J. Neurol. Neurosurg. Psychiat., 1961, 24, 240.

THE EFFECTS OF HEMISPHERECTOMY ON INTELLECTUALFUNCTIONING IN CASES OF INFANTILE HEMIPLEGIA

BY

JOHN McflEFrom the National Hospital, Queen Square, London

The recent increase in the number of reports ofresults of hemispherectomy, after which the majorityof patients show considerable clinical improvement,prompts an inquiry into the effects of this operationon the exercise of intellectual abilities, and theirimplications for the understanding of cerebralorganization.

Until a decade ago, the operation was rarelyperformed, and then usually for the removal ofextensively infiltrating gliomata. Moreover, themajority of these removals were of the right hemi-sphere: of 16 cases collected by Mensh, Schwartz,Matarazzo, and Matarazzo (1952), only one, that ofZollinger (1935), was of a left hemisphere. Hillier(1954) reported another case of left hemispherectomyfor glioma, and in the series of Gardner, Karnosh,McClure, and Gardner (1955) there was one case ofleft-sided removal. Earlier accounts (Dandy, 1928;Gardner, 1932; Diven, 1934; Rowe, 1937) did notreport any psychological impairment following theright-sided operation; however, the patients werenot given performance tests of the kind sensitive toright hemisphere lesions, and the more detailedstudies of Gardner et al (loc. cit.) led these authorsto conclude that 'removal of a cerebral hemisphereleft the patients with defects injudgment and inabilityto plan for the future; and in all patients psycho-metric studies indicated an impairment in insight, inemotional control, in initiative, and in perseverance'.In the three cases of left hemispherectomy (Zollinger;Hillier; Gardner et al) speech disturbance wasassociated with a marked degree of intellectual im-pairment, but the dissolution of language was notabsolute and in the youngest patient (that of Hillier,a 14-year-old boy) a considerable improvement inspeech was observed during the two years followingoperation. In general, then, the psychological resultsof hemispherectomy for glioma are seen to be, whenthe left hemisphere is involved, a profound but notabsolute impairment of speech, and when the righthemisphere is involved, at least a reduction injudgment and insight.

In cases of infantile hemiplegia, on the other hand,the changes reported are entirely different. Williamsand Scott (1939) gave a brief description of a patientaged 20 years, who had suffered a left cerebral injuryat the age of 3 weeks: removal of the damaged hemi-phere resulted in 'no apparent mental deterioration',and two years later the patient was able to cooperateintelligently as a subject in a physiological experi-ment. One of the four patients of Marshall andWalker (1950) was a case of birth injury to the righthemisphere; and it is interesting to note that in thispatient speech was reported to be more retarded indevelopment than was walking. It was Krynauw(1950), however, who suggested the operation as atherapeutic measure, and presented a series of 11patients with infantile hemiplegia and epilepsy,ranging in age from 7 months to 21 years, who hadimproved after hemispherectomy. In one (Case 10)partial ablation resulted in no improvement, and theentire hemisphere was removed at a second opera-tion. In 10 of the patients, it was the left hemispherewhich was involved; yet in none of these was anysignificant impairment of speech reported as a con-sequence of the operation, and in some there wasstriking improvement. In all except one of thesepatients, the injury was in the first 10 months afterbirth; in the remaining one (Case 9) there was ahistory both of difficult birth and of a severe febrileillness at 4j years. From this evidence, Krynauwargued not only that removal resulted in liberationof the remaining hemisphere from the 'abnormalinfluences of the pathological side', but also that'with regard to language function . . . hemispheredominance had adjusted itself before the removal ofthe affected hemisphere, and that it was the minorhemisphere which was removed in all cases'.Krynauw did not make any statement about the ageat which this 'adjustment' might take place: Obrador(1951), however, reported four cases of hemi-spherectomy, one of which (Case 3) was of the lefthemisphere in a child of 7 years, who had beennormal and right-handed until the age of 5, when a

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meningitic infection had left her with a right hemi-plegia and dysphasia. Removal of the left hemisphereresulted in no increase in the dysphasia but in animprovement in speech. Obrador concluded that 'upto the age of 5 years language functions can beintegrated in the right hemisphere'.

Cairns and Davidson (1951) presented the resultsof hemispherectomy on three patients to a meetingof the Neurological Section of the Royal Society ofMedicine. In addition to clinical improvement, everypatient showed an increase in score on psychologicaltests after the operation, the average being in theregion of 20 points of I.Q. Two of the operationswere on the right side and one on the left, but onlyin Case 2 (right-sided, for Sturge-Weber-Dimitridisease) can the age of injury be inferred from thereports. At the same meeting, McKissock and hiscolleagues (unpublished) reported a series of 11hemispherectomies, seven right and four left, and Iobserved that in only one patient (whose left hemi-sphere was injured at 20 months) had there been afall in I.Q. after operation, but that in the majorityof patients language abilities were inferior to abilitieson performance tests, irrespective of which hemi-sphere was damaged. With the younger children anddefectives, this amounted to virtual absence oflanguage, while motor performances were at a con-siderably higher level; on the Terman-Merrill scale,some reached a higher standard on the non-verbalthan on the verbal items, and on the Bellevue scale,this discrepancy was represented in the differencebetween I.Q.s on the verbal and performance partsof the test. McKissock (1953) reviewed his experienceof 18 hemispherectomies, and established firmly hiscriteria for recommending the operation, namely, thecoexistence of infantile hemiplegia with epilepsy andbehaviour disorder.Achslogh and Ectors (1954) reviewed the litera-

