Language dominance: Correlation of radiological and functional data

Nmopsychologia, Printed in Great

Vol. 23, No. 3. pp 415420, Britam.

1985 0

002X-3932/85 %3.00+000 1985 Pergamon Prw Ltd.

NOTE LANGUAGE

DOMINANCE: CORRELATION OF RADIOLOGICAL FUNCTIONAL DATA

AND

ESTHER STRAUSS,* J~CELYNF S. LAPoINTE,t JI:HN A. WADA,: W. GADDFS* and B. KOSAKA* *Department of Psychology, University of Victoria, Victoria, B.C., Canada TDepartment of Radiology, University of British Columbia, Vancouver, B.C., Canada iDivision of Neurological Sciences, University of British Columbia, Vancouver, B.C., Canada (Accepted

18 Nooember

1984)

Abstract-Morphological asymmetry of the posterior sylvian region was measured in carotid arteriograms of patients with medically refractory seizures. Anatomical asymmetry correlated with ear superiority on dichotic listening tests.

INTRODUCTION THE past century, interest has focused on the neuroanatomical asymmetries that might underlie the left hemisphere’s dominance for language (for recent reviews of this topic, see [12, 22, 24, 34, 351). The left temporal plane, or planum temporale, a portion of the posterior language zone (Wernicke’s area), lying on the upper surface of the temporal lobe posterior to Heschl’s gyrus, is typically larger than the corresponding area in the right hemisphere, both in the adult [S, 11, 15, l&21, 26,31-333 and in the fetus and newborn [2, 18, 31 333. This size asymmetry probably reflects the greater extent on the left side of area TPt which corresponds roughly to von Economo’s area TA and represents a transition between auditory association cortex and cortex of the inferior parietal lobule [9]. There are reports of other physical asymmetries in the perisylvian region. One concerns the configuration of the sylvian fissure [4, S]. The fissure on the right side curls up while that on the left side remains horizontal and reaches further back. A longer left sylvian fissure, a lower left sylvian point and a smaller left arch of the middle cerebral artery leaving the posterior end of the sylvian fissure have also been described (e.g. [3, 13, 16, 20, 21, 23, 28, 361). These differences imply a larger left parietal operculum and temporal plane. In addition, there is evidence to suggest that the posterior part of the thalamus, usually the left, participates in language function [19] and cytoarchitectonic asymmetry with left preponderance of the lateralis posterior nucleus has been documented [6]. This nucleus projects to the inferior parietal lobule [6,27] in which a cytoarchitectonic asymmetry of the angular gyrus in favour of the left side has also been found [7]. Finally, it is noteworthy that asymmetries have also been reported for the anterior speech region (Broca’s area). The frontal operculum in the left hemisphere is larger than the homologous area in the right hemisphere [S, lo]. Moreover, the left opercular region has more higher-order dendritic branching patterns in contrast to more lower-order ones on the right side (Scheibel, cited in [17]). There is some evidence in favour of the view that these asymmetries represent the neuroanatomical substrates for the left hemisphere’s dominance for language. First, the anatomical asymmetries coincide with classical language zones. Moreover, the anatomical differences appear less pronounced, and are sometimes even reversed, in people with atypical patterns of speech representation and in left-handers, a group characterized by considerable variability in language lateralization [13, 16, 20, 25, 35, 373. In this study, we attempted to determine the possible relationship between dichotic listening test results and morphological asymmetry in the posterior sylvian region as measured in carotid arteriograms. The dichotic listening test assesses the abilities to understand speech [14], a function thought to be mediated by the posterior sylvian region. Therefore, using the dichotic listening test to provide an index of language lateralization, we expected that a larger left posterior sylvian region would be found in people with left-hemisphere language dominance whereas a reversed or reduced pattern of anatomical asymmetry would be evident in those with right-hemisphere language representation. The subject population consisted of medically refractory seizure cases who had been investigated in-depth for possible surgical treatment. They had undergone monitoring of electroclinical seizures to find the brain area of epileptogenic lesion responsible for their habitual seizures, carotid Amytal testing (through femoral catheterization performed bilaterally on different days) in order to establish cerebral speech dominance [29, FOR

