Localization of sound in space after unilateral and bilateral ablation of auditory cortex

EXPERIMEKTAL

NEUROLOGY

25, 521-533

Localization Unilateral

and

(1969)

of

Sound

Bilateral

in Space

Ablation

After

of Auditory

Cortex

NORMAN L. STROMINGER 1 University

of

Chicago, Chicago, Illinois

Received

July

21, 1969

Seven cats were trained to localize sound in space in a two-choice food-reward situation. Localizing ability was tested at angles from 90 to 5” and a threshold angle, where animals scored 75% correct responses, was determined. Six of them were deprived of auditory cortex unilaterally. The smallest lesion involved auditory areas I and II, the posterior ectosylvian gyrus, and the insular-temporal region, while the largest lesions included these plus somatic area II and the anterior and middle parts of the suprasylvian gyrus. Five animals had different degrees of deficit. One cat with an ablation of all cortical areas listed above except the suprasylvian gyrus, was unimpaired. Most discrimination errors were committed when the sound was on the side contralateral to the lesion. Symmetrical ablations later were produced in the opposite cortex of four animals. One other was deprived of auditory cortex bilaterally in a single operation. The only cat with all the regions ablated bilaterally was completely unable to localize sounds ; the others discriminated above chance at 90”. Introduction

Results of earlier studies have shown that bilateral ablation of portions of the cerebral cortex receiving auditory projections causesa severe impairment but does not totally abolish the ability of cats to localize sound in space. Ablations were restricted to auditory areas I (AI), II (AII), and the posterior ectosylvian gyrus (Ed) 2 (2, 28, 35). Evidence from anatomical and behavioral experiments has indicated that additional areas should be considered as part of the cortical projection region of the auditory system. The insular-temporal cortex (I-T), located inferior to AI1 and superior to the rhinal fissure, receives projecti’ons from the medial geniculate body (GM) ( 15, 27, 36). Ablations confined to it produce partial retrograde cell degeneration near the caudal end of the 1 Supported by the Office of Naval Research, Air Force Office of Scientific Research, National Science Foundation, and NIH Grant NB-06350. Present address: Department of Anatomy, Albany Medical College of Union University, Albany, New York, 12208. Appreciation is expressed to Prof. William Neff in whose laboratory this research was conducted. ‘2 See Fig. 1 in previous paper for map of auditory cortex (44). 521

522

STROMINGER

principal division of GM ( 15). Complete loss of cells occurs in the principal division only after lesionswhich include I-T in addition to AI, rlII. and Ep (27, 36). Evoked potentials to acoustic stimuli have been recorded from IT (13, 24. 52). This region also gives rise to descending auditory fibers (14, 34). Behavioral evidence suggests that I-T has distinctive auditory functions. Ablation of it produces severe or total deficit in ability to relearn a previously acquired tonal pattern discrimination (18) ; and also interferes with retention and relearning of a discrimination of difference in duration of two tones (43). Somatic area II (SII) is another area from which evoked responsesto acoustic stimuli can be recorded (4, 5, 10, 26, 32, 47). There is evidence that ablation of SII in addition to other auditory cortical areas may increase the postoperative deficit for someauditory discriminations (25, 43). Evoked responsesto acoustic signals can be recorded from the suprasylvian gyrus (SS j in unanesthetized animals (8)) and in those anesthetized with Dial (23) or chloralose ( 1, 9, 47). Lombroso and Merlis (23), finding that contralateral pinna twitches could often be elicited by application of a small strychnine patch to the anterior portion of SS. suggested that this area might be important for localization of sound direction. Ablations in earlier studies of sound localization in cats did not include all cortical areas now known to constitute the projection field of GM, and to be activated by auditory stimulation. Therefore, the present experiment was undertaken to re-evaluate the effects of bilateral cortical ablations upon sound localization. These experiments were also designed to determine whether unilateral ablations of auditory cortex may causeimpairments in localizing ability. Although Neff et al. (28) reported no changes in localizing ability in the cat after unilateral ablations of auditory cortex, ablations in their experiments were restricted to AI, AII, and EP, and tests of localization were made only at wide angles. Methods