ture of hemispherectomies to that date, which, theystated, 'must exceed a hundred'. Their own patientwas aged 17 years, with a right hemiplegia followinga febrile illness at the age of 9 months. Before theoperation the patient refused to do any tests, butafter left hemispherectomy (the authors observe thatit should really be called hemidecortication) hisTerman-Merrill I.Q. was 87, with an almost 'averageadult' vocabulary. The authors noted that 62% ofthe hemispherectomies published were of the leftside, yet in no case of infantile hemiplegia had thisresulted in aphasia. Perlstein and Sugar (1954)reported briefly on two hemispherectomies, one rightand one left, for infantile hemiplegia; Sugar stated'in communication with Dr. J. M. Nielsen, I learnedthat if the speech center is damaged before the age of10, the child will recover his speech'. Uecker,French, and Johnson (1954) reported the results of

psychological tests of hemispherectomy in seven epi-leptic hemiparetics, injured 'in infancy or early child-hood'. They took particular care to eliminatepractice effects by using different forms of tests oneach occasion or by delaying retesting with identicaltests: the results showed no marked losses followingoperation, and some improvement in the twopatients whose pre-operative I.Q.s were near theaverage normal level. Unfortunately, in no case wasthe side of operation or actual age of injury stated.Zulch (1954) described two cases: the first, aged 27,with birth injury of the left hemisphere, began to walkat 13 months and first spoke at 3 years, and had 'anaverage intelligence, which was not changed' afterhemispherectomy. The second, aged 5, with a birthinjury to the right hemisphere, had an intelligence'in keeping with her age', and was improvedfollowing operation.

In addition to their cases of hemispherectomy forglioma, Gardner et al. (1955) described a 29-year-old infantile hemiplegic, with a verbal I.Q. of 67which rose, 37 days after right hemispherectomy, to78. Comparison with the other patients showed thathemispherectomy for glioma resulted in more im-pairment than for infantile hemiplegia, and theauthors concluded that 'immature cortex can acquirefunctions planned for the cortex of the other side,but (with the possible exception of speech) once afunction has become established in the cortex it can-not be transferred'. 'Transfer' is perhaps not thebest definition for acquisition of a function by an areaof cortex following excision of the area previouslyexercising that function; and, as far as psychologicalabilities are concerned, there is no direct evidenceof the exercise of any other function than that ofspeech. None of the reports is concerned witharithmetical ability, visual-spatial analysis, or anyother specific ability, and even reading and writingare only briefly mentioned in a few cases.

In fact, the criticism of Mensh et al. (1952) thatearlier reports were mostly 'in general terms' ratherthan detailed accounts may be levelled also at sub-sequent studies. In very few cases are the sidedamaged, the age at injury, and the pre- and post-operative scores (or changes) on tests, given for eachpatient. Nevertheless, certain definite conclusionsmay be drawn from the foregoing series, and certainquestions asked. Perhaps the clearest inference,following upon the descriptions of cases of earlyinjury to the left hemisphere without marked dis-turbance of speech, is that, as Krynauw put it, 'hemi-sphere dominance had adjusted itself before removalof the affected hemisphere'. This immediately raisestwo questions: Is there a critical age beyond whichthis adjustment does not take place? And is there asimilar adjustment in respect of 'right hemisphere

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JOHN McFIE

functions', such as spatial analysis, in cases ofdamage to the right hemisphere? A third, subsidiaryquestion might be asked: Is there similar adjustment,in cases of left hemisphere injury, of other 'lefthemisphere functions' such as calculation, abstrac-tion, and constructional ability (c.f. McFie andPiercy, 1952)? The answer to the question of age ofadjustment may be that it is a gradual process. Innone of the patients with birth injury was any reduc-tion in speech reported after the operation; inKrynauw's Case 3, injured at 10 months, speech wasimpaired immediately following (left) hemispherec-tomy, but later improved greatly; Obrador's Case 3appears to have been normal up to 5 years, when theleft hemisphere was injured with resultant dysphasia,and two years later hemispherectomy resulted in im-provement in speech; according to Sugar, Nielsenasserted that recovery of speech would take place ifthe damage had been done before 10 years; and thecase of Hillier makes it clear that considerable im-provement is possible even after 14 years of age.Nevertheless, it appears to be possible to distinguishbetween the results of birth injury, in which no im-pairment of speech follows left hemispherectomy,and of injury at some later age, in which removalresults in deficit but is followed by improvement. Itmay be of some theoretical interest, and of clinicalvalue, to establish whether or not such a critical ageexists. The question of adjustment ofother functions,or of their establishment in the undamaged hemi-sphere, cannot be answered from the foregoingreports; in very few cases was any other psychologicalability than speech studied in sufficient detail.Another conclusion which is affirmed by several

authors is that greater improvement in cases ofinfantile injury results from complete hemispherec-tomy (or hemidecortication) than from partialremoval of a damaged area even if the remainingcortex appears normal. Laine, Fontan, Delandt-sheer, and Delandtsheer (1951) compared the resultsof 14 cases of various types of restricted operationwith two cases of hemispherectomy, and concluded'we must abandon localised intervention in thesecases: we must follow the Anglo-Saxon example ofpreference for hemispherectomy'. Krynauw sug-gested that the remaining hemisphere was able tofunction normally once it had been 'released fromabnormal influences from the pathological side'. Inview of the almost unaminous agreement on thebeneficial effects of the operation, it is of interest toask what is the extent of the improvement, whetherit varies with side affected, and to what influences itmay be attributed. Many of the patients reportedwere mentally defective, but even the most scepticalauthors, Uecker et al., reported the greatest post-operative improvement in those patients whose pre-

operative I.Q.s were nearest to normality; thereforeit may be that those with the highest pre-operativelevels show the greatest benefits. Table I sum-marizes the post-operative I.Q.s of patients in thestudies quoted. It will be noted that the mean I.Q.is 63-4, and that the distribution is skewed, with apreponderance of individuals with low values.