415

NOTE

416 303, carotid arteriograms dichotic listening tests.

to obtain

structural

information,

and neuropsychological

examination

including

verbal

METHODS Subjects Internal-carotid angiograms and CT scans were available on 73 patients who had undergone carotid Amytal speech testing. Thirty cases were excluded from the study because their angiograms and/or CT scans revealed neoplastic or atrophic processes, and/or because of technical inadequacies. In addition, seven patients were excluded because their dichotic listening test scores were not available. Thus, our final sample consisted of 36 patients (18 males, 18 females) whose angiograms and CT scans were read as normal. Carotid amytal testing revealed that in 27 patients, speech was exclusively mediated by the left hemisphere and in two patients, speech was in the right hemisphere. Seven patients had bilateral speech representation. The majority of the patients were right-handed. Only three patients were left-handed, one had speech represented in the left hemisphere, the other two patients had right-hemisphere speech representation. At the time of angiography and Amytal testing, the ages of the patients ranged from 15 to 55, with a mean age of 30.9 yr. Procedure Dichotic listening test. The dichotic listening test consisted of 22 trials, each containing three dichotic pairs of mono-syllabic words. The subject was instructed to repeat as many of the six words as possible on each trial. Scores were derived for each subject using the formula (R -L)/(R + L) where R represents the number of words correctly reported from right-ear presentations and L the number of words correctly reported from left-ear presentations. A right-ear advantage (REA) suggests left-hemisphere dominance for processing verbal material while a left-ear advantage (LEA) indicates right hemisphere superiority [14]. Anatomical measures Two anatomical measures of the posterior sylvian region were determined from the angiograms: (a) sylvian arch asymmetry and (b) posterior width asymmetry. Syloian arch asymmetry. The first is a measure of the angle formed by the last branch of the middle cerebral artery as it leaves the posterior portion of the sylvian fissure and courses downward under the parietal operculum. Typically, a narrower arch is found on the left side, which is thought to reflect the greater expanse of the left, as opposed to right, parietal operculum. Following the method of HOCHBERGand LEMAY [13], the most medial posterior branch of the sylvian vessels was deemed the sylvian point. The apex of its curve was marked (S) and a second point was marked 1 cm distal to the first point (X). A perpendicular from the first point was dropped to a line drawn through the orbital roof (0). The angle formed by the two lines (XSO) was then measured separately on each side for each patient (see Fig. 1). A measure ofsylvian arch asymmetry was obtained by subtracting the angle formed by the middle cerebral artery in the left hemisphere from the equivalent angle in the right hemisphere (R-L). Posterior width asymmetry. The width of the posterior temporal lobe at the level of the sylvian point (the apex of the sylvian arch used in the previous measure) was also measured as a ratio of the inner diameter of the skull at the same level: AS/AB (see Fig. 2). Each side was measured separately for each subject because magnification of the head varied from the left to the right side, each carotid angiogram having been done on different days. Ratios were converted to proportions. The value obtained for the left hemisphere was subtracted from that for the right hemisphere to give a measure of width asymmetry (R-L).

RESULTS On the dichotic listening test, the majority of the patients (32/36) showed a REA on the dichotic listening task. Only four patients showed a LEA. Most of the patients (24/36) had a wider left posterior sylvian region whereas the right side was wider in 12 of the cases, In about half of the patients (19/36), the sylvian arch was narrower on the left side. In the other half of the sample (17/36), the right side was narrower. In order to subdivide our sample on the dichotic and anatomical measures, if a difference score (R -L) of 0 was obtained, the case was classed as showing a right-hemisphere advantage. Relation between language

and anatomical measures

Analysis of the difference scores, using a Pearson product&moment correlation, revealed a significant correlation between the dichotic listening test results and the measure of posterior width asymmetry (r = - 0.34, n = 36, P = 0.04, two-tailed test). Seventy-two per cent (23/32) of the patients who showed a REA on the dichotic listening task had a wider left sylvian region. Three of the four patients who showed a LEA had a wider right posterior sylvian area. The association between the measure of sylvian arch asymmetry and dichotic listening behavior was non-significant, although a trend for a linkage was evident (r =0.24, n = 36, P=O.16, two-tailed test). The measure of

417

NOTE

R

L

of both carotid angiograms of the same patient illustrates FIG. 1. A composite photograph difference in the angle XSO on the right side compared to that on the left side.