Seven adult cats were trained to indicate the direction of a sound source. ‘4 measure of localizing ability was determined. Six cats were subjected to large unilateral ablations of auditory cortex; the smallest ablation included -41, AII, Ep, and I-T; the largest included these plus SS and SII. In the seventh animal, AI, AII, Ep, and I-T were ablated bilaterally in one stage. Cortical ablations were made by subpial suction aseptically under pentobarbital. After a recovery of at least 3 weeks, animals were retested. and scores on the localization task were compared with preoperative scores. When testing and retraining had been completed in four of the cats with unilateral cortical removal, symmetrical ablations were made in the opposite intact

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LOCALIZATION

hemisphere. These animals were retested as during the interoperative period. Experiments were conducted in a sound-shielded room. Cats were trained to apprmoach one of two food boxes which could be positioned at any point along the periphery cf a semicircular enclosure.3 The correct box was indicated by the sound from a 6-volt buzzer placed behind the apparatus on a separate stand. The buzzer was sounded five times ; the animal was then released from the starting cage. A correct response was reinforced by a food reward. Food was placed in both food boxes to prevent the animal from localizing on the basis of olfactory cues. The door of the box behind which the buzzer was sounded was unlocked ; the door of the other box was locked. Trials were conducted in complete darkness ; a luminous collar on the cat enabled the experimenter to follow its movements. A luminous stripe, visible only to the experimenter, was als’o painted on a portion of each food box assembly. Visual cues were eliminated as a control for visual field defects often caused by damage done to the optic radiations during cortical ablations. Fifteen trials were given at each daily session. Food boxes were separated by an angle of 90” until a criterion of 90% correct responses was reached in two consecutive test sessions. The angle between successive positions of the buzzer was then reduced to 40” followed by 20”, and training was continued until the same criterion was again reached. Thereafter, trials were conducted at 40, 20, and 10” discrimination angles (five trials per day at each angle). Animals scoring 14 correct responses at 10” on three consecutive days within the first lo-day period were also tested at a 5” discrimination angle. Scores were grouped into consecutive IO-day periods for comparison of preoperative and postoperative performance. Since a correct choice could be made by chance 50% of the time, the threshold was defined as the angle at which a score of 75% correct responses was made. If an animal scored better than 75% correct responses at the smallest angle tested, it was assumed that at 0” performance would be chance, and the threshold was estimated by interpolation. After completion of behavioral tests, the animals were deeply anesthetized with pentobarbital and perfused transcardially with 500 ml of 0.9% saline solution, followed by an equal amount of 10% formalin. Brains were dehydrated, infiltrated with celloidin, and sectioned serially at 50 IL. Two adjacent sections of every 10 were stained with thionine and by Weil’s hematoxylin method. Cortical lesions were reconstructed, and retrograde degeneration in the thalamus was plotted. 3 This

apparatus

was illustrated

in a previous

article

(44).

524

STROMINGER

Results

Anatomy. Reconstructions of cortical ablations for all animals are shown in Fig. 1. With bilateral lesions, the serial order is indicated, except for cat NS-862 which had a bilateral one-stage operation. The smallest unilateral ablation (in cat NS-645) included AI, AII, Ep, I-T. and part of SII. The largest unilateral lesions (in animals NS-784, NS-860, and NS-833) involved these together with SS from the coronal sulcus to the level of the posterior suprasylvian sulcus. In the single animal (NS-784) with all of these areas removed bilaterally, a narrow strip of cortex was spared directly above the rhinal fissure on the right side. Cortex lining the banks of sulci completely surrounded by a lesion was removed in all cases. At the boundaries between preserved and ablated cortical tissue, only cortex lining the same side of a sulcus as the lesion was injured. Retrograde degeneration in the thalamic portion of the auditory system was similar in all animals. Degeneration, representative for the group as a whole, is shown for animals NS-645 and NS-784 (Figs. 2 and 3). The principal division of GM underwent an almost complete loss of cells on the same side as operated hemispheres. Some normal-appearing cells remained at its caudal pole, particularly on the right side in cat NS-784, and to a lesser extent on the degenerated side in cats NS-833 and NS-860 with uni-

FIG. 1. Reconstructions ferred to standardized with bilateral two-stage

of cortical hemispheres. ablations.

