Mouth asymmetry, dichotic ear advantage and tachistoscopic visual field advantage as measures of language lateralization

Neuropsychologto, Vol. 21, No. 6, PP. 641649, Pnnted in Great Britain.

1983. 0

0028-3932/83$3.00+0.00 1983 Pergamon Press Ltd.

MOUTH ASYMMETRY, DICHOTIC EAR ADVANTAGE AND TACHISTOSCOPIC VISUAL FIELD ADVANTAGE AS MEASURES OF LANGUAGE LATERALIZATION ROGER GRAVES Departmentof Psychology, University of Victoria, Victoria, B.C., Canada (Accepted

16 June 1983)

Abstract-Clinical evidence suggests that speech expression, speech comprehension and reading have distinct anatomical representations and that these functions may have differential degrees of laterahzation. Experimental measures sensitive to the lateralization of these functions may be, respectively, mouth asymmetry, dichotic listening and visual field advantage. These measures, individually, showed relatively low success in estimating overall “language dominance” and had low intercorrelations. A composite measure was more successful. Language lateralization may not be unitary, and even if it is, a composite of several distinct measures may be necessary to index it.

INTRODUCTION ALMOST 120 years have passed since the discovery

that, typically, one side of the human brain is more essential for language functions than is the other side [4], During most of this time the only way to determine which was an individual’s dominant hemisphere was by observation of the consequences of brain damage. About 30 years ago experimental, but invasive, methods were devised, notably the Wada method [36]. More recently, noninvasive techniques have been discovered and intensively developed. Nevertheless, there is as yet no generally available, reliable, non-invasive technique for discovering the language lateralization of an individual. Such a technique would have many potential research, clinical and theraeeutic uses. The overall purpose of this study was to examine the problem of determining lateralization of language functions with relatively simple non-invasive techniques. Three measures, auditory dichotic ear advantage, tachistoscopic visual field advantage, and mouth asymmetry, were obtained from the same subjects. The data from each measure were analyzed separately in three ways. First, conventional univariate ANOVAs assessed the group effects. Second, the results were dichotomized in the conventional manner, according to whether there was any left vs right difference. The resulting asymmetry percentages were then compared to previous published results and to the hypothetical percentages based on Wada test findings, and estimates of the validity of each measure as an index of “language dominance” was calculated [31]. The third anaIysis, motivated by criticism of the conventional dichotomization of laterality data [6, 9, 393, determined the reliability of results for each individual subject and obtained new validity estimates. While several previous studies have obtained multiple laterality measures from the same subjects for comparison purposes [S, 12,32,40], none of these has attempted to combine the measures. For reasons which will be discussed later, a composite measure could be more 641

dependable than any single measure. This possibility was explored by combining the results from all three measures into a composite score and obtaining a new validity estimate. An additional purpose of this study was to provide a further replication and development of the mouth asymmetry technique which was proposed as an indicator of the lateralization of expressive speech function [ 191.

METHOD Suhiecls Subjects were 60 paid volunteers from males, females, left and right hdnders writing. which. in all cases. corresponded responded “yes” to the question: “Have any subject included who wore dental

the university community between the ages of 18and 36. Equal numbers of were included. Handedness was defined as the hand the person used for with the sign of the Edinburgh index 1281. No subject was included who you had any serious injury or surgery to your head. face or jaw’?” Nor was braces.

Mouth as.vmmerr? Videotape recording was employed as described previously [19]. A word-list generation task [19] was used, followed by a second speech task. For this latter task the subject produced words beginning with “B” which rhymed with words spoken by the experimenter. This task was chosen because (a) it would produce a fixed number of scoredbte mouth openings, not the variable number with word list generation, (b) it should be less likely to elicit stress or embarassment-related smiling, and (c) rhyming clearly requires dominant hemisphere processing as shown by right hemisphere failure in split brain patients [24] and extreme sensitivity to left hemisphere damage in aphasic patients (T. LAWIS, personal communication). Instructions were: “Now I’m going to read a list of words to you. After I say a word. I’d like you to give me a word beginning with “B” which rhymes with my word. For example, if I said “like”, you would say “bike”. Please say each word clearly and fairly loud”. Scoring employed the previous procedure 1191 with frame-by-frame playback in which the third frame from initial lip opening was scored by placing rulers tangent to the lip opening at points equidistant from the lip midline. The angle between the rulers was scored as right (> ), equal (= ), or left (< ). A laterality index was calculated as: (R- L)/(R+ L), where R equals the number of right side greater openings, and L equals the number of left side greater openings. Since the results showed a correlation between the word list and rhyme task indices of +0.93, the rhyme task data were used in all subsequent analyses because they were based on almost twice as many trials, and because undesired smiling was indeed infrequent. Statistical significance was defined using the exact binomial probability method [ 341 which determined the probability of the observed number of right side greater asymmetries occurring by chance. Dichotic lisfeninq A tape containing 22 trials was used. Each trial consisted of three dichotic pairs of concrete mono-syllabic words (6 words total). The subject was instructed to repeat as many of the six words as possible on each trial. Volume to the two earphones was balanced at 70 db using a sound pressure level meter. After one run through the tape, the headphones were reversed and the last 12 trials were repeated. Data from the last IO trials from both runs (120 stimulus words total) were combined and used to calculate a laterality index using the method of MARSHALI. et ul. 1253. Statistical significance was defined with a Zscore test [1 l] of the difference between the proportion of left side words correct and the proportion of right side words correct. 2 > 2.13 (or < -2.13) corresponds to a (2-tail) significance level of Pi 0.033. Tachisfoscopic

reading

Smce double simultaneous stimulation 126. 401 and verbal report [I. 271 enhance the usual right visual field advantage (presumably improving the reliability and validity of the technique as a measure of lateralization for language), these procedures were employed. Using verbal accuracy rather than manual reaction time also allowed the data to be compared directly with other studies using this method and allowed the computation of a laterality index which could be directly compared with indices from the other two measures. Stimuli were 36 four-letter words varying in frequency (for list see 1231). Each word was paired with a pronounceable four-letter nonsense string (e.g. buit half). A randomized order presented each word once in each visual field (72 trials total). The letters were lower case “Helvetica Medium” with the string beginning 1.8 from fixation. The subject’s index fingers held down telegraph keys placed on either side of the body midline. Subjects were told that a real English word would appear in each flash and were asked to release the telegraph key on the side corresponding to the word as quickly as possible and then to say the word aloud. Stimuli were presented automatically in a Gerbrands tachistoscope at a rate of one trial every 7 sec. The pre- and post-stimulus field was white except for a central fixation spot. To maintain an approximate overall 500/{,accuracy rate for each subject, an initial 16 trials were run to set exposure duratton using

LANGUAGE

643

LATERALIZATION

similar but different word/nonsense pairs. Over these trials exposure was reduced or increased from 50 msec until approximately 50% correct report was obtained. The exposure remained at this duration for the final 72 trials. Final durations ranged from 140 to 9 msec. A laterality index and the statistical significance were calculated using the same methods as were used for dichotic listening. Composite measure Subjects were classified if at least two individual measures exceeded a criterion level of significance in the same direction. This method was chosen to require a convergence of evidence from more than one measure. Methods which average the measures [30] would allow one highly “significant” measure to dominate the average. This is undesirable in the present situation. Mouth asymmetry scores were often highly consistent but such scores would not necessarily be any more valid than a less consistent (but still significant) result. Highly consistent results on either of the other two tests would actually be suspect. For example, a large dichotic ear advantage could result from an undetected hearing impairment in one ear or from an attentional strategy and such data should not be weighted more than the more typical small effect. For comparison with the conventionally dichotomized individual measures, left hemisphere dominance was predicted if at least two individual measures showed any right side bias (i.e. exceeded a P< 0.5 criterion). This corresponds to an overall P-c 0.5 level of significance since random data would result in 50% left predictions. For comparison with the “reliable” individual measures, left hemisphere dominance was predicted if at least two individual measures showed a right side bias at a P=O.153 (2-tail) level of significance. This results in an overall P
“Validity” was defined as the estimated probability that a left side result (e.g. left ear advantage) actually came from a right hemisphere dominant subject. SATZ’ method [3l] was followed except that (a) the “true” incidence of left and right hemisphere dominance among right handers was assumed to be 96 and 4:; 1291, and (b) the probability of left side advantage with right dominance was assumed to be equal to the probability of right side advantage with left dominance.

RESULTS Predicted

hemispheric

dominance

Results for all measures broken down by sex and handedness are shown in Table 1. For this table only the sign of the laterality difference is considered (i.e. a P~0.5 criterion of significance is accepted). Table 2 shows results broken down by handedness and sex when a P~O.033 criterion of significance is demanded. Group effects Manora

indices Table

und correlations.

showed

a significant

I. Fraction

(and percentage)

Handedness: Sex :

A multivariate analysis of variance for the three laterality side effect, F (1, 56) = 38.5, P
Male

Right Female

Both

Male

Left Female

Both

Mouth asymmetry

12115 (XO”$)

II/l5 (73 “0)

23/30 (77 “J

lljl5 (73 “0)

I?/15 (80”“)

23/30 (77”“)

Visual field advantage

12/15 (80”,,)

12115 (X0”“)

24/30 (X0”,,)

13/15 (87 “J

Dichotic ear advantage

13/15 (X7”,,) l3/15 (87 “,,)

IO/IS (67”“)

23/30 (77”,,) 26130 (87”“)

7115 (47 ““) II/l5 (73 1’“)

IO/IS (67 “0) 6115 (40 ““)

23130 (77”,) 13130 (43 “,) 22130 (73 “J

Composite measure

13/15 (87 ‘I,,)

1 l/l5 (73 “J

performance

Estimated validity 0.14 0.17 0.14 0.2x

644

ROWZR GRAV1.S Table 2. Fraction

(and percentage) of subjects showing superior right side (left hemisphere) accepting only statistically reliable (P < 0.033) asymmetries

Handedness: Sex :

Male

Right Female

Both

Male

S/IO (X0”“)

X/10 (X0”,,)

16/20 (X0”,,)

X/II (73 “J

IO/l0 ( 100 ‘:,,)

l/7 (IOO”,,)

17117 (loon’<,)

Y/Y (1001’,,)

616 (loo”,,)

15’15 (loo”,,)

Dichotic ear advantage

414 (IOO~‘,,)

414 (loo”,,)

X/X (loo”,,)

5/x

7113 (54 ‘I,,)

‘)

(63 “,,I

2/5 (40”,,)

Composite measure

lo/II (Yl “A

x,/x (lOO”<,)

IX/19 (YS”,,)

Y,‘lO (YO”,,)

415 (X0”,,)

l3;‘lS (X7 ‘I,,)

0.79

Mouth asymmetry Visual field advantage

hemisphere

group

Left Female

performance

X/IO (X0 ‘I,,)

Both 16;‘21 (76”,,)

Estimated validity 0.17

‘?

effect; and

a significant task effect (individual means given below), listening showed a smaller overall right side bias. No other effect or interaction was significant. P> 0.2. Pearson correlations between the three laterality indices were (with I-tail probabilities corrected for performing three tests): mouth asymmetry with dichotic listening, i-0.12; mouth asymmetry with visual field, +0.25 (P> 0.05); dichotic listening with visual field, + 0.41 (PC 0.005). Moutlz usymmetry. An ANOVA for the mouth asymmetry index showed a significant side effect (mean f0.338, greater right mouth opening), F(1, 56)= 18.3, P 0.2. Dichotic listening. An ANOVA for the dichotic listening index showed a significant side effect (mean f0.064, right ear advantage), F (1, 56)= 3.57, P=O.O3. The hand effect was significant, F (1, 56) = 5.63, P=O.Ol (left handers showing less right ear advantage). Sex and the interaction were not significant, P> 0.3. Tuchistoscopic retidiny. For the tachistoscopic task, overall accuracy ranged from 35 to 75% with a mean of 54x, indicating that the method of adjusting duration to produce an approximate 5O’,I, error rate had been successful. An ANOVA for the visual field laterality index showed a significant side effect (mean +0.27X, a strong right visual field advantage), F (1.56)= 56.0. P 0.1. F (2, 55) = 8.8, P< 0.001, i.e. dichotic

DISCUSSION Indiriduul

meusures

Mouth asymmetry. Asymmetry in mouth opening during speech has been proposed as an indicator of underlying hemispheric asymmetry in neural control of articulation, i.e. of expressive language dominance [ 193. The present results provide a replication of the earlier studies in finding that 78’/, of the subjects showed greater opening of the right side of the mouth during speech. In the earlier data there was inconsistent evidence for a sex difference. The present results show only a weak, statistically nonsignificant, