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Handedness in Relation to Direction and Degree of Cerebral Dominance for Language
HANDEDNESS IN RELATION TO DIRECTION AND DEGREE OF CEREBRAL DOMINANCE FOR LANGUAGE
w.
A. Lishman and E. R. L. McMeekan
(Institute of Psychiatry, University of London)
INTRODUCTION
Many sources of evidence combine to suggest that the usual patterns of hemispheric dominance for language are disturbed in a proportion of nonright handed individuals. Thus while the great majority of right handers show left hemisphere dominance for language this appears to apply in only two-thirds to three-quarters of left handers. The evidence has come from studies of the effects of unilateral cerebral lesions (Zangwill, 1960; Piercy, 1964; Hecaen and Sauguet, 1971), from investigating the effect of intracarotid amy tal injections (Milner, Branch and Rasmussen, 1964, 1966) or of administering electroshock to either hemisphere alone (Warrington and Pratt, 1973). Dichotic listening experiments applied to healthy volunteer subjects have often given a similar distribution (Satz, Achenbach, Patti shall and Fennell, 1965; Dee, 1971; Kimura, 1973). But further complexities have proved to underlie this situation. There are indications that dominance for language functions may be less securely established in left handers and ambidexters than in pure right handers. A family history of sinistrality has sometimes emerged as significant in relation to patterns of dominance, likewise the strength and consistency of left hand preference in the individual. These issues are, however, open to conflicts of evidence. With regard to insecure dominance, dysphasia has been found to be milder and with a better prognosis among sinistrals than dextrals regardless of the hemisphere damaged, thus suggesting a degree of cerebral bilaterality for speech in a considerable number of left handed subjects (Subirana, 1958; Zangwill, 1960; Luria, 1970; Hecaen and Sauguet, 1971). Similarly Hecaen and Piercy (1956) found a higher incidence of dysphasic phenomena in the auras of non-right handed than right handed epileptics, no matter on which side the epileptogenic discharge originated. Carotid amy tal injections, as a means of determining language laterality in epileptics, have shown disruption Cortex (1977) 13, 30·43.
Handedness and cerebral dominance for language
31
of speech from either side in 15 per cent of left handers or ambidexters compared to 1 per cent of right handers (Milner et al., 1966). In the nonright handers, moreover, the language disturbances produced were usually slight and short lived. The clinical evidence is not, however, uniform. Russell and Espir (1961), studying circumscribed brain wounds, found that the incidence of dysphasia was no higher in sinistrals than dextrals when left and right brain lesion cases were added together, as would have been expected if the left handers had had bilateral speech representation. Similarly in a study of missile wounds of the brain Newcombe and Ratcliff (1973) were unable to detect significant differences in the residual language deficits of dextrals and sinistrals, and there was no indication of speedier recovery from dysphasia in the sinistrals in the early acute stages. The evidence from dichotic listening tests on healthy subjects has usually been interpreted as supporting lessened language lateralization in left handers, by the demonstration of reduced perceptive asymmetry between the ears in sinistrals as compare to dextrals (Satz, Achenbach, Patti shall and Fennell, 1965; Satz, Achenbach and Fennell, 1967; Curry, 1967; Curry and Rutherford, 1967). Tachistoscopic tests of verbal recognition in right and left half fields of vision have also given similar results (Zurif and Bryden, 1969). However, as discussed below the dichotic and tachistoscopic data on this issue may to some extent beartefactual owing to the manner in which the data are analysed and presented. The influence of a family history of sinistrality has been studied in various ways. Hecaen and Sauguet (1971) found that in familial left handers disturbances of oral language and of reading occurred with similar frequency following either right or left-sided lesions, whereas in non-familial left handers these disturbances were very rarely seen with right sided lesions. Right hemisphere dominance for language, or cerebral bilaterality, thus appeared to characterise familial left handers alone. Newcombe and Ratcliff (1973), however, in a much smaller group of patients with missile wounds, found trends in the opposite direction, similarly Warrington and Pratt (1973) studying the effects of ECT. Dichotic and tachistoscopic testing in healthy individuals has sometimes indicated a higher proportion of left handers with right hemisphere dominance when the family history is positive (Bryden, 1965; Zurif and Bryden, 1969), but occasionally the reverse has emerged (Curry, 1967, Satz et aI., 1967). Zurif and Bryden (1969) further interpreted their data as indicating that familial left handers showed greater hemispheric equipotentiality as well as being more variable with regard to side of dominance for language. The strength and consistency of left handedness has been explored with directly contradictory results. Thus Satz et al. (1967) found indications of
32
W. A. Lishman and E. R. L. McMeekan
right hemisphere dominance in a much higher proportion of strong sinistrals than of weak sinistrals, whereas Dee (1971), also using dichotic tests, found the reverse. How far differences in criteria for strength of handedness, ot differences in techniques of dichotic testing can explain such discrepancies is unclear. Lesional studies (Hecaen and Sauguet, 1971) and studies of unilateral electroshock (Warrington and Pratt, 1973) have failed to reveal any clear differences between strength of left handedness and patterns of dominance. All of the above has attracted detailed attention because of the growing interest in patterns of cerebral organisation, and the recognition that in many respects left handers are liable to prove exceptions to the rule. Clearly, however, left handedness is not a unitary concept and this may be a principal source of many of the discrepant findings in the literature outlined above. Hand preference has been shown to be a graded characteristic, extending from pure left handedness for multiple tasks and skills through various grades of "ambidexterity" or "mixed handedness" to the common pattern of pvre right handedness (Annett, 1970; Olfield, 1971). Moreover the factors which contribute to hand preference appear to be multiplegenetic influences of uncertain operation, cultural pressures to adopt the usual dextral pattern, and the effects of minimal brain dating from early life. The nature of the left handers and ambidexters included in a given sample will therefom often differ considerably from one investigation to another. Thus it has seemed worthwhile to examine the relationships between handedness and cerebral dominance anew, controlling as far as possible for the variables likely to be of significance in the non-right handed population. A series of healthy subjetcs has been recruited and their hand preference patterns charted by the method established by Annett (1970). A special effort has beeu made to obtain pure left handed and mixed handed volunteers, corresponding to the criteria laid down by Annett, so that adequate comparisons could be made with pure right handers. By restricting recruitment to healthy per~()ns of above average intelligence we have hoped to minimise the likelihcood of pathological left handedness resulting from covert brain damage in earl)' life. The presence or absence of a family history of sinistrality has been determined in all subjects. Dichotic listening has been employed as the indicator of cerebral dominance since the technique may readily be applied to healthy volunteers. It has shown to correlate reasonably well with the results of cerebral dominance as determined byintracarotid amy tal injections (Kimura, 1961), and to show in general a parallel with other lines of evidence regarding the proportion of subjects who are right or left dominant for language (Roberts, 1969). It has also the advantage of perhaps indicating something of the degree as well as the direction of lateralization of language functions.
Handedness and cerebral dominance for language
33
MATERIALS AND METHODS
Subjects The subjects were recruited from the staff of the Institute of Psychiatry and the Maudsley HospitaL Special efforts were made to obtain left handed or ambidextrous subjects, and recruitment continued until the three principal groups of left, right and mixed handers (see below) were reasonably well represented and with an approximately equal number of males and females in each group.
Procedure Hand preference was examined by means of Annett's (1970) questionnaire. This consists of questions about the hand preferred for twelve activities, six of which are designated "primary" (in brief writing, throwing, using a racket, striking a match, hammering, and using a toothbrush) and six are designated" secondary" (use of scissors, threading a needle, hand at top of broom, at top of shovel, dealing cards and unscrewing the lid of a jar). The distinction between primary and secondary items was arrived at by Annett by a process of association analysis on data gathered from over 2000 individuals, allowing an assessment of which items cluster most closely together in a normal population. A number of separate handedness categories were thus established, representing mutually exclusive classes on a continuum from pure right handedness through various grades of mixed handedness to pure left handedness. The groupings were then further validated against a test of manual speed. The number of individuals in several of these categories proved to be very small, but a useful classification, recommended by Annett, involves distinctions based on the primary questions alone and this has been used in the present study. Subjects who state right preference for all six of the primary questions have been designed "strong right handers," and subjects who consistently state left preference for all six are designated "strong left handers." Subjects who showed any admixture of preferences for the six primary questions were designated "mixed handers". For inclusion in this group it was necessary for the subject to have shown a clear anomalous preference for one (or more) of the primary actions; claims to equal facility with the hands on individual items did not suffice. The mixed handed group can, of course, be subdivided according to the hand used for writing, yielding "right mixed" and "left mixed" sub-categories. The incidences of these main categories in Annett's normal standardisation population were approximately 86 per cent" right handed" (Classes 1 to 4 of Annett), 7 per cent "mixed handed" (Classes 5 and 6 of Annett) and 7 per cent "left handed" (Classes 7 and 8 of Annett), with "mixed handers" consisting approximately equally of "left mixed" and "right mixed." The dichotic listening test involved delivering pairs of words simultaneousl) to the two ears of the subject via earphones connected to an Akai 4000 stereophonic tape recorder. Monaural presentations were first carefully balanced to ensure subjective equality on the right and left ears. Any subject who showed impaired hearing in either ear was not utilized further. A practice period then followed for familiatization with the dichotic procedure.
. w.
34
A. Lishman and E. R. L. McMeekan
In the definitive test words were delivered in groups of three pairs at halfsecond intervals, each group being followed by a fifteen second pause during which the subject reported what he had heard. The tape contained 20 sets of triplets, i.e. 60 words delivered to the left ear and 60 delivered synchronously to the right ear. The words were all common monosyllabic words consisting of consonant-vowelconsonant. In testing each subject the tape was played through twice, interchanging the headphones between ears for the second delivery in order to allow for any channel differences which might have been built into the construction of the tape. Thus the maximum score obtainable at either ear was 120 words correctly reported. Subjects were not constrained as to ear order of report, but merely asked to repeat in any way they chose the words heard after each presentation of triplets. The score allotted to an individual on the test was computed as the percentage ratio of the difference in absolute scores between the ears to the total score obtained at both ears.' This method was adopted in preference to simple ear difference scores in order to yield scores which would be better comparable between one subject and another. Thus a subject who obtained 90 words at the right ear and 60 at the left has obviously shown a l~ss striking ear difference than a subject who obtained 60 words at the right ear and 30 at the left. Absolute ear difference scores would in both instances be 30, but with the present formula the first subject would score 20 and the second 33.3. Manual dexterity was separately tested in each subject by a pursuit rotor task using Jhe apparatus described by Wyke (1968). This consisted of three 1 cm equidistant targets mounted near the edge of a circular metal disc 12 cm in diameter. A turntable revolving on top of the disc at 46 revolutions per minute was designed to uncover only one target at a time, and the subject was required to touch each of the targets successively with an electric stylus as it appeared to view. Successful contact with targets closed an electric circuit and activated a counter, thus measuring the number of successes (" hits") during a test period. Contact with any other part of the apparatus activated another counter recording false attempts or "misses." After one 30-second practice period with each hand performance was measured over three test trials of 30 seconds each with each hand. The total possible score for hits with either hand was therefore approximately 200. Scores were computed as the percentage ratio of the difference in hand scores to their total. Computations were made separately for hits and misses.
RESULTS
Forty-two volunteers, 22 female and 20 male, were eventually obtained and tested, ranging in age from 18 to 56. Twenty-two used the right hand for writing and 20 the left. When subdivided as described above 15 were strong right handers, 12 mixed and 15 strong left handers. Table I shows that the average age, male/female ratio and overall performance on the dichotic test was similar in all subgroups. Altogether x-v
=
, i.e. - - X 100, where x total number of words correctly reported from the better x+y performing ear, and y = total number of words correctly reported from the poorer performing ear.
.35
Handedness and cerebral dominance for language TABLE I
Performance on Dichotic Testing in Subgroups
Ave. total score on dichotic test
Females/
All subjects Females Males Right handed for writing Left handed for writing Strongly right handed Mixed handed* Strongly left handed
Number
Males
42 22 20 22 20 15 12 15
22/20
13/9 9/11 7/8 7/5 8/7
Ave. age
Proportion with superior performance at left ear 23.8% 27.3% 20.0% 13.6% 35.0% 0 33.3%** 40.0%
104.1 103.9 104.3 103.5 104.8 104.8 99.8 106.7
32.5 33.4 31.5 33.8 31.1 30.7 34:1 33.0
* 6 females and 1 male "right mixed," i.e, used right hand for writing. males "left mixed," i.e. used left hand for writing. ** 42.9% of right mixed, 20.0% of left mixed.
1 females and 4
23.8 per cent of subjects have shown better performance ort the left than right ear, indicative of right hemisphere dominance for speech perception. The proportion is markedly higher when the left rather than the right hand is used for writing. In the three groups at the bottom of the table the proportion with left ear superiority increases progressively with increasing left hand preference (0 in strong right handers, 33.3 per cent in mixed handers, and 40 per cent in strong left handers). Table II shows the dichotic ratio scores, calculated for each individual TABLE II
Dichotic Ratio Scores in Subgroups
Mean dichotic. ratio scores (xx Ignoring whether Lor R ear superior All subjects Females Males Right handed for writing Left handed for writing Strongly right handed Mixed handed Strongly left handed
28.5 31.8 24.9 30.3 26.6 25.3 38.4* 23.9
* Right mixed = 40.9, Left mixed = 34.9.
+~ y
Right ear superior 28.0 33.2 22.8 28.6 27.2 25.3 39.2 22.6
(N = (N = (N = (N = (N = (N = (N = (N =
32) 16) 16) 19) 13) 15) 8) 9)
X 100 - see text) Left ear superior 30.2 28.2 33.3 41.0 25.6
(N = (N= (N= (N = (N =
10) 6) 4) 3) 7)
37.0 (N = 4) 25.7 (N = 6)
W , A. Lishman and B. R. 1. McMeekan
then averaged for each subgroup. The ratio scores do not show any consistent tendency for inter-ear differences to be smaller in subjects showing left ear superiority than in subjects showing right ear superiority. In fact, though numbers in subgroups are mostly very small, the reverse tendency often appears to obtain. Thus the data provide no support for the idea that subjects·· who are right brained for language functions (as measured by dichotic. listening) show a lessened degree of lateralization, or greater hemispheric equipotentiality, when compared to subjects who are left brained for .language functions. The differences in ratio scores between males and females, though sometimes considerable, are not statistically significant on t-test comparisons. Right handers who are right brained for language show larger ratio scores than left handers who are right brained for language (41.0 compared to 25.6) but again the difference is not · statistically significant. When strongly right handed, mixed handed and strongly left handed subjects are compared the left handers obtain scores which are very similar to the right handers, no matter whether they are right or left ear preferent . .Thus there iSn9 indication that hemispheric dominance is less securely est;tblished in left handers than 'ih right handers. The mixed handers show 'considerably Jarger ratio scores ihan the other groups. This applies whether the.mixedhanders are left or right brained for speech .. Thus the data provide no support 'f or the ldea that~mhjects with mixed hand preference patterns show a .greater tendency than other groups towards "bilateral speech representation"; indeed they appear to. show more marked lateralization of speech than either the right or left handed subjects as judged by the dichotic listening task. However none of the differences between ambidexters and other groups proved to be statistically significant on t-test comparisons. Fainili~l sznistrality
A farilily history of sinistrality was obtained in 16 subjects, representing rather more than half of the females (12) and one-fifth of the males (4). Familial sinistrality was .charted only when a parent or full sibling of the subject was declared to be left handed (or in three cases ambidextrous, one each in the strongly right handed, mixed handed, and strongly left handed gr01-lps).Table III shows the dichotic ratio scores when the subjects are so divided. Left ear superionty, indicative of right brainedness for language, is seen to be commoner in' the pr~sence of a family history of sinistrality only amo,ng s.trongly left handed subjects (50.0 per cent compared to 33.3 per cent). A,mong mixed handed subjects the reverse is obtained. All males and all dextral writers who were right brained for language proved to be without a family history of sinistrality.