TABLE II.Q.s AFTER HEMISPHERECTOMY FOR INFANTILE

HEMIPLEGIA IN PUBLISHED CASES

Authors Case Number I.Q.

Cairns and Davidson (1951) I 1112 743 106

Achslogh and Ectors (1954) 1 87

Uecker et al (1954) 1 372 203 184 165 766 887 38

Gardner et al (1955) 1 78

French et al. (1955) 1 82

Mean 63-4

There remains my earlier suggestion that infantilehemiplegics show an impairment of language ability,irrespective of the hemisphere actually damaged, incomparison with their non-language functions. Ifconfirmed, this would dispose of the earlier questionconcerning pre-operative 'adjustment' of right hemi-sphere functions; it would appear to be moreefficient than that of left hemisphere functions.Again, however, the question of age would be raised.Is there evidence of a critical age at which thisapparent relative impairment of language functionsis replaced by the usual pattern of impairmentaccording to hemisphere affected?

Present StudyThe number of hemispherectomies for juvenile

hemiplegia performed at the National Hospital isnow over forty: the clinical indications and operativetechnique have already been made clear (McKissock,1953, 1954). Of these patients, psychological testrecords are available for 34, and, in addition, recordsare available for nine patients who underwent partialremovals, i.e., excision of evidently damaged tissue.(One of these subsequently had the rest of the hemi-sphere removed, and is therefore in both groups.)The clinical indications for the two types of opera-tion were essentially the same. The relevant informa-tion about the patients is given in Table II. The in-telligence quotients are those achieved on whatevertest was appropriate to the patient's level: for the

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EFFECTS OF HEMISPHERECTOMY ON INFANTILE HEMIPLEGIA 243

TABLE IIPARTICULARS OF PATIENTS

Ptet Hospital Age at Heipee Pre- Age at Post- Post-Patient No. In Hemisphere operative Operation operative operative PathologyNo. No. Injury I.Q. (years) I.Q. E.E.G.

A Hemispherectomy1 15623 Birth R 29 5 35 N Porencephalic cyst2 20809 Birth L 23 11 23 1 Diffuse changes3 22069 Birth R (a)* 4 - 2 Porencephalic cyst4 23239 5 yr. R 64 10 60 3 Diffuse changes5 22684 Birth R 75 20 91 N Porencephalic cyst6 22797 15 mth. R 48 7 43 2 Diffuse changes7 25473 Birth R 13 23 19 1 Porencephalic cyst8 27415 3 mth. L 55 21 62 N Porencephalic cyst9 29312 20 mth. L 38 12 25 3 Diffuse changes10 29310 6 mth. R 37 13 38 1 Diffuse changes1 1 616 Birth R 35 14 40 2 Diffuse changes12 29776 Birth R 73 18 88 N Porencephalic cyst13 30185 15 mth. L 67 5 67 N Porencephalic cyst14 31140 21 yr. R (b)t 25 (b) I Diffuse changes15 14805 Birth L 79 23 93 N Porencephalic cyst16 34270 Birth L 50 3 50 1 Diffuse changes17 34357 Birth R 47 19 55 1 Sturge-Weber-Dimitri disease18 36382 3 mth. L (a) 6 - 3 Diffuse changes19 38776 12 mth. R 66 13 66 1 Diffuse changes20 39712 3 mth. L 43 5 83 2 Diffuse changes21 36517 4 mth. L 30 1 62 N Porencephalic cyst22 42162 Birth R 75 7 65 N Sturge-Weber-Dimitri disease23 43346 3 yr. R 27 12 38 1 Diffuse changes24 51472 21 mth. L 75 3 75 N Diffuse changes25 51025 Birth L 48 13 66 N Porencephalic cyst26 52847 6 mth. L 35 2 47 3 Diffuse changes27 52665 Birth R 53 19 65 1 Diffuse changes28 55734 11 mth. R 55 7 (c0 (c) Diffuse changes29 57057 Birth R 51 7 59 2 Diffuse changes30 57161 Birth R 59 31 (c) I Diffuse changes31 59160 Birth L 69 15 74 N Porencephalic cyst32 61924 Birth R 80 24 90 N Porencephalic cyst33 29350 Birth R 68 11 (c) (c) Diffuse changes34 50512 10 mth. R 81 22 93 N Diffuse changes

B Partial Removals1 12534 Birth R 116 15 1082 16235 3 mth. L 61 18 583 13769 Birth L 71 25 694 616 Birth R 40 13 365 33202 2 yr. R 74 4 716 39232 Birth L 70 11 777 39401 6 mth. R 72 9 598 46620 Birth R 69 15 669 68285 Birth R 100 12 102

(a)* Too low to be scored.(b)t Patient's English only fragmentary.(c)t Not seen after operation.E.E.G.:N, no abnormality in remaining hemisphere; 1, slight abnormality; 2, moderate abnormality; 3, gross abnormality.

grossly defective children, on Griffiths' develop-mental scale; for the intermediate groups, on theTerman-Merrill scale; and for the higher levels, onthe Wechsler-Bellevue scale. The description of post-operative E.E.G.s is limited to the presence orabsence of major abnormalities as reported at thetime of recording, particularly of slow waves, of fastactivity, or of foci of spike discharges. The descrip-tion of pathology in the removed hemisphere islimited to three categories: porencephalic cyst;diffuse scarring and atrophy; and unilateral Sturge-Weber-Dimitri disease (cutaneous-leptomeningealangiomatosis).