.2. The width of the temporal lobe was measured at the level of the sylvian point and converted a ratio of the skull diameter (AS/AB).

I.he

to

NOTE

419

sylvian arch asymmetry was unrelated to that of the posterior width asymmetry (r= -0.03, n= 36, n.s., two-tailed test). A multiple regression analysis based upon the anatomical measures (sylvian arch and posterior width) revealed that about 12% of the variance in dichotic listening scores could be explained by the posterior width asymmetry, and this amount was significant [F (1, 34) = 4.52, P= 0.041. The other variable, in combination with the posterior width measure, did not add a significant contribution. One might also ask whether there is a relation between the pattern of speech representation, as determined by the carotid Amytal test, and the anatomical measures, For these analyses, the patients with right-hemisphere speech dominance and bilateral speech representation were treated together. No significant associations emerged when the sylvian arch asymmetry (r =0.007, n = 36, n.s.) or posterior width asymmetry (r = 0.19, n = 36, n.s.) were considered. There was also no significant relation between the dichotic listening test results and the Amytal findings (r= -0.22, n= 36, ns.). At the present time, it is impossible to elaborate on the significance of these findings given the small number of subjects with right-hemisphere speech dominance (n=2) in the atypical speech group. Location

of focus

Given the neurological status of our population, it was necessary to determine whether location of epileptogenic lesion contributed to the pattern of results. For this purpose, the patients were subdivided into those with evidence of unilateral left, right or bilateral dysfunction. Laterality of the focus had no significant effect on the dichotic listening scores [F (2, 29)=0.32, ns.], the sylvian arch asymmetry [F (2, 29)=0.86, n.s.] or the posterior width asymmetry [F (2, 29) = 2.2, ns.].

DISCUSSION The results of this study reveal that neurological patients who show a REA on a verbal dichotic listening test, indicative of left-hemisphere language dominance, are more likely to have a wider left posterior sylvian region. Similarly, patients who show a LEA, suggesting right-hemisphere language lateralization, are more likely to have a wider right posterior sylvian region, but this conclusion must be tempered given the small number of subjects. A novel approach in the current study was the measurement of the width of the posterior temporal lobe at the level of the sylvian point. This region consists of the posterior temporal to temporal-parietal junction, where known anatomical asymmetries exist. However, more needs to be determined about this measure’s relation to these other anatomical features of the posterior temporal region (e.g. planum asymmetry) before any firm conclusions can be made. It is difficult to draw inferences regarding structure-function relations in normal people, given the nature of our population. Although care was taken to exclude from investigation patients with abnormal angiograms and CT scans, many of our patients had long-standing epilepsy that might have altered hemispheric organization. In support of this notion is the observation that the distribution of sylvian arch asymmetry (narrower on the left side in 53 “/, of the cases) is considerably different from that found in other published series (narrower on the left side in about 75”” of the cases). On the other hand, if we exclude cases with onset of damage prior to the end of the first year of life, the period of most rapid brain change, then we are left with a group of patients that is probably more representative of the normal population. Analysis of the data nonetheless suggests a relation between performance on the dichotic listening test and posterior width asymmetry (r= -0.42, n= 19, P=O.O8, two-tailed test). It is important to stress that in our patient population, the dichotic listening test results do not provide a very reliable indicator of anatomical asymmetry. This may be an indication of the fact that the anatomical measurements made were too crude to correlate well with the behavioral variable. On the other hand, it may well be that the dichotic listening test is not a precise measure of functional hemispheric asymmetry [l]. Studies that correlate functional variables with sophisticated neuroanatomical data (see for example [35]) are needed to decide the issue. In summary, our findings, if replicable, would indicate that in patients with medically refractory seizures, a behavioral measure of language dominance is linked to an anatomical asymmetry in a language-related region, However, interpretation of the results is limited by the nature of our population and the novelty of one of our anatomical measures. Acknowledgements-This research was supported by MRC of Canada, Grant MA-6973 to Esther Strauss. We are grateful to Dr. J. Zaide for many helpful comments. We also thank Dr. M. Moscovitch, Dr. D. Read and two anonymous referees for their valuable suggestions.