Handedness and cerebral dominance for language
37
TABLE III
Dichotic Ratio Scores in Relation to Familit;zl.Sinistrality
Subjects without familial sinistrality No. All subjects Females Males Right handed for writing Left handed for writing Strongly right handed Mixed handed Strongly left handed
26 10
16 15 11 10 7 9
% with . Dichotic left ear ratio superiority scores*
26.9 30.0 25.0 20.0 36.4 57.1 33.3
29.5 37.5 24.4 30.3 28.3 24.4 36.7 29.5**
Subjects with familial sinistrality No. 16 12 4 7 9 5 5 6
% with Dichotic left ear ratio superiority scores
18.8 25.0
33.3
50.0
27.0 27.1 27.0 30.2 24.6 27.1 40.9 15.4**
* Ignoring whether left or right ear superior. ** t = 2.34, d.£. = 13, p < 0.05.
With regard to the size of dichotic ratio scores a family history of sinistrality is seen to be associat~d with reduced ratio scores among the females (27.1 compared to 37.5) and among the left handers (24.6 compared to 28.3), though in neither case is the difference statistically significant. In the lower part of the table it can be seen that among the sttongly left handed subjects familial sinistrality is associated with markedly smaller ratio scotes (15.4 compared to 29.5) and here the difference is statistically significant (p < 0.05). In fact by fat the majority of strongly left handed subjec~swith familial sin.istrality were female (5 out of 6, compared to 3 out of9i itf the group without familial sinistrality), thus accounting for the finding in females generally earlier in the table. Table IV shows that familial sinistrality in strongly left handed subjects is associated with reduced ratio scores whether the subjects have shown a right or a left ear preference on dichotic testing. Manual skill The pursuit rotor test of manmlI skill was carried out on 39 of the 42 subjects. Table V shows the range and means of the hand skill ratios when subjects are divided into three equal sized groups 'on the basis 6£ relative manual skill. Results are shown both for "hits" an.d Iitriisses" on the task. The table also shows the reclassifications involved when skill groupings are compared to the hand preference groupings derived from Annett's question~ naire. In all subjects the hand used for writing proved to be the more skilled on the pursuit rotor task, ils might' he expected. But the tripartite
W. A. Lishman and E. R. L. McMeekan
38
TABLE IV
Dichotic Ratio Scores in Strongly Left Handed Subjects in Relation to Familial Sinistrality
Subjects with familial sinistrality
Subjects without familial sinistrality No.
Dichotic ratio scores
No.
= 14.1)
3
15.5* (S.D.
= 8.2)
=
3
15.3** (S.D.
= 4.5)
Strongly left handed subjects with right ear superiority
6
26.2*
Strongly left handed subjects with left ear superiority
3
36.1** (S.D.
(S.D.
4.6)
Dichotic ratio scores
* t = 1.08, d.f. = 7, p> 0.05. t = 4.43, d.f. = 4, p < 0.02.
**
TABLE V
Subdivisions of Subjects According to Relative Manual Skill
Hand preference groups
Mean hand* difference ratios
Range
Female/ Male
6.7 0.3 -S.l
14.S to 2.6 2.5 to -3.0 -3.4 to -19.S
7F,6M 7F,6M 5F, SM
40.1 Pursuit } Right Skilled Intermediate -6.0 motor misses Left skilled -5S.6
66.3 to 2S.6 27.2 to -39.S ~42.2 to -79.5
6F,7M 9F,4M 4F,9M
Pursuit ) Right """'" Intermediate rotor hits Left skilled
Strong Mixed Strong right handed left handed handed 9
5
4 6 2
9
4
5
5
3
2
11 3 10
., R-L ... L-R For purSUlt rotor hits calculated R+L X 100 and for pursUlt rotor misses .,!{+L_ X lOC where R = score with right hand and L = score with left hand. Thus in· both cases positiv scores indicated superior performance with the right hand, and negative scores superic performance with the left hand.
*
divisions on hand. skill scores have led to a number of interchanges betwee the extreme hand preference groups and the mixed handed group. Nor at the groupings according to pursuit rotor hits and misses entirely congruen1 fot example only 6 of the 9 subjects in the "right skilled" groups are t1 same individuals where hits·· and misses are concerned. Table VI shows the proportion of subjects in each manual skill grou who showed left ear preference (i.e., right brainedness) on dichotic testin also the size of the dichotic ratio scores obtained. The proportion showir left ear preference increases fairly regularly with an increasing degree .1
39
Handedness and cerebral dominance for language TABLE VI
Dichotic Rotio Scores in Relation to Manual Skill
Proportion with superior performaFlce at left ear
) ru~, Pursuit
Ignoring whether left or right ear superior
Subjects with right eat superior
Subjects with left ear superior
23 .9 (N = 11) 35.9 (N = 11) 21.9 (N = 9)
19.4 (N=2) 59.4 (N = 2) 30.0 (N = 4)
24.8 (N::=: 12) .31.2 (N = 11) 26.6 (N = 8)
12.7 (N= 1) 55.0 (N = 2) 30.9 (N= 5)
~
15.4%
23.2
Intermediate
15.4%
39.5
\ Left skilled
30.8%
24.3
Ri~' ,kill'"
7.7%
23 .9.
