss seems therefore justified despite the logical impossibility of establishing the negative case. Even if the evidence for permanent loss is considered to be not strong enough, the great impairments seen lead to two conclusions about auditory cortex in monkey. First, the definition of auditory cortex which correlates most closely with function is anatomical-the projection field of the anterior portions of the principal division of the medial geniculate body. Severe and lasting impairments in auditory capacity have been shown to exist in animals with no damage to large areas of cortex activated by click stimuli. These data, together with the findings of Pribram, Rosner and Rosenblith (13) suggest that the larger evoked potential fields are supplied either by intracortical connections or by collaterals from the primary projection of such small diameter as to fall short of sustaining the parent neurons. According to Pribram et al., evoked responses cannot be obtained from these surrounding areas after degeneration has occurred in thalamus. A role of such regions of cortex in the lengthy and difficult recovery of function following partial focal zone lesions is not entirely ruled out from these data, but the evidence here and in Wegener’s study (19) suggests it is a minor one. Second, the deficits which follow ablations of auditory cortex are purely auditory in character, and are in fact primarily a deficit in the ability to utilize periodicity cues in auditory input. The striking contrast between performance on intermittent noise discrimination and tone vs noise discrimination observed in the auditory retention control group is a clear confirmation of the hypothesis advanced by Neff as to the common feature of auditory tasks permanently failed by operated cats (11). Therefore despite differences in the details of the anatomical basis of auditory function between cat and monkey, at least some similar operations are performed in the cortices of both. Utilization of periodicity cues depends entirely on cortical centers in the auditory modality, and little or not at all in the visual modality (17). References ALES, H. W. 1959. Central auditory mechanisms, pp. 585.613. In “Handbook of Physiology, Sect. 1, hTeurophysiology” Vol. 1. J. Field led.]. Am. Physiol. Sot., Washington, D.C. APERT, K., C. N. WOOLSEY, I. T. DIA&,ZOXD, and W. D. NEFE. 1959. The cortical projection area of the posterior pole of the medial geniculate body in Macaca mzdatta. Anat. Record 133: 242. BATTIG, K., H. E. ROSVOLD, and M. MISHPIN. 1962. Comparison of the effects of

214

4. 5. 6. 7. a.

10. 11. 12. 13. 14. 1.5. 16. 17. 18. 19. 20. 21.

SYMMES

frontal and caudate lesions on discrimination learning in monkeys. /. Camp. Physiol. Psychol. 55: 458-463. BURTON, D., and G. ETTLINGER. 1960. Cross-modal transfer of training in monkeys. Nature 186: 1071-1072. CHOW, K. L. 19.51. Numerical estimates of the auditory central nervous system of the rhesus monkey. J. Comp. Neural. 95: 159-175. DAVIS, S. W. 1955. Auditory and visual flicker-fusion as measures of fatigue. Am. J. Psychol. 68: 654-657. EVARTS, E. V. 1952. Effect of auditory cortex ablation on frequency discrimination in monkey. J. Neurophysiol. 15: 443-448. GOLDSTEIN, M. H., JR., N. Y-S. KIANG, and R. M. BROWN. 1959. Responses of the auditory cortex to repetitive acoustic stimuli, J. Acoust. Sot. Am. 81: 356-364. GROSS, C. G. 1963. Comparison of the effects of partial and total lateral frontal lesions on test performance by monkeys. J. Camp. Physiol. Psychol. 56: 41-47. MASSOPUST, L. C., JR., H. W. BARNES, and J. VERDURA. 1965. Auditory frequency discrimination in cortically ablated monkeys. J. Auditory Res. 5: 85-93. NEFF, W. D. 1961. Neural mechanisms of auditory discrimination, pp. 259-278. In “Sensory Communication.” W. A. Rosenblith fed.]. Wiley, New York. “The Main Afferent Fiber Systems of the Cerebral Cortex in POLYAK, S. 1932. Primates.” Univ. of California Press, Berkeley, California. PRIBRAM, K. H., B. S. ROSNER, and W. A. ROSENBLITH. 1952. Electrical responses to acoustic clicks: extent of neocortex activated. J. Neurophysiol. 1’7: 336-344. 1962. Response of the cerebral cortex of SMALL, A. M., JR., and N. B. GROSS. the cat to repetitive acoustic stimuli. J. Camp. Physiol. Psychol. 55: 445-448. SNIDER, R. S., and J. C. LEE. 1961. “A Stereotaxic Atlas of the Monkey Brain.” Univ. of Chicago Press, Chicago, Illinois. SYMMES, D., L. F. CHAPMAN, and W. C. HALSTEAD. 1955. The fusion of intermittent white noise. J. Acoust. Sot. Am. 27: 470-473. Flicker discrimination by brain damaged monkeys. J. Camp. SYMMES, D. 1965. Physiol. Psychol. 60: 470-473. WALKER, A. E. 1938. “The Primate Thalamus.” Univ. of Chicago Press, Chicago, Illinois. WEGENER, J. G. 1964a. Auditory discrimination behavior of brain-damaged monkeys. J. duditory Res. 4: 227-254. WEGENER, J. G. 1964b. Auditory discrimination behavior of normal monkeys. J. Auditory Res. 4: 81-106. WEISKRANTZ, L., and M. MISKKIN. 1958. Effects of temporal and frontal cortical lesions on auditory discrimination in monkeys. Brain 81: 406-414.