Intelligence Quotients.-The level of two childrenwas so low as to be unscorable on any scale, one wasof foreign birth and education, and three patientswere not seen post-operatively. The scores of theremaining 28 patients at intervals after the operation

are represented graphically in Fig. 1. The distribu-tion of the pre- and post-operative intelligencequotients is shown in Table III. This includes thegrossly defective patients, and also those seen on oneoccasion only. The scores were all on the same testsas those given pre-operatively, and there is thereforea possibility that some of the increases may be dueto the effect of practice. While this may reduce thesignificance to be attributed to a number of increases,it must by the same token throw emphasis on those

TABLE IIIDISTRIBUTION OF INTELLIGENCE QUOTIENTS

I.Q. 0-19 20-39 40-59 60-79 80-99

Number of patientspre-operative 3 8 10 10 2

Number of patientspost-operative 3 5 6 10 6

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FIG. 1.-Changes in intellectual level after hemispherectomy.

cases in which increase is absent or in which there isa fall in score.For the purpose of evaluating the changes in

intelligence, the score at retesting at an intervalnearest to two years after operation has been used,and the average change between the pre-operativescore and this retest score is given, for variousgroups, in Table IV, together with the significance ofthe difference between groups. The mean change forthe whole series of hemispherectomies is nearly + 8points of I.Q., and this differs significantly from theaverage for partial removals, namely, 3 points.Between left and right hemispherectomies, on theother hand, the difference in change is not significant.This might have been the consequence of differencesin pre-operative intelligence between the two groups,but again the slight difference is not significant.

Since it is likely that the remaining hemisphere wasnot entirely free of pre-operative pathology in allcases, the average change in I.Q. has been comparedfor groups with evidence of various degrees of ab-normality in the post-operative E.E.G.s; apart froma fall in the group with the greatest abnormalities(three patients only), there is no evidence ofassociated differences. Between the group withporencephalic cysts in the removed hemisphere, and

those with other changes, the difference in change inI.Q. does not reach the conventional level ofsignificance, but may be regarded as worth furtherinvestigation.

Age of Injury.-The most striking difference inmean change, however, is that associated with theage at which the injury to the hemisphere occurred.The positive change in those injured at birth and inthe first 12 months of life contrasts with the negativechange in the group injured after 1 year of age. Thealteration in I.Q. is shown in Fig. 2 to occur inassociation with injuries after 11 to 12 months ofage, and the difference between averages for thebirth-and-infantile groups, compared with thejuvenile group, is highly significant. In the light ofthis evidence, it is necessary to re-examine the com-parisons of Table IV, omitting the scores of the sevenpatients with juvenile injury, since these may haveobscured differences in the infantile injury group. Inthe comparison of partial with total removals, thiscorrection leaves the average for the group withpartial removals the same, but increases the changein the group with total removals, thus furtheremphasizing the difference. With regard to hemi-sphere damaged, the correction results in a slight

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40[30O

20

10

0

A *S0 0

Birth 1 2 3 4 5

FIG. 2.-The relationship of change in I.Q. after hemispherectomyto age at which the hemisphere was injured.

increase of both averages, without increase in sig-nificance. In the E.E.G. groups, the correction hasthe effect of removing the two negative scores fromthe last group (3); the remaining patient showed a

change of + 12 I.Q. points, and the variation be-tween groups practically disappears. The suggestivedifference between cyst and non-cyst groups alsodisappears after the correction, since none of thecases ofjuvenile injury is in the group with cysts. Thegeneral effect, then, of omission of these patients isto confirm the significant conclusions which may bedrawn from the data in Table IV.

Other variables which may be associated withpost-operative change in intellectual level are the ageat which operation is undertaken, and the patient'spre-operative intellectual level. Correlation co-

efficients between these variables have been com-

puted for the infantile injury group, i.e., excludingthose with injury over 1 year of age, and are (1)change in I.Q. with age at operation, r = -0-02 (notsignificant); and (2) change in I.Q. with pre-operativeI.Q., r = 007 (not significant). There is thus no

evidence of association between change in I.Q. andeither of these variables. It is interesting to note thatfor the correlation (3) of age at operation with pre-operative I.Q., r = 0-362. For 21 observations, thisjust exceeds the P = 0-1 level of significance, andmay be regarded as indicative of a reluctance on thepart of the surgeon to operate on apparently intel-ligent young children.