Intermediate
15.4%
34.9
Left skilled
38.5%
28.2
rotor hits
Pursuit to.tOt ffilsses
Dichotic ratio scores
)
left hand skni, though in a rather less clear cut fashion than was observed in relation to manual preference patterns (in Table I). ':the degree or language lateralization as judged from dichotic ratio scores closely re~embles the results in Table II - thus left manual skill, like left manual preference, is not associated with diminution in the size of the dichotic ratio s~ores; and intermediate skill, like the mixed preference pattern, tends to be associated with augmented ear difference scores. When the direction of ear preference is considered there is no indication that left ear preference (right hemisphere dominance) is less securely established than ' right ear preference either among intermediate or left skilled subgroups. The results obtained in relation to m'anual skill when i family 'history of sinistrality is taken into account are not presented, budn general followed the patterns observed in the 'manual preference groups. as s!imvn in Tables III and IV. DISCUSSION
The results show that cerebral domina~ce for language, as inferred from dichotic testing, tends more often to lie with the right hemisphere in mixed handers than in strong right handers, and more often still in strong left handers. The incidence in strong left handers (40 per cent) is rather higher than in many other studies, perhaps as a result of the strict criteria used for inclusion in this group. No individual classified as a strong right hander has proved to show right hemisphere dominance. Other surveys using dichotic
40
W . A. Lishman and E. R. L. McMeekan
listening have often found such examples (Dee, 1971 = 17 per cent; Zurif and Bryden, 1969 = 10 per cent; Kimura, 1973 = 18 per cent; Satz et aI., 1965 = 11.5 per cent). Here, however, the strict criterion of consistent right preference on all six of Annett's primary questions has been required for inclusion in the strong right handed group. If the hand used for writing had been the sole criterion for designating right handedness we would have obtained 13.6 per cent of right handers with right hemisphere dominance. Of perhaps some interest is the finding that 3 out of 7 (43 per cent) of the mixed handers who wrote with the right hand (i.e., left preferent for one or more of Annett's primary questions even though writing with the right hand) have shown indications of right hemisphere dominance. Though numbers are very small this is a similar proportion to that found with strong left handers. It is possible that these individuals represent cultural shift towards using the right hand for writing in persons who were otherwise destined to be strong left handers. An important finding is that left handers and mixed handers do not show reduced ear asymmetries when compared to right handers. If anything the trend is for mixed handers to show considerably larger ear differences than strong right or strong left handers. Nor do individuals with indications of right hemisphere dominance show lessened ear asymmetry than individuals with left hemisphere dominance - the size of the ear differences corresponds closely, only the direction of ear preference ' is reversed. Subdivisions of the material according to relative manual skill on a pursuit rotor task show similar findings. Females in general have shown larger ear difference scores than males when left hemisphere dominant, but the above results do not depend ' on sex imbalance in the principal subgroups. A family history of sinistrality is, however, associated with significantly reduced ear difference scores. This applies only in strongly left handed subjects, not in mixed handed or right handed subjects. The smaller ear asymmetry in left handers with sinistral relatives applies whether they are left or right hemisphere dominant. The present data have been able to demonstrate this clearly in females only. These findings may be viewed in relation to other studies. The clinical evidence suggesting bilateral speech representation in non-right handers must be viewed with caution for a number of reasons. Lesional studies suffer from uncertainties with regard to the size of the responsible lesions and the extent of anatomical involvement of the language areas of the hemispheres. Work on epileptics suffers from possible contaminating effects due to early brain damage which may have encouraged transfet or diffusion of language functions to the opposite hemisphere of the brain. Pre~ious work involving dichotic listening deserves closer scrutiny here.
Handedness and cerebral dominance for language
41
Satz et a1. (1967) reported smaller ear asymmetries in sinistrals than dextrals, but presented only group means for errors on the left and right ears. Their group mean differences are certainly much smaller in sinistrals than dextrals, when mean left ear errors are subtracted from mean right ear errors, but this would be expected since a much larger proportion of the former than the latter had performed better on the left ear than the right. Others present their data in a manner which avoids this difficulty, and display smaller absolute ear difference scores in sinistrals than dextrals (Satz et aI., 1965, Curry, 1967; Curry and Rutherford, 1967), but none of these workers have analysed their results in relation to the presence or absence of a family history of sinistrality. Zurif and Bryden (1969) do examine familial and non-familial sinistrals separately, and compare them with dextrals on a number of dichotic and tachistoscopic tests. The non-familial sinistrals have dichotic (and tachistoscopic) difference scores of similar magnitude to dextrals, but the familial sinistrals show very small ear or half field differences. However only group mean scores for each ear or half field are given, so it is hard to know whether or not the findings are entirely analogous to our own. Thus the present data do not support the idea of "weak dominance" or "bilateral speech representation" or "hemispheric equipotentiality" among the generality of sinistrals or ambidexters as has often been proposed. Such statements would seem applicable only to strong lefthanders with a family history of sinistrality. These conclusions do not appear to be at direct variance with other reported studies when one takes into account the methods used for presenting results and when one notes that a family history of sinistrality has not always been recorded in previously published work. The present results must, of course, be viewed with caution since dichotic listening tests are no more than indirect and approximate indicators of cerebral dominance. .In particular they can give indications of receptive language functions only and do not necessarily reflect the neural organisation subservingexpressive aspects of language. Our data, indicating welliateralized ear preferences in nonright handers, do not therefore necessarily countermand the evidence from lesional and amy tal studies discussed above - it is possible that well lateralized receptive functions may yet co-exist with bilateral cerebral representation for expressive language. In this connection it should be noted, however, that studies of left hemispherectomised and callosal sectioned patients suggest the reverse, viz. that receptive functions are more liable to be organised bilaterally than expressive functions (Smith, 1966; Gazzal1iga and Sperry, 1967; Sperry and Gazzaniga, 1967; Zangwill, 1967). Unfortunately we lack a method for exploring the lateralization of expressive language functions in a normal volunteer population with which to attempt to resolve this dilemma.
W. A. Lishman and E. R. L. McMeekan
42
SUMMARY
In so far as ear asymmetries on dichotic listening reflect cerebral dominance for language, the present evidence indicates a progressively decreasing incidence of left hemisphere dominance in right handed, mixed handed and left handed individuals. In the absence of a. family history of sinistrality there are no indications that the degree of dominance is reduced in left handers or mixed handers when compared to right handers, nor that right hemisphere dominance is less securely established than left hemisphere dominance. Among strong left handers with a family history of sinistrality, however, ear difference scores are significantly smaller, indicating reduced lateralization or bilateral representation of language in such individuals. This applies equally in left dominant and right dominant left handers.
Acknowledgments. This work was supported by a grant from the Medical Research Council, which is gratefully acknowledged. We are indebted to the many volunteer subjects who took part, and to Mr. Peter Nicholls for statistical advice.
REFERENCES ANNETT, M. (1970) A classification of hand preference by association analysis, "Brit. J. Psychol.," 61, 303-321. BEAUMONT, J. G. (1974) Handedness and hemispheric function, in Hemisphere Function in the Human Brain, ed. by S. J. Dimond and J. G. Beaumont, Elek Science, London. BRYDEN, M. P. (1965) Tachistoscopic recognition, handedness, and cerebral dominance, "Neuro. psychologia," 3, I-B. CURRY, F. W. K. (1967) A comparison of left handed and right handed subjects on verbal and non-verbal dichotic listening tasks, "Cortex," 3, 343-352. - , and RUTIlERFORD, D. R. (1967) Recognition and recall of dichotically presented verbal stimuli by right and left handed persons, "Neuropsychologia," 5, 119-126. DEE, H. L. (1971) Auditory asymmetry and strength of manual preference, "Cortex," 7, 236-245. GAZZANIGA, M. S., and SPERRY, R. W. (1967) Language after section of the cerebral commissures, "Brain," 90, 131-14B. HtCAEN, H., and PIERCY, M. (1956) Paroxysmal dysphasia and the problem of cerebral dominance, "J. Neurol. Neurosurg. Psychiat.," 19, 194-201. - , and SAUGUET, J. (1971) Cerebral dominance in left handed subjects, "Cortex,". 7, 19-4B. KIMURA, D. (1961) Cerebral dominance and the perception of verbal stimuli, "Canad. J. Psychol.," 15, 166-171. (1973) Manual activity during speaking. II: Left handers, "Neuropsychologia," 11, 51-55. LURIA, A. R. (1970) Traumatic Aphasia: Its Syndromes, Psychology and Treatment, Mouton, The Hague. MILNER, B., BRANCH, and RASMUSSEN, T. (1964) Observations on cerebral dominance, in Disorders of Language, ed. by A. V. S. De Reuck and M. O'Connor, Ciba Found. Symp., Churchill, London. - , - , - (1966) Evidence for bilateral speech representation in some non-right handers, "Trans. Amer. Neurol. Ass.," 91, 306-30B. NEWCOMBE, F., and RA.TCLIFF, G. (1973) Handedness, speech lateralization and ability, "Neuropsychologia," 11, 399-407. OLDFIELD, R. C. (1971) The assessment and analysis of handedness: The Edinburgh Inventory, "Neuropsychologia," 9, 97-113. PIERCY, M. (1964) The effects of cerebral lesions on intellectual function: a review of current research trends, "Brit. J. Psychiat.," 110, 310-352. ROBERTS, L. (1969) Aphasia, apraxia and agnosia in abnormal states of cerebral dominance, in Handbook of Qinical Neurology, Vol. 4, ed. by P. J. Vinken and G. W. Bruyn, North Holland Publishing Company, Amsterdam. RUSSELL, W. R., and ESPIR, M. L. E. (1961) Traumatic Aphasia, Oxford University Press.