REFERENCES I. BRYDEN, M. P. Laterality:

Functional Asymmetry in the Intact Brain. Academic Press, New York, 1982. E. C. and GILLES, F. H. Gyral development of the human brain. Ann. Nrurol. 1,8693,

2. Cm, J. G.. DOOLING, 1977. 3. CONNOLLY, C. J. External Morphology of the Primate Brain. Charles C. Thomas, Springfield, Illinois, 1950. 4. CUNNISGHAM, D. J. Contribution to the surface anatomy of the cerebral hemispheres. Cunningham Memoirs, No. VII, Royal Irish Academy, Dublin, 1892.

420

NOTE

5. EBERSTALLER,0. Zur Ober flachenanatomie der Groshirn-Hemispharen. Wien. mrd. BI. 7,479.642,644, 1X84. 6. EIDELBERG, D. and GALABURDA, A. M. Symmetry and asymmetry in the human posterior thalamus. I. Cytoarchitectonic analysis in normal persons. Archs Ncurol. 39, 325-332, 1982. 7. EIDELBERC;,D. and GALABIJKDA, A. M. Inferior parietal lobule: divergent architectonic asymmetries in the human brain. Archs Neural. 41, X43-852, 1984. 8. FALZI, G., PERRONE, P. and VIGNOLA, L. Right-left asymmetry in anterior speech region. A&s Neural. 39, 239--240, 1982. 9. GALABURDA, A. M., SANIDES, F. and GESCHWIND, N. Human brain: cyto-architectonic left-right asymmetries in the temporal speech region. Archs New-d. 35, 812-8 17, 1978. 10. GALABURDA, A. M. La rkgion de Broca: observations anatomiques faite un sikcle apt& la mart de son decouvreur. Rev. Neurd. 138, 603-616, 1980. I 1. GESCHWIND, N. and LEVITSKY, W. Human brain: left- right asymmetries in temporal speech region. Science 161, 186187, 1968. 12. GESCHWIND. N. The anatomical basis of hemispheric specialization. In Hmlisp/zeric Function of the Humun Brain, S. J. DIMOND and J. G. BEAUMONT(Editors), pp. 7 24. Paul Elek, London, 1974. 13. HOCHBERG, F. H. and LEMAY, M. Arteriographic correlates of handedness. Neurology 25, 218-222. 14. ffiMURA, D. Cerebral dominance and the perception of verbal stimuli. Can. J. Psycho/. 15, 166-170, 1961. 15. KOPP, N., MICHEL, F., CARRIER. H.. BIRON, A. and DUVILLARD, P. Etude de certaines asymetries hemisphkriques du cerveau humain. J. nruroi. Sri. 34, 349-363, 1977. 16. LEMAY. M. and CULEBRAS. A. Human brain morphologic differences in the hemispheres demonstrable by carotid arteriography. N. Enyl. J. Med. 287, 168-170, 1972. 17. MARX, J. L. The two sides of the brain. Science 220, 488490, 1983. 18. NIKKUNI, S., YASHIMA, Y., KISHIGE, K., SUZUKI, S., OHNO, E., KUMASHIRO, E., KOBAYASHI, E., AWA, H., MIHARA, T. and ASAKURA, T. Left-right hemispheric asymmetry ofcortical speech zones in the Japanese brain, Bruin Nan-e, Tokyo 33, 77-84, 1981. 19. OJEMANN, G. Asymmetric function of the thalamus in man. Ann. N. Y. Acad. Sci. 236, 38@ 396, 1977. 20. RATCLIFF, G., DILA, C.. TAYLOR, L. and MILNER. B. The morphological asymmetry of the hemispheres and cerebral dominance for speech: a possible relationship. Brain Lung. 11, 87-98, 1980. 