Differential Impairment.-So far, the only measureof intellectual level which has been considered is theintelligence quotient. This has the advantage that itis a measure related to the normal levels of achieve-ment at each age, which is provided by every test;and, while not strictly comparable between tests,

TABLE IVMEAN CHANGE IN I.Q. APPROXIMATELY TWO YEARS

AFTER OPERATION IN DIFFERENTCLINICAL CATEGORIES

I Nature of Operation

TotalHemispherectomy Partial Removal Significance of

n = 28 n = 9 Difference

7-72 -3-00 P <0-01

2* Side of Hemispherectomy

Left Right Significance ofn = 11 n = 17 Difference

10-46 5-95 n.s.(51-0) (54 8) (n.s.)

3t E.E.G. of Remaining HemisphereNormal 1 2 3n = 13 n = 8 n = 4 n = 3

9-31 6-33 12-00 -1-67

4 Nature of Pathology in Removed Hemisphere

Porencephalic Cyst Diffuse or Sinfcceon = 10 Sturge-Weber-Dimitri Significance ofn = 18 Dfeec

12-9 4-80 P <0-1

5 Age at Time of Injury

(a) Birth 0-11 months Over 1 yearn = 15 n = 6 n = 7

7 53 16-67 -1-57

Significance of(b) Under 1 year Over 1 year Difference

10-07 -1-57 P < 0-01

*The figures in brackets are mean pre-operative I.Q.s.tThe figures 1, 2, 3 represent different degrees of abnormality.

may nevertheless be used to estimate changes on re-testing with the same test. On the other hand, theI.Q. is unsatisfactory in that it is a measure of totalachievement, and provides no information on thesubject'srelativelevelsin different fields of intellectualfunction. In making comparisons of the effects oflesions in each hemisphere, it is essential to obtainseparate measures of different abilities, in particularof those in the verbal and non-verbal (or 'per-formance') fields. For these to be accurately com-pared, it is necessary to have scores on differentsubtests, and the only test of this type used in thepresent study was the Bellevue scale (Wechsler,1944). However, in only six of the patients was theintellectual level sufficient to enable them to attemptthis scale. The pre-operative subtest scores andverbal and performance I.Q.s of these patients,together with the post-operative changes, are givenin Table V, and of other tests in Table Va. Thenumbers are too small for significant statistical com-parisons to be made, but it will be seen that both

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TABLE VRESULTS ON WECHSLER-BELLEVUE TESTS

Case Digit AnVerbal Picture Pictorial Block Digit PerformanceNumber Span Arithmetic Similarities Vocabulary I.Q. Completion Arrangement Design Symbol I.Q.

Left Hemisphere8 3 (+3) 0 (0) 2 (+1) 3 (+1) 57 (+7) 8 (+4) 4 (0) 7 (0) 3(-) 61 (+8)15 4 (+5) 7 (+2) 8 (+I) 7 (+2) 82 (+15) 8(-) 8 (-) 8 (+3) 5(-) 80 (+9)

Right Hemisphere5 6 (0) 4 (0) 7 (1) 6 (0) 70 (+7) 11 (+1) 6 (+4) 9 (+2) 4 (+5) 85 (+24)12 4 (0) 3 (0) 5 (+2) 5 (+I) 68 (+8) 14 (0) 8 (-1) 7 (+2) 4 (0) 85 (+7)17 2 (-2) 0 (+1) 5 (+2) 4 (0) 58 (+1) 3 (-1) 3 (-2) 3 (0) 2 (0) 47 (-3)34 4 (0) 10 (0) 7 (+1) 6 (+I) 80 (+7) 10 (0) 6 (+3) 9 (+I) 7 (+3) 85 (+16)

- = Test not done. ( ) = Change in score after operation.

TABLE VARESULTS ON ADDITIONAL TESTS

Case Number Weigl's Sorting Learning Memory Design

8 F (P) 7 (0) 1(+)15 F (P) -(-) 4 (0)5 F (F) 9 (+1) 4 (0)12 F (P) 9 (0) 4 (0)17 F (F) --34 -(-) 10+ (-3) 4(0)

-= Test not doneChange in score after operation.

Weigl's Sorting: F, failed; P, passed; ( ) post-operative result.Sentence Learning: Score = number of repetitions required to learn.

with left- and right-sided lesions all patients but onescored higher on performance than on verbal tests,and that in general (again with the exception of onecase) the post-operative increases were greater onperformance than on verbal tests. These differencesare emphasized by the results of the additional testsshown in Table Va. The failures on Weigl's test andon the sentence learning test (normally learnt in fiverepetitions), in contrast to the majority obtaining amaximum score (four points) on memory for designstest, is conventionally characteristic of left hemi-sphere lesions (McFie, 1960). Two points are note-worthy: that all these patients are in the group ofinfantile injuries, i.e., under 1 year of age, and thatthe case with anomalous results (Case 17) was oneof Sturge-Weber-Dimitri disease.Whether there is a similar discrepancy between

verbal and performance level in the remainingpatients cannot, as has been explained, be assessedas accurately as in those able to attempt the Bellevuescale. It is possible, however, to make a rough esti-mate of the relative levels reached, by comparison ofthe age levels reached in verbal and performanceparts of Griffiths' developmental scale, and byexamination of the individual items passed in theTerman-Merrill scale. Moreover, since this com-parison concerns only pre-operative scores, it ispossible to include in the classification the patientswho ultimately underwent only partial removal.Table VI shows the number of patients with left- and

right-sided lesions, subdivided according to the rela-tive impairment of their abilities, i.e., whether theirgeneral verbal level was lower than their performancelevel, or vice versa. With conventional cerebralorganization, it would be expected that a greaternumber with left-sided lesions would show verbaldeficits, and a greater number with right-sidedlesions, performance deficits. In fact, the data inTable VI show that there is a large group of patients