c.,
Handedness and cerebral dominance for language
43
SATZ, P., ACHENBACH, K., PATTISHALL, E., and FENNELL, E. (1965) Order of report, ear asymmetry and handedness in dichotic listening, "Cortex," 1, 377-396. - , - , and FENNELL, E. (1967) Correlations between assessed manual laterality and predicted speech laterality in a normal population, "Neuropsychologia," 5, 295-310. SMITH, A. (1966) Speech and other functions after left (dominant) hemispherectomy, 'T Neurol. Neurosurg. Psychiat.," 29, 467-471. SPERRY, R. W., and GAZZANIGA, M. S. (1967) Language following surgical disconnection of the hemispheres, in Brain Mechanisms Underlying Speech Language, ed. by C. H. Millikan and F. L. Darley, Grune and Stratton, New York. SUBIRANA, A. (1958) The prognosis in aphasia in relation to the factor of cerebral dominance and handedness, "Brain," 81, 415-425. WARRINGTON, E. K., and PRATT, R. T. C. (1973) Language laterality in left handers assessed by unilateral ECT, "Neuropsychologia," 11, 423-428_ WYKE, M. (1968) The effect of brain lesions in the performance of an arm-hand precision task, "Neuropsychologia," 6, 125-134. ZANGWILL, O. L. (1960) Cerebral Dominance and its Relation to Psychological Function, Oliver and Boyd, Edinburgh_ (1967) Speech and the minor hemisphere, "Acta Neurol. Psychiat. Belg.," 67, 1013-1020. ZURIF, E. B., and BRYDEN, M. P. (1969) Familial handedness and left-right differences in auditory and visual perception, "Neuropsychologia," 7, 179-187.
Dr. W. A. Lishman and Miss E. R. L. McMeekan, Institute of Psychiatry, De Crespigny Park, London, SE5.
w.
A. Lishman and E. R. L. McMeekan
(Institute of Psychiatry, University of London)
INTRODUCTION
Many sources of evidence combine to suggest that the usual patterns of hemispheric dominance for language are disturbed in a proportion of nonright handed individuals. Thus while the great majority of right handers show left hemisphere dominance for language this appears to apply in only two-thirds to three-quarters of left handers. The evidence has come from studies of the effects of unilateral cerebral lesions (Zangwill, 1960; Piercy, 1964; Hecaen and Sauguet, 1971), from investigating the effect of intracarotid amy tal injections (Milner, Branch and Rasmussen, 1964, 1966) or of administering electroshock to either hemisphere alone (Warrington and Pratt, 1973). Dichotic listening experiments applied to healthy volunteer subjects have often given a similar distribution (Satz, Achenbach, Patti shall and Fennell, 1965; Dee, 1971; Kimura, 1973). But further complexities have proved to underlie this situation. There are indications that dominance for language functions may be less securely established in left handers and ambidexters than in pure right handers. A family history of sinistrality has sometimes emerged as significant in relation to patterns of dominance, likewise the strength and consistency of left hand preference in the individual. These issues are, however, open to conflicts of evidence. With regard to insecure dominance, dysphasia has been found to be milder and with a better prognosis among sinistrals than dextrals regardless of the hemisphere damaged, thus suggesting a degree of cerebral bilaterality for speech in a considerable number of left handed subjects (Subirana, 1958; Zangwill, 1960; Luria, 1970; Hecaen and Sauguet, 1971). Similarly Hecaen and Piercy (1956) found a higher incidence of dysphasic phenomena in the auras of non-right handed than right handed epileptics, no matter on which side the epileptogenic discharge originated. Carotid amy tal injections, as a means of determining language laterality in epileptics, have shown disruption Cortex (1977) 13, 30·43.
Handedness and cerebral dominance for language
31
of speech from either side in 15 per cent of left handers or ambidexters compared to 1 per cent of right handers (Milner et al., 1966). In the nonright handers, moreover, the language disturbances produced were usually slight and short lived. The clinical evidence is not, however, uniform. Russell and Espir (1961), studying circumscribed brain wounds, found that the incidence of dysphasia was no higher in sinistrals than dextrals when left and right brain lesion cases were added together, as would have been expected if the left handers had had bilateral speech representation. Similarly in a study of missile wounds of the brain Newcombe and Ratcliff (1973) were unable to detect significant differences in the residual language deficits of dextrals and sinistrals, and there was no indication of speedier recovery from dysphasia in the sinistrals in the early acute stages. The evidence from dichotic listening tests on healthy subjects has usually been interpreted as supporting lessened language lateralization in left handers, by the demonstration of reduced perceptive asymmetry between the ears in sinistrals as compare to dextrals (Satz, Achenbach, Patti shall and Fennell, 1965; Satz, Achenbach and Fennell, 1967; Curry, 1967; Curry and Rutherford, 1967). Tachistoscopic tests of verbal recognition in right and left half fields of vision have also given similar results (Zurif and Bryden, 1969). However, as discussed below the dichotic and tachistoscopic data on this issue may to some extent beartefactual owing to the manner in which the data are analysed and presented. The influence of a family history of sinistrality has been studied in various ways. Hecaen and Sauguet (1971) found that in familial left handers disturbances of oral language and of reading occurred with similar frequency following either right or left-sided lesions, whereas in non-familial left handers these disturbances were very rarely seen with right sided lesions. Right hemisphere dominance for language, or cerebral bilaterality, thus appeared to characterise familial left handers alone. Newcombe and Ratcliff (1973), however, in a much smaller group of patients with missile wounds, found trends in the opposite direction, similarly Warrington and Pratt (1973) studying the effects of ECT. Dichotic and tachistoscopic testing in healthy individuals has sometimes indicated a higher proportion of left handers with right hemisphere dominance when the family history is positive (Bryden, 1965; Zurif and Bryden, 1969), but occasionally the reverse has emerged (Curry, 1967, Satz et aI., 1967). Zurif and Bryden (1969) further interpreted their data as indicating that familial left handers showed greater hemispheric equipotentiality as well as being more variable with regard to side of dominance for language. The strength and consistency of left handedness has been explored with directly contradictory results. Thus Satz et al. (1967) found indications of
32
W. A. Lishman and E. R. L. McMeekan
right hemisphere dominance in a much higher proportion of strong sinistrals than of weak sinistrals, whereas Dee (1971), also using dichotic tests, found the reverse. How far differences in criteria for strength of handedness, ot differences in techniques of dichotic testing can explain such discrepancies is unclear. Lesional studies (Hecaen and Sauguet, 1971) and studies of unilateral electroshock (Warrington and Pratt, 1973) have failed to reveal any clear differences between strength of left handedness and patterns of dominance. All of the above has attracted detailed attention because of the growing interest in patterns of cerebral organisation, and the recognition that in many respects left handers are liable to prove exceptions to the rule. Clearly, however, left handedness is not a unitary concept and this may be a principal source of many of the discrepant findings in the literature outlined above. Hand preference has been shown to be a graded characteristic, extending from pure left handedness for multiple tasks and skills through various grades of "ambidexterity" or "mixed handedness" to the common pattern of pvre right handedness (Annett, 1970; Olfield, 1971). Moreover the factors which contribute to hand preference appear to be multiplegenetic influences of uncertain operation, cultural pressures to adopt the usual dextral pattern, and the effects of minimal brain dating from early life. The nature of the left handers and ambidexters included in a given sample will therefom often differ considerably from one investigation to another. Thus it has seemed worthwhile to examine the relationships between handedness and cerebral dominance anew, controlling as far as possible for the variables likely to be of significance in the non-right handed population. A series of healthy subjetcs has been recruited and their hand preference patterns charted by the method established by Annett (1970). A special effort has beeu made to obtain pure left handed and mixed handed volunteers, corresponding to the criteria laid down by Annett, so that adequate comparisons could be made with pure right handers. By restricting recruitment to healthy per~()ns of above average intelligence we have hoped to minimise the likelihcood of pathological left handedness resulting from covert brain damage in earl)' life. The presence or absence of a family history of sinistrality has been determined in all subjects. Dichotic listening has been employed as the indicator of cerebral dominance since the technique may readily be applied to healthy volunteers. It has shown to correlate reasonably well with the results of cerebral dominance as determined byintracarotid amy tal injections (Kimura, 1961), and to show in general a parallel with other lines of evidence regarding the proportion of subjects who are right or left dominant for language (Roberts, 1969). It has also the advantage of perhaps indicating something of the degree as well as the direction of lateralization of language functions.