21. RUBENS, A. B.. MAHOWALD, M. W. and HUTTON, J. T. Asymmetry of the lateral sylvian fissures in man. Neuroloyy 26, 626624, 1976. 22. RUBENS, A. B. Anatomical asymmetries of human cerebral cortex. In Lateralization in Ihe Newous System, S. HARNAD. R. W.. DOZY. L.. GOLDSTEIN, J. JAYNESand G. KRAUTHAMER(Editors), .pp. . 503-516. Academic Press, New York, 19?7. a study in cerebral morphology. Phi/. Trans. R. Sot. 23. SHELLSHEAR,J. L. The brain of the aboriginal Australian: 227B, 293-409, 1937. basis of lateralized cerebral function: a review. 24. STRAIISS, E., KOSAKA, B. and WADA, J. A. The neurobiological Human Neurobiol. 2, I 15- 127, 1983. 25. SZIKLA, G.. HORI, T. and BOUVIER, G. The third dimension in cerebral angiography. In Adzw~ces in Cerebral Ayiogrcrphy, G. SALAMON (Editor). Springer, New York, 1975. 26. TESZNER, D. A., TZAVARAS, A., GRUNER, J. and HBCAEN, H. L’asymetrie droit -gauche du planum temporale: i propos de I’btude anatomique de 100 cerveaux. Rev. Nrurol. 126, 444 449, 1972. 27. VAN BUREN, J. and BURKE, R. VuriationsunclConn~~/ionsqf’thc~ Human Thulamus, Vols. I and 2. Springer, New York, 1972. masse- und rindenarchitektonik der supra28. VON ECONOMO, C. and HORN, L. Uber windungsrelief, temporalflache. Ihre individuellen und. ihre seitenunterschiede. Z. ges. Neural. Psyhiu/. 130, 678-757, 1930. of the side of cerebral speech dominance: clinical~experimental 29. WADA, J. A. New Method for determination observations on the intracarotid injection of sodium amytal. Meal. Biol. 14, 221-222, 1949. injection ofsodium amytal for the lateralization ofcerebral speech 30. WADA, J. A. and RASMUSSEN,T. Intracdrotid dominance: experimental and clinical observations. J. Neurosurg. 17, 226 282, 1960. sharing and shift of cerebral speech function. Eucerptu med. Int. Congress 31. WADA. J. A. Interhemispheric Services 193, 296 297, 1965. in humans. Archs New-o/. 32, 32. WADA, J. A., CLARKE, R. and HAMM. A. Cerebral hemisphere asymmetry 239m~246, 1975. for language in the newborn: neuroanatomical 33. WITELSON, S. F. and PALLIE. W. Left hemisphere specialization evidence of asymmetry. Brrrirl 96, 640 646, 1973. phylogenesis. and relationships 34. WI~ELSON, S. Anatomic asymmetry in the temporal lobes: its documentation. to functional asymmetry. Aun. ,Y. Y. Aud. Sci. 299, 3X-354. 1977. anatomic asymmetry as a key to functional asymmetry. In 35. WITELSON. S. Bumps on the brain: right-left Lrmgutyr Fum~/io~~ mu/ Bruit1 Or,q:yrmiztrtion. S. SEGALOWITZ (Editor). pp. 117 144. Academic Press, New York, 19X2. 36. YENI-KOMSHIAN, G. H. and BENSON. D. A. AnatomIcal study of cerebral asymmetry in the temporal lobe of humans. chimpanzees, and rhesus monkeys. Scirncc~ 192, 387 389, 1976. in a case ofcrossed aphasia in 37. YORK HAALAND. K. and MIRANDA, F. Psychometric and CT scan measurements a dextral. Bruit1 Lam/. 17, 240 260. 1982.