TABLE VIRELATIVE IMPAIRMENT IN WHOLE SERIES

Side of Lesion

Left Right

Relative loss ] Verbal 9 15Relatieloss Performance 4 8

with apparently anomalous verbal deficit in associa-tion with right-sided lesions. We have seen (Table V)that this association occurred in a small group ofpatients with infantile, i.e., at birth or under 12months, injury: it is therefore relevant to inquirewhether this association is significant for the seriesas a whole, and whether it varies with side of lesion.Table VII shows that relative verbal impairment is

TABLE VIIRELATIVE IMPAIRMENT ACCORDING TO SIDE

AND AGE OF INJURY

Side of Lesion Left RightInjury Infantile Juvenile Infantile Juvenile

_~~ ~ ~~~~Relative Verbal 8 1 14 1loss Performance 3 1 5 3

more frequent in cases of infantile injury; but where-as this may not be unexpected with left-sided lesions,it is unexpected in association with right-sidedlesions. Comparison between numbers with verbaland performance losses associated with infantile andjuvenile injuries to the right hemisphere (in the

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second part of Table VI) yields a value of x2 = 1-46,which does not reach the P = 0X1 level of significancefor the 23 cases. However, it has been possible to addfrom our records the results of testing a further 42unoperated children with pneumoencephalographicevidence of unilateral (right-sided) cerebral injury, inwhom the age of injury could be ascertained fromthe history. Using the same criteria as for theoperated children, all cases of right hemisphere injuryare analysed in Table VIII. For these proportions,

TABLE VIIITOTALS OF OPERATED AND UNOPERATED CASES

FOR RIGHT HEMISPHERE INJURY

Injury Infantile Juvenile

Relative loss Verbal 34 8Performance 9 14

x2 = 9-89 (P < 0-01), indicating a significant con-trast between the type of impairment resulting from

4 right hemisphere lesions sustained in infancy (verbaldeficit) and in subsequent years (performancedeficit). Returning to the operative series, the recordsof the group of 11 patients in whom right cerebralinjury had occurred in infancy, and who showed arelative verbal loss, were examined for possibleassociation with E.E.G. or pathological abnormali-ties. Five of these had normal E.E.G.s in the remain-ing hemisphere; three had grade 1 and three grade 2abnormalities. Six of these had porencephalic cystsand five had diffuse lesions. (The two cases ofSturge-Weber-Dimitri disease both showed 'con-ventional', i.e., performance deficit.) There is thusno suggestion that this anomalous verbal impairmentwith right infantile lesions is significantly associatedwith any E.E.G. or pathological abnormality.

Dysphasia.-The relative verbal intellectual im-pairment noted above is a 'high level'-perhaps thehighest level-manifestation of a language disability.In many patients there was also evidence of lowerlevel disorder of language, in the form of dysphasia,generally of the nominal type but occasionallyincluding receptive errors. In five of these patientsthere were also signs of other left hemisphere dis-abilities such as dyscalculia, constructional dys-praxia, and 'simultanagnosie'. The association ofdysphasia with side and age of injury is shown inTable IX: it will be noted that the occurrence of thissymptom with right hemisphere injury is almost ex-clusively in those patients with injuries sustained ininfancy, thus agreeing with the evidence of the pre-ceding section. It may further be observed that ofthe two patients with juvenile left cerebral injury whounderwent total hemispherectomy (Cases 9 and 24),

TABLE IXPATIENTS WITH CLINICAL DYSPHASIA

Side of InjuryLeft Right

Age at injury Juvenile 4 1

the first was almost asphasic for some weeks afteroperation, and showed a fall in I.Q. post-operatively,while the second showed no change in I.Q., in con-trast to the general increase after operation seen inpatients with infantile injury, together with disap-pearance of dysphasic symptoms.

DiscussionThe data from the present series of patients

support the main conclusions which may be drawnfrom the literature on hemispherectomy. Changes inoverall intelligence following hemispherectomy forinfantile hemiplegia are generally positive, in con-trast to the effects of limited or partial removals.Whereas some of this improvement may be due topractice effects, and to better adjustment to thehospital environment, this only emphasizes the lackof improvement, or deterioration, following partialremovals. This evidence, then, supports Krynauw'ssuggestion that the remaining hemisphere is free tofunction normally when the abnormal influences ofthe damaged hemisphere are removed, and amongabnormal influences must be included the dis-turbances associated with epileptic activity.The few post-operative intellectual losses in our

series are all except one (Case 22) in patients whosustained their injury above the age of 1 year, i.e.,in patients suffering from juvenile rather than frominfantile hemiplegia. As far as can be judged fromreports in the literature, this is in keeping withgeneral experience: in cases described as of 'infantilehemiplegia', hemispherectomy has resulted in im-provement, while in cases of injury later in life thereis some post-operative deficit, although relearningmay occur. The one exception to this (apart fromthe reported dictum of Nielsen) is Obrador's Case 3,in whom the evidence is clearly that the left hemi-sphere injury was sustained at 5 years of age, andthat the consequent aphasia was diminishing follow-ing hemispherectomy. Nevertheless, the greatmajority of reports support Krynauw's second sug-gestion, that 'adjustment' of hemisphere dominancehad occurred before operation, with the limitationthat this adjustment is only complete if the injury isinfantile. By the end of the first year, it appears likelythat the conventional partition of functions intoright and left hemispheres has begun, and that sub-sequent injury to a hemisphere does not entirely

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JOHN McFIE

dislodge its functions to the other side, with theresult that removal of a hemisphere removes a certainamount of functioning tissue.

Liberated from the influences of the damagedhemisphere, the remaining hemisphere is able tofunction normally, but it is doubtful whether it canbe called 'normal' function: 'supernormal' might bemore appropriate. For not only does it performmotor and sensory functions for both sides of thebody, it performs the associative and intellectualfunctions normally allocated to two hemispheres.The remaining hemisphere is dominant with regardto speech, but it is not, as Krynauw suggested, the'minor' hemisphere which was removed, for 'minor'is conventionally used in relation to language, andcomprises a range of cognitive functions associatedwith pictorial, spatial, and non-verbal material. Itis more satisfactory to refer to normal left and righthemisphere functions, and to state that in theinfantile hemiplegic these are both mediated bythe remaining hemisphere. Following removal of theabnormal hemisphere, this double function is moreefficiently performed; but it is interesting to enquirewhether there appears to be a limit to the level whichit may reach. Our figures (Table III) for the intel-ligence quotients of the series of patients beforeoperation show a somewhat skewed distribution,with a preponderance of low values. This might beexpected, since in many patients cerebral functionwas grossly disorganized. The post-operative I.Q.s,though generally higher, show an even more skeweddistribution, with a greater number of individualsspread over the lower end of the range: this was alsofound in the cases quoted in the literature (Table I).However, a large part of the 'tail' at the lower endis associated with electrical disturbance (and there-fore, possibly, some cerebral damage) in the remain-ing hemisphere, as shown by the figures in Table X,

TABLE XINTELLECTUAL LEVEL AND E.E.G. RECORD

Post-operative E.E.G.

Post-operative I.Q. below 6060 and above

Normal

12

Abnormal(1, 2, or 3)

144

for which x2 = 12-17, P <0001. Although thenumbers are small, it seems likely that the distribu-tion of intelligence quotients may be 'normal', i.e.,more or less symmetrical, but limited to an averagevalue in the region of 60, and it may be postulatedthat this limitation is the result of both left and righthemisphere functions being undertaken by a singlehemisphere.

Moreover, our evidence suggests that this limita-

tion may bear particularly heavily upon language, asopposed to non-language, functions. This wouldperhaps be expected in cases of left hemisphere in-jury, in which the right hemisphere had to assumeunwonted language functions; but the data make itclear that relative language impairment is commonalso in cases of right hemisphere injury, if thisoccurred during infancy. It is not possible to stateprecisely the age at which the earliest languagefunctions are established, normally in the left hemi-sphere. Griffiths (1954) gives 10 months as theaverage age at which two words are used, 12 monthsfor three words, and 21 months for the shortestphrases. Probably the most satisfactory criterion foreach individual is the age at which he begins to usewords; and our results suggest that, while the transferof intellectual functions from the damaged hemi-sphere may be complete until that age, there is arestriction on the development of verbal intelligence,so that it does not reach the same level in the in-dividual as does non-verbal intelligence. It is knownthat verbal ability is often reduced in patients withepilepsy (Halstead, 1957); and it is also probablethat a part of the intellectual impairment shown byour patients may have been educational in origin.However, the relative verbal impairment persistedafter the removal of the damaged hemisphere, andthe post-operative increases, in the few patients whowere tested on a comprehensive scale (Table V), wasgreater on non-verbal than on verbal tests, suggestingthat neither epilepsy nor educational retardation aremaior factors in determining the verbal deficiency.

Further evidence against the suggestion that therelative verbal impairment is educational in originis the occurrence of dysphasia and associated 'lefthemisphere' disabilities, in cases of infantile damageto either hemisphere, in contrast to the absence ofspatial disorientation or other 'right hemisphere'signs. Dysphasia is not a consequence of neglectedschooling, and its frequent disappearance followinghemispherectomy emphasizes its origin in physio-logical disturbance. On the other hand, this relativeverbal impairment is not found invariably in everypatient with infantile hemiplegia. The numbers inthe operated series (Table VII) are not sufficientto establish the tendency, and an analysis of furtherunoperated cases had to be added (Table VIII) toconfirm the suggestion. This is in part due to therelative inaccuracy of the distinction between verbaland performance levels when the tests used were notexplicitly designed to provide this information. It isprobably also due to the inclusion in the groups ofcases in which the 'intact' hemisphere was also infact partly damaged, thus disturbing the expectedpattern of development; for example, our two casesof right-sided Sturge-Weber-Dimitri disease both

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EFFECTS OF HEMISPHERECTOMY ON INFANTILE HEMIPLEGIA

showed relative performance impairment, as did thepatient (Case 2) of Cairns and Davidson (1951).As stated in an earlier section, this demonstration

of limitation of verbal abilities disposes of thequestion of adjustment of right hemisphere func-tions: it appears that in cases of infantile injury toeither hemisphere these are adequately integrated inthe remaining hemisphere, together with left hemi-sphere functions. Although a few cases of infantileinjury have shown a relative deficiency on perfor-mance, as contrasted with verbal, tests, this has notamounted to the syndrome of spatial agnosia incontrast to the relatively frequent occurrence ofdysphasia in association with verbal deficiency.Apart from the association of specific types of

intellectual impairment with lesions in certaincerebral areas nothing is known of the neuro-physiological basis of intellectual functions in thetwo hemispheres. Consequently, little can be sur-

mized concerning the neurophysiological organiza-tion which underlies the execution of the functionsof both hemispheres by one hemisphere alone.Whether these functions are distributed in the sameantero-posterior locations in the one hemisphere as

they would be in their normal hemispheres, whetherthey occupy relatively discrete regions, or are

closely intermingled with other 'contralateral' func-tions, these cannot be guessed at. Evidently there isa suggestion that some sort of quantitative limit tothe capacity of cerebral tissue has been reached. Theaverage intelligence of our patients is well below thenormal average; even minor electrical abnormalitiesin the remaining hemisphere are associated withlower I.Q.s, and there is a tendency, even in thoseapproaching normal I.Q.s, for verbal ability to bereduced, suggesting that this normally requires a

greater number of neurones for its expression thando 'non-verbal' performances. Otherwise, it can

only be observed that these patients are repositoriesof cerebral organizations of the greatest interest,further understanding of which will amply repay themost detailed follow-up study.

SummaryA review of published reports suggests that greater

improvement in cases of infantile hemiplegia resultsfrom complete hemispherectomy than from partialremoval. In cases of injury to the left hemisphere,removal has rarely resulted in speech disturbance,and the majority of reports show a rise in intellectuallevel following removal of either hemisphere.Comparison of test scores of a series of 28 cases

of hemispherectomy with nine of partial removaldemonstrates a significantly greater increase inscores in the former group. Taking the cases ofhemispherectomy alone, this increase is found to beexclusively in the patients with infantile hemiplegiain the strict sense, i.e., with injuries sustained in thefirst year.

There is no significant difference in post-operativeincrease in scores between cases of left and righthemispherectomy in the infantile injury group.Analysis of results shows that greatest improvementis on those patients with normal E.E.G.s in theremaining hemispheres. It is also demonstrated thatthe majority of patients with infantile hemiplegiashow a verbal intellectual deficit, amounting in somecases to dysphasia, irrespective of hemispheredamaged.

It is suggested that these results indicate a limit tothe capacity of the remaining hemisphere, imposedby the mediation of the normal functions of bothhemispheres by one hemisohere alone.

I am indebted to Mr. Wylie McKissock and Dr. E. A.Carmichael for the interest they have shown in thisstudy, to Dr. E. A. Cobb for the E.E.G. reports and Dr.W. P. G. Mair for the pathological reports, and to Mr.C. V. Jackson and Mrs. E. Warrington, who tested anumber of the patients. I am particularly grateful toDr. P. W. Nathan and Dr. G. E. Ettlinger for theirvaluable criticism of the draft of this paper.

REFERENCESAchslogh, J., and Ectors, L. (1954). Acta. neurol. belg., 54, 457.Cairns, H., and Davidson, M. A. (1951). Lancet. 2, 411.Dandy, W. E. (1928). J. Amer. med. Ass., 90, 823.Diven, K. (1934). Amer. J. Psychol., 46, 500.French, L. A., Johnson, D. R., Brown, I. A., and Van Bergen, F. B.

(1955). J. Neurosurg., 12, 154.Gardner, W. J. (1932). Arch. Neurol. Psychiat. (Chicago), 28, 470.

Karnosh, L. J., McClure, C. C., and Gardner, A. K. (1955).Brain, 78, 487.

Griffiths, R. (1954). The Abilities of Babies. University of LondonPress, London.

Halstead, H. (1957). J. ment. Sci., 103, 28.Hillier, W. F. (1954). Neurology, 4, 718.Krynauw, R. A. (1950). J. Neurol. Neurosurg. Psychiat., 13, 243.Laine, E., Fontan, W., Delandtsheer, M., and Delandtsheer (1951).

Rev. neurol., 85, 489.McFie, J. (1960). J. nerv. ment. Dis., 131, 383.- and Piercy, M. F. (1952). Brain, 75, 292.McKissock, W. (1953). Proc. roy. Soc. Med., 46, 431.

(1954). Zbl. Neurochir., 14, 42.Marshall, C., and Walker, E. A. (1950). Electroenceph. clin. Neuro.

physiol., 2, 147.Mensh, I. N., Schwartz, H. G., Matarazzo, R. G., and Mattarazzo,

J. D. (1952). A.M.A. Arch. Neurol. Psychiat., 67, 787.Obrador, Alcalde, S. (1951). Arch. Neuro-psiquiat. (S. Paulo), 9, 191.Perlstein, M. A., and Sugar, 0. (1954). A.M.A. Arch. Neurol. Psychiat.,

72, 256.Rowe, S. N. (1937). Amer. J. Psychiat., 94, 605.Uecker, A. E., French, L. A., and Johnson, D. R. (1954). A.M.A.

Arch. Neurol. Psychiat., 72, 555.Wechsler, D. (1944). The Measurement of Adult Intelligence, 3rd ed.

Williams and Wilkins, Baltimore.Williams, D. J., and Scott, J. W. (1939). J. Neurol Psychiat., 2, 313.Zollinger, R. (1935). Arch. Neurol. Psvchiat. (Chicago), 34, 1055.Zulch, K. J. (1954). Zbl. Neurochir., 14, 48.

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