Handedness and cerebral dominance for language
33
MATERIALS AND METHODS
Subjects The subjects were recruited from the staff of the Institute of Psychiatry and the Maudsley HospitaL Special efforts were made to obtain left handed or ambidextrous subjects, and recruitment continued until the three principal groups of left, right and mixed handers (see below) were reasonably well represented and with an approximately equal number of males and females in each group.
Procedure Hand preference was examined by means of Annett's (1970) questionnaire. This consists of questions about the hand preferred for twelve activities, six of which are designated "primary" (in brief writing, throwing, using a racket, striking a match, hammering, and using a toothbrush) and six are designated" secondary" (use of scissors, threading a needle, hand at top of broom, at top of shovel, dealing cards and unscrewing the lid of a jar). The distinction between primary and secondary items was arrived at by Annett by a process of association analysis on data gathered from over 2000 individuals, allowing an assessment of which items cluster most closely together in a normal population. A number of separate handedness categories were thus established, representing mutually exclusive classes on a continuum from pure right handedness through various grades of mixed handedness to pure left handedness. The groupings were then further validated against a test of manual speed. The number of individuals in several of these categories proved to be very small, but a useful classification, recommended by Annett, involves distinctions based on the primary questions alone and this has been used in the present study. Subjects who state right preference for all six of the primary questions have been designed "strong right handers," and subjects who consistently state left preference for all six are designated "strong left handers." Subjects who showed any admixture of preferences for the six primary questions were designated "mixed handers". For inclusion in this group it was necessary for the subject to have shown a clear anomalous preference for one (or more) of the primary actions; claims to equal facility with the hands on individual items did not suffice. The mixed handed group can, of course, be subdivided according to the hand used for writing, yielding "right mixed" and "left mixed" sub-categories. The incidences of these main categories in Annett's normal standardisation population were approximately 86 per cent" right handed" (Classes 1 to 4 of Annett), 7 per cent "mixed handed" (Classes 5 and 6 of Annett) and 7 per cent "left handed" (Classes 7 and 8 of Annett), with "mixed handers" consisting approximately equally of "left mixed" and "right mixed." The dichotic listening test involved delivering pairs of words simultaneousl) to the two ears of the subject via earphones connected to an Akai 4000 stereophonic tape recorder. Monaural presentations were first carefully balanced to ensure subjective equality on the right and left ears. Any subject who showed impaired hearing in either ear was not utilized further. A practice period then followed for familiatization with the dichotic procedure.
. w.
34
A. Lishman and E. R. L. McMeekan
In the definitive test words were delivered in groups of three pairs at halfsecond intervals, each group being followed by a fifteen second pause during which the subject reported what he had heard. The tape contained 20 sets of triplets, i.e. 60 words delivered to the left ear and 60 delivered synchronously to the right ear. The words were all common monosyllabic words consisting of consonant-vowelconsonant. In testing each subject the tape was played through twice, interchanging the headphones between ears for the second delivery in order to allow for any channel differences which might have been built into the construction of the tape. Thus the maximum score obtainable at either ear was 120 words correctly reported. Subjects were not constrained as to ear order of report, but merely asked to repeat in any way they chose the words heard after each presentation of triplets. The score allotted to an individual on the test was computed as the percentage ratio of the difference in absolute scores between the ears to the total score obtained at both ears.' This method was adopted in preference to simple ear difference scores in order to yield scores which would be better comparable between one subject and another. Thus a subject who obtained 90 words at the right ear and 60 at the left has obviously shown a l~ss striking ear difference than a subject who obtained 60 words at the right ear and 30 at the left. Absolute ear difference scores would in both instances be 30, but with the present formula the first subject would score 20 and the second 33.3. Manual dexterity was separately tested in each subject by a pursuit rotor task using Jhe apparatus described by Wyke (1968). This consisted of three 1 cm equidistant targets mounted near the edge of a circular metal disc 12 cm in diameter. A turntable revolving on top of the disc at 46 revolutions per minute was designed to uncover only one target at a time, and the subject was required to touch each of the targets successively with an electric stylus as it appeared to view. Successful contact with targets closed an electric circuit and activated a counter, thus measuring the number of successes (" hits") during a test period. Contact with any other part of the apparatus activated another counter recording false attempts or "misses." After one 30-second practice period with each hand performance was measured over three test trials of 30 seconds each with each hand. The total possible score for hits with either hand was therefore approximately 200. Scores were computed as the percentage ratio of the difference in hand scores to their total. Computations were made separately for hits and misses.
RESULTS
Forty-two volunteers, 22 female and 20 male, were eventually obtained and tested, ranging in age from 18 to 56. Twenty-two used the right hand for writing and 20 the left. When subdivided as described above 15 were strong right handers, 12 mixed and 15 strong left handers. Table I shows that the average age, male/female ratio and overall performance on the dichotic test was similar in all subgroups. Altogether x-v
=
, i.e. - - X 100, where x total number of words correctly reported from the better x+y performing ear, and y = total number of words correctly reported from the poorer performing ear.
.35
Handedness and cerebral dominance for language TABLE I
Performance on Dichotic Testing in Subgroups
Ave. total score on dichotic test
Females/
All subjects Females Males Right handed for writing Left handed for writing Strongly right handed Mixed handed* Strongly left handed
Number
Males
42 22 20 22 20 15 12 15
22/20
13/9 9/11 7/8 7/5 8/7
Ave. age
Proportion with superior performance at left ear 23.8% 27.3% 20.0% 13.6% 35.0% 0 33.3%** 40.0%
104.1 103.9 104.3 103.5 104.8 104.8 99.8 106.7
32.5 33.4 31.5 33.8 31.1 30.7 34:1 33.0
* 6 females and 1 male "right mixed," i.e, used right hand for writing. males "left mixed," i.e. used left hand for writing. ** 42.9% of right mixed, 20.0% of left mixed.