lesions Numbers

in all seven animals I and II indicate

of this study transserial order in cases

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LOCALIZATION

FIG. 2. Cat NW545 Numbers I and II indicate serial order of cortical ablations. Drawings of frontal sections through thalamus. The drawing labeled “1” represents the most anterior section in which thalamic degeneration was present. Successive integers represent drawings of sections 0.5 mm caudal to the preceding section. A skip of one integer indicates that a drawing represents a section 1.0 mm caudal to the preceding section. Thalamic degeneration is indicated by stippling. The abbreviations used for thalamic nuclei are: AV, anteroventral; CL, central lateral; CM, centromedian; GL, lateral geniculate body, dorsal division ; GM, medial geniculate body, rostra1 part; GMp, medial geniculate body, principal division ; LD, laterodorsal ; LP, lateral posterior ; mc, medial geniculate body, magnocellular division; MD, mediodorsal; PO, posterior group; Pul, pulvinar ; RE, reuniens ; TO, optic tract; VL, ventral lateral ; VM, ventromedial ; VP, ventroposterior ; VPL, ventroposterior lateral ; VPM, ventroposterior medial.

lateral ablations. Degeneration in this region was most severe in cat NS645. The magnocellular division of GM also was severely degenerated, as was the posterior group of thalamic nuclei. Cell loss and a proliferation of neuroglia cells, attributed to subcortical interruption of thalamic radiations

I FIG.

3. Thalamic

3

degeneration

5

7

9

in cat NS-784. For explanation,

II

12

13

see legend of Fig. 2.

526

STROMINGER

to cortical areas outside the projection field of GM, were found in the latera posterior nucleus and in the pulvinar. The dorsal lateral geniculate body (GL) was almost completely devoid of neurons, except in animals NS-633, NS-784, and NS-645. The middle portion of right GL was preserved in cat NS-663. In cat NS-784, left GL was severely degenerated throughout, but on the right side the anterior half was preserved and incomplete cell loss was seen ii1 the posterior half. In cat NS-645, the anterior half of GL was preserved bilaterally and degeneration in the remainder of the nucleus was less severe than in cat NS-784. Degeneration in some cases was seen in the anterodorsal, laterodorsal, ventral anterior, ventrolateral, and ventroposterior nuclei of the thalamus. Behavior. The localizing ability of five of six cats was impaired after unilateral ablation of auditory cortex ; the degree of impairment was variable. After ablation of an approximately equal and symmetrical region of the opposite auditory cortex in four of the animals, a severe deficiency in localizing ability occurred. The cat with a one-stage bilateral ablation also was severely impaired. Tables 1 and 2 summarize the behavioral tindings before and after unilateral and bilateral cortical ablations, respectively. Thresholds and scores at angles indicated in Table 1 are based on data collected after an animal was first trained to a criterion of 90% correct responses for two successive days at angles of 90, 40, and 20”, a procedure requiring a minimum of 6 days of testing. After surgery, unimpaired animals might reasonably be expected to attain this level of performance with little difficulty. The TABLE UXILATEKAL

1

CORTICAL

ABLATION

(70) Correct responses Ablation

Cat no.

40” NS-663 I,eft

AI,

Left

AI,

NS-664

Rt.

AI,

Ep, I-T,

SII

AII,

Ep,

I-T,

SII,

SS

SII,

SS

Preoperative

NS-860 Rt.

NS-833

AII,

Preoperative

NS-78-l

NS-645

Preoperative AII, Ep, I-T, SII Preoperative

AI,

AII,

Ep,

I-T.

Preoperative Rt. AI, AII, Ep, I-T Preoperative Left

AI,

AII,

‘Sk days is minimum

Ep,

I-T,

SII,

SS

91 100 91 95 100 95

20”

10"

5"

94 85 100 91 98 84 94 81 96 81 98 82

81 82 93 83 80 75 75 68 83 53 85 66

66 68 76 65 72 68 61 56 69

time possible to reattain 90%

84

criterion at 20”.

Threshold (ded 8.0 7.5 1.8 7.8 6.9 10.0 10.0 15.4 6.1 17.6 3.7 15.6

20”Criter.O (day) 11 12 20 6

6 4.3

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LOCALIZATION

TABLE 2 BILATERAL CORTICAL ABLATION

Thresholdbefore Cat no.

second

NS-664 NS-645 NS-862 NS-663 NS-784 “Bilateral

7.8” 17.6” 12.4” 7.5” 10.0” ablations,

Correctresponses Ablation=

at 90” (%)

AI, AII, Ep, I-T, SII AI, AII, Ep, I-T AI, AII, Ep, I-T AI, AII, Ep, I-T, SII AI, AII, Ep, I-T, SII, SS

67 62 62 57 49

lesion

two-stage

except

NS-862.

number of days required to reattain the criterion of 900/o correct responses with the food boxes separated by a 20” angle was calculated, because the need for protracted retraining indicates an initial impairment, although subsequent performance, upon which thresholds and scores in Table 1 are based, n~ay bc TInaffected. The time required for each animal with unilateral ablations to s-ore 90% correct responsesat a 20” discrimination angle is shown in the inst coiumn of Table 1. Cat NS-663, as shown in Table 1, performed as well at 10 and 5” after ablation of left AI, AII, Ep, I-T, and SII as it had before operation. After operation scores at 20” were inferior to preoperative scores ; the difference was significant at better than the 0.04 level of confidence as determined by the chi-square statistical test using calculations for one-tailed probability. The other five animals given unilateral cortical ablations had elevated postoperative thresholds. The changesin threshold varied from 3” in cat NS-664 to 11.9” in cat NS-833. In these five animak, postoperative scoresat two or more angles listed in Table 1 were inferior to preoperative scoresat better than the 0.01 level of confidence. The number of incorrect responsesmade by animals with unilateral cortical ablations on the contralateral versus ipsilateral side was calculated for the last 300 trials. All six animals committed a greater number of errors when the sound was on the side contralateral to the lesion. The greatest bias was 1 :0 in cat NS-645, the least bias was 6:s in cat NS-860. After completion of postoperative tests, symmetrical lesions were produced on the opposite side in four animals (NS-645, NS-663, NS-664, NS-784). Another cat (NS-862) was deprived of AI, AII, Ep, and I-T bilaterally in a single operation. With the food boxes separated by an angle of 90”, cat NS-784 discriminated at change levels ; this animal sustained the largest bilateral cortical ablation in the group. While the other animals localized poorly at a 90” discrimination angle, scoreswere higher than would be expected on the basis of random performance (Table 2). One animal (NS-645) scored 90% correct responsesat 90” after 210 trials. The angle

528

STROMINGER

between the food boxes was reduced to 40” and the animal averaged 58% correct responses in the course of 490 trials. With the food boxes again separated by an angle of 90”, cat NS-645 averaged 62% correct responses in 570 trials, discounting another 210 trials in which the systematic order of stimulus presentation was altered to counter a position habit. The number of trials given different animals after bilateral ablations ranged from 780 to 1480. Scores of all animals tended to decline as testing progressed. Additional trials initially were given at 90” to two cats in order to determine whether they could select the correct food box if the buzzer was sounded continuously until termination of the trial. Cat NS-663 required 660 trials before scoring 90% correct responses, and thereafter averaged 80% correct responses during 750 trials. Cat NS-664 scored 90% correct responses for 2 days after 400 trials and maintained this level of performance during five successive sessions. Discussion

Three animals deprived unilaterally of AI, AII, Ep, I-T, SII, and SS had impaired ability to localize sound as measured in the present experiment. Localization was also impaired in two of three animals with less extensive cortical lesions. The threshold of one animal showed no change after operation. The cat with the least amount of cortical damage showed one of the greatest deficits in localization. All animals had nearly complete degeneration of GM. For the group as a whole, positive correlations could not be established between amount of deficit in localizing performance and any of the following variables : size of ablation, hemisphere (right or left) in which cortex was ablated, amount of GM degeneration, or other thalamic degeneration. When the food boxes were separated by angles of 90 or 40”, all animals with unilateral ablations were able to reach a criterion of 90% correct responses on two successive days. This may explain why Neff et al. (28) did not find an impairment after unilateral ablation in cats that were required to make a discrimination with the successive positions of the buzzer separated by an angle of approximately 50”. Furthermore, the smallest ablation in the present study included the entire projection region of GM while lesions in the earlier study were less extensive. After unilateral cortical removal, animals tended to select the food box located on the same side as the lesion more often than the food box located on the contralateral side. It seems unlikely that this bias was caused by a loss of vision in the heterolateral visual field resulting from damage to the optic radiaions. There is no correlation between the amount of degeneration in GL and the degree of bias. The homolateral GL was completely degenerated in the single unimpaired cat, whereas the anterior half was entirely pre-

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529

served in two animals that were deficient in localizing ability. Furthermore, testing was conducted in complete darkness in an attempt to control for asymmetrical visual field defects caused by unilateral ablations. In the light, animals were able to move about in normal fashion ; all cats routinely ran from the animal room to the testing room, a distance of about 23 meters, without making circling movements. Another possible explanation for the tendency of postoperative animals to choose the box located on the same side as the lesion is that damage to auditory cortex has a greater effect in the contralateral as opposed to the homolateral auditory field. This interpretation would be consistent with the finding of Sanchez-Long0 and Forster (42) who reported that blindfolded patients with temporal-lobe defects showed impairment in localization predominantly in the contralateral field. Other data from human patients with partial temporal lobe ablations and one with right hemisphrectomy also suggest that ability to localize a sound signal may be more impaired in the sound field contralateral to the cortical lesion, but the results do not provide conclusive evidence (45). On the other hand, Walsh (51) failed to find any relation between hemisphere of temporal lobe damage and accuracy of localization in ipsilateral versus contralateral auditory fields. In studies not involving localization, various observers (3, 11, 19, 21), demonstrated that patients with unilateral temporal lobe damage have a greater deficit in discrimination of distorted speech in the contralateral ear than in the homolateral ear. Epileptic patients at onset of a seizure sometimes hear sounds which are referred to the side opposite the epileptic focus (30). Sounds heard after electrical stimulation of the temporal lobe typically are referred to the contralateral ear (31). Electrophysiological evidence suggests that ascending auditory fibers which cross the midline may be more important than uncrossed auditory pathways. Studying the response of single units in the medial geniculate to clicks, Galambos et al. (17) found units responsive to stimulation of both ears, the contralateral ear only, or the ipsilateral ear only. More units were activated by stimulation of the contralateral ear than of the ipsilateral ear. Results of several studies indicate that electrical or sound stimulation of one cochlea produces a greater amplitude evoked response at the contralateral cortex than at the ipsilateral cortex (6, 38, 39, 41, 49, 50). According to Bremer (4) and Rosenzweig (39, 40)) a differential amplitude in response between the two hemispheres forms the basis for localization of sound. Coleman (12), on the other hand, observing that the relative amplitude of evoked potentials at different cortical loci changed as a click stimulus was moved around the head, suggested that each cortex receives information representing spatial location in both auditory fields. Using single-unit recording techniques, Brugge, Dubrovsky and Rose (7) and Hall and Gold-

530

STROMINGER

stein (20)) with unanesthetized preparations, confirmed Coleman’s ( 12) predictions. Evans and Whitfield, as reported by the former (16), found that over half of 45 consecutive single units studied in auditory area I of unanesthetized cats were specifically or preferentially sensitive to specific locations of a sound source with reference to the head. The majority of these neurons were preferentially sensitive to contralateral sound stimuli ; a small percentage of cells exhibited preferences for ipsilateral stimulus locations. Results of the above studies suggest that although auditory space is represented bilaterally at the cerebral cortex, there is a stronger contralateral representation. Thus deficits in sound localization might reasonably be expected to be greater in the contralateral than in the ipsilateral field after unilateral cortical ablations, as seen in this study as well as clinically (42, 45). Unilateral interruption of the main neural pathways leading t,o auditory cortex at midbrain levels produces similar results (46). Bilateral ablation of AI, AII, EP, I-T, SII, and SS, produced a total inability to localize sound in cat NS-784. Animals with less extensive cortical damage, but with elimination of the cortical projection region of GM, showed severe impairments but were not totally unable to localize sound. The deficit was more severe than previously reported (28), due to the more extensive ablations of auditory cortex. With the exception of AI, bilateral ablations of subdivisions of auditory cortex were found to have no efl’ect upon sound localization (44). Lesions limited to AI produced small transient or longer lasting impairments. Bilateral ablation of auditory cortex is without effect on the absolute or differential intensity limen (22, 29, 33, 37). Data from cats NS-663 and NS-664 are in agreement with findings that orientation to sound in animals deprived bilaterally of auditory cortex is proportional to duration of the stimulus (35, 48). References 1. +.hlAssrAN, including 2.

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47. 48. 49. 50. 51. 52.

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