1 females and 4
23.8 per cent of subjects have shown better performance ort the left than right ear, indicative of right hemisphere dominance for speech perception. The proportion is markedly higher when the left rather than the right hand is used for writing. In the three groups at the bottom of the table the proportion with left ear superiority increases progressively with increasing left hand preference (0 in strong right handers, 33.3 per cent in mixed handers, and 40 per cent in strong left handers). Table II shows the dichotic ratio scores, calculated for each individual TABLE II
Dichotic Ratio Scores in Subgroups
Mean dichotic. ratio scores (xx Ignoring whether Lor R ear superior All subjects Females Males Right handed for writing Left handed for writing Strongly right handed Mixed handed Strongly left handed
28.5 31.8 24.9 30.3 26.6 25.3 38.4* 23.9
* Right mixed = 40.9, Left mixed = 34.9.
+~ y
Right ear superior 28.0 33.2 22.8 28.6 27.2 25.3 39.2 22.6
(N = (N = (N = (N = (N = (N = (N = (N =
32) 16) 16) 19) 13) 15) 8) 9)
X 100 - see text) Left ear superior 30.2 28.2 33.3 41.0 25.6
(N = (N= (N= (N = (N =
10) 6) 4) 3) 7)
37.0 (N = 4) 25.7 (N = 6)
W , A. Lishman and B. R. 1. McMeekan
then averaged for each subgroup. The ratio scores do not show any consistent tendency for inter-ear differences to be smaller in subjects showing left ear superiority than in subjects showing right ear superiority. In fact, though numbers in subgroups are mostly very small, the reverse tendency often appears to obtain. Thus the data provide no support for the idea that subjects·· who are right brained for language functions (as measured by dichotic. listening) show a lessened degree of lateralization, or greater hemispheric equipotentiality, when compared to subjects who are left brained for .language functions. The differences in ratio scores between males and females, though sometimes considerable, are not statistically significant on t-test comparisons. Right handers who are right brained for language show larger ratio scores than left handers who are right brained for language (41.0 compared to 25.6) but again the difference is not · statistically significant. When strongly right handed, mixed handed and strongly left handed subjects are compared the left handers obtain scores which are very similar to the right handers, no matter whether they are right or left ear preferent . .Thus there iSn9 indication that hemispheric dominance is less securely est;tblished in left handers than 'ih right handers. The mixed handers show 'considerably Jarger ratio scores ihan the other groups. This applies whether the.mixedhanders are left or right brained for speech .. Thus the data provide no support 'f or the ldea that~mhjects with mixed hand preference patterns show a .greater tendency than other groups towards "bilateral speech representation"; indeed they appear to. show more marked lateralization of speech than either the right or left handed subjects as judged by the dichotic listening task. However none of the differences between ambidexters and other groups proved to be statistically significant on t-test comparisons. Fainili~l sznistrality
A farilily history of sinistrality was obtained in 16 subjects, representing rather more than half of the females (12) and one-fifth of the males (4). Familial sinistrality was .charted only when a parent or full sibling of the subject was declared to be left handed (or in three cases ambidextrous, one each in the strongly right handed, mixed handed, and strongly left handed gr01-lps).Table III shows the dichotic ratio scores when the subjects are so divided. Left ear superionty, indicative of right brainedness for language, is seen to be commoner in' the pr~sence of a family history of sinistrality only amo,ng s.trongly left handed subjects (50.0 per cent compared to 33.3 per cent). A,mong mixed handed subjects the reverse is obtained. All males and all dextral writers who were right brained for language proved to be without a family history of sinistrality.
Handedness and cerebral dominance for language
37
TABLE III
Dichotic Ratio Scores in Relation to Familit;zl.Sinistrality
Subjects without familial sinistrality No. All subjects Females Males Right handed for writing Left handed for writing Strongly right handed Mixed handed Strongly left handed
26 10
16 15 11 10 7 9
% with . Dichotic left ear ratio superiority scores*
26.9 30.0 25.0 20.0 36.4 57.1 33.3
29.5 37.5 24.4 30.3 28.3 24.4 36.7 29.5**
Subjects with familial sinistrality No. 16 12 4 7 9 5 5 6
% with Dichotic left ear ratio superiority scores
18.8 25.0
33.3
50.0
27.0 27.1 27.0 30.2 24.6 27.1 40.9 15.4**
* Ignoring whether left or right ear superior. ** t = 2.34, d.£. = 13, p < 0.05.
With regard to the size of dichotic ratio scores a family history of sinistrality is seen to be associat~d with reduced ratio scores among the females (27.1 compared to 37.5) and among the left handers (24.6 compared to 28.3), though in neither case is the difference statistically significant. In the lower part of the table it can be seen that among the sttongly left handed subjects familial sinistrality is associated with markedly smaller ratio scotes (15.4 compared to 29.5) and here the difference is statistically significant (p < 0.05). In fact by fat the majority of strongly left handed subjec~swith familial sin.istrality were female (5 out of 6, compared to 3 out of9i itf the group without familial sinistrality), thus accounting for the finding in females generally earlier in the table. Table IV shows that familial sinistrality in strongly left handed subjects is associated with reduced ratio scores whether the subjects have shown a right or a left ear preference on dichotic testing. Manual skill The pursuit rotor test of manmlI skill was carried out on 39 of the 42 subjects. Table V shows the range and means of the hand skill ratios when subjects are divided into three equal sized groups 'on the basis 6£ relative manual skill. Results are shown both for "hits" an.d Iitriisses" on the task. The table also shows the reclassifications involved when skill groupings are compared to the hand preference groupings derived from Annett's question~ naire. In all subjects the hand used for writing proved to be the more skilled on the pursuit rotor task, ils might' he expected. But the tripartite
W. A. Lishman and E. R. L. McMeekan
38
TABLE IV
Dichotic Ratio Scores in Strongly Left Handed Subjects in Relation to Familial Sinistrality
Subjects with familial sinistrality
Subjects without familial sinistrality No.
Dichotic ratio scores
No.
= 14.1)
3
15.5* (S.D.
= 8.2)
=
3
15.3** (S.D.
= 4.5)
Strongly left handed subjects with right ear superiority
6
26.2*
Strongly left handed subjects with left ear superiority
3
36.1** (S.D.
(S.D.
4.6)
Dichotic ratio scores
* t = 1.08, d.f. = 7, p> 0.05. t = 4.43, d.f. = 4, p < 0.02.
**
TABLE V
Subdivisions of Subjects According to Relative Manual Skill
Hand preference groups
Mean hand* difference ratios
Range
Female/ Male
6.7 0.3 -S.l
14.S to 2.6 2.5 to -3.0 -3.4 to -19.S
7F,6M 7F,6M 5F, SM
40.1 Pursuit } Right Skilled Intermediate -6.0 motor misses Left skilled -5S.6
66.3 to 2S.6 27.2 to -39.S ~42.2 to -79.5
6F,7M 9F,4M 4F,9M
Pursuit ) Right """'" Intermediate rotor hits Left skilled
Strong Mixed Strong right handed left handed handed 9
5
4 6 2
9
4
5
5
3
2
11 3 10
., R-L ... L-R For purSUlt rotor hits calculated R+L X 100 and for pursUlt rotor misses .,!{+L_ X lOC where R = score with right hand and L = score with left hand. Thus in· both cases positiv scores indicated superior performance with the right hand, and negative scores superic performance with the left hand.
*
divisions on hand. skill scores have led to a number of interchanges betwee the extreme hand preference groups and the mixed handed group. Nor at the groupings according to pursuit rotor hits and misses entirely congruen1 fot example only 6 of the 9 subjects in the "right skilled" groups are t1 same individuals where hits·· and misses are concerned. Table VI shows the proportion of subjects in each manual skill grou who showed left ear preference (i.e., right brainedness) on dichotic testin also the size of the dichotic ratio scores obtained. The proportion showir left ear preference increases fairly regularly with an increasing degree .1
39
Handedness and cerebral dominance for language TABLE VI
Dichotic Rotio Scores in Relation to Manual Skill
Proportion with superior performaFlce at left ear
) ru~, Pursuit
Ignoring whether left or right ear superior
Subjects with right eat superior
Subjects with left ear superior
23 .9 (N = 11) 35.9 (N = 11) 21.9 (N = 9)
19.4 (N=2) 59.4 (N = 2) 30.0 (N = 4)
24.8 (N::=: 12) .31.2 (N = 11) 26.6 (N = 8)
12.7 (N= 1) 55.0 (N = 2) 30.9 (N= 5)
~
15.4%
23.2
Intermediate
15.4%
39.5
\ Left skilled
30.8%
24.3
Ri~' ,kill'"
7.7%
23 .9.
Intermediate
15.4%
34.9
Left skilled
38.5%
28.2
rotor hits
Pursuit to.tOt ffilsses
Dichotic ratio scores
)
left hand skni, though in a rather less clear cut fashion than was observed in relation to manual preference patterns (in Table I). ':the degree or language lateralization as judged from dichotic ratio scores closely re~embles the results in Table II - thus left manual skill, like left manual preference, is not associated with diminution in the size of the dichotic ratio s~ores; and intermediate skill, like the mixed preference pattern, tends to be associated with augmented ear difference scores. When the direction of ear preference is considered there is no indication that left ear preference (right hemisphere dominance) is less securely established than ' right ear preference either among intermediate or left skilled subgroups. The results obtained in relation to m'anual skill when i family 'history of sinistrality is taken into account are not presented, budn general followed the patterns observed in the 'manual preference groups. as s!imvn in Tables III and IV. DISCUSSION
The results show that cerebral domina~ce for language, as inferred from dichotic testing, tends more often to lie with the right hemisphere in mixed handers than in strong right handers, and more often still in strong left handers. The incidence in strong left handers (40 per cent) is rather higher than in many other studies, perhaps as a result of the strict criteria used for inclusion in this group. No individual classified as a strong right hander has proved to show right hemisphere dominance. Other surveys using dichotic
40
W . A. Lishman and E. R. L. McMeekan
listening have often found such examples (Dee, 1971 = 17 per cent; Zurif and Bryden, 1969 = 10 per cent; Kimura, 1973 = 18 per cent; Satz et aI., 1965 = 11.5 per cent). Here, however, the strict criterion of consistent right preference on all six of Annett's primary questions has been required for inclusion in the strong right handed group. If the hand used for writing had been the sole criterion for designating right handedness we would have obtained 13.6 per cent of right handers with right hemisphere dominance. Of perhaps some interest is the finding that 3 out of 7 (43 per cent) of the mixed handers who wrote with the right hand (i.e., left preferent for one or more of Annett's primary questions even though writing with the right hand) have shown indications of right hemisphere dominance. Though numbers are very small this is a similar proportion to that found with strong left handers. It is possible that these individuals represent cultural shift towards using the right hand for writing in persons who were otherwise destined to be strong left handers. An important finding is that left handers and mixed handers do not show reduced ear asymmetries when compared to right handers. If anything the trend is for mixed handers to show considerably larger ear differences than strong right or strong left handers. Nor do individuals with indications of right hemisphere dominance show lessened ear asymmetry than individuals with left hemisphere dominance - the size of the ear differences corresponds closely, only the direction of ear preference ' is reversed. Subdivisions of the material according to relative manual skill on a pursuit rotor task show similar findings. Females in general have shown larger ear difference scores than males when left hemisphere dominant, but the above results do not depend ' on sex imbalance in the principal subgroups. A family history of sinistrality is, however, associated with significantly reduced ear difference scores. This applies only in strongly left handed subjects, not in mixed handed or right handed subjects. The smaller ear asymmetry in left handers with sinistral relatives applies whether they are left or right hemisphere dominant. The present data have been able to demonstrate this clearly in females only. These findings may be viewed in relation to other studies. The clinical evidence suggesting bilateral speech representation in non-right handers must be viewed with caution for a number of reasons. Lesional studies suffer from uncertainties with regard to the size of the responsible lesions and the extent of anatomical involvement of the language areas of the hemispheres. Work on epileptics suffers from possible contaminating effects due to early brain damage which may have encouraged transfet or diffusion of language functions to the opposite hemisphere of the brain. Pre~ious work involving dichotic listening deserves closer scrutiny here.
Handedness and cerebral dominance for language
41
Satz et a1. (1967) reported smaller ear asymmetries in sinistrals than dextrals, but presented only group means for errors on the left and right ears. Their group mean differences are certainly much smaller in sinistrals than dextrals, when mean left ear errors are subtracted from mean right ear errors, but this would be expected since a much larger proportion of the former than the latter had performed better on the left ear than the right. Others present their data in a manner which avoids this difficulty, and display smaller absolute ear difference scores in sinistrals than dextrals (Satz et aI., 1965, Curry, 1967; Curry and Rutherford, 1967), but none of these workers have analysed their results in relation to the presence or absence of a family history of sinistrality. Zurif and Bryden (1969) do examine familial and non-familial sinistrals separately, and compare them with dextrals on a number of dichotic and tachistoscopic tests. The non-familial sinistrals have dichotic (and tachistoscopic) difference scores of similar magnitude to dextrals, but the familial sinistrals show very small ear or half field differences. However only group mean scores for each ear or half field are given, so it is hard to know whether or not the findings are entirely analogous to our own. Thus the present data do not support the idea of "weak dominance" or "bilateral speech representation" or "hemispheric equipotentiality" among the generality of sinistrals or ambidexters as has often been proposed. Such statements would seem applicable only to strong lefthanders with a family history of sinistrality. These conclusions do not appear to be at direct variance with other reported studies when one takes into account the methods used for presenting results and when one notes that a family history of sinistrality has not always been recorded in previously published work. The present results must, of course, be viewed with caution since dichotic listening tests are no more than indirect and approximate indicators of cerebral dominance. .In particular they can give indications of receptive language functions only and do not necessarily reflect the neural organisation subservingexpressive aspects of language. Our data, indicating welliateralized ear preferences in nonright handers, do not therefore necessarily countermand the evidence from lesional and amy tal studies discussed above - it is possible that well lateralized receptive functions may yet co-exist with bilateral cerebral representation for expressive language. In this connection it should be noted, however, that studies of left hemispherectomised and callosal sectioned patients suggest the reverse, viz. that receptive functions are more liable to be organised bilaterally than expressive functions (Smith, 1966; Gazzal1iga and Sperry, 1967; Sperry and Gazzaniga, 1967; Zangwill, 1967). Unfortunately we lack a method for exploring the lateralization of expressive language functions in a normal volunteer population with which to attempt to resolve this dilemma.
W. A. Lishman and E. R. L. McMeekan
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SUMMARY
In so far as ear asymmetries on dichotic listening reflect cerebral dominance for language, the present evidence indicates a progressively decreasing incidence of left hemisphere dominance in right handed, mixed handed and left handed individuals. In the absence of a. family history of sinistrality there are no indications that the degree of dominance is reduced in left handers or mixed handers when compared to right handers, nor that right hemisphere dominance is less securely established than left hemisphere dominance. Among strong left handers with a family history of sinistrality, however, ear difference scores are significantly smaller, indicating reduced lateralization or bilateral representation of language in such individuals. This applies equally in left dominant and right dominant left handers.
Acknowledgments. This work was supported by a grant from the Medical Research Council, which is gratefully acknowledged. We are indebted to the many volunteer subjects who took part, and to Mr. Peter Nicholls for statistical advice.
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Dr. W. A. Lishman and Miss E. R. L. McMeekan, Institute of Psychiatry, De Crespigny Park, London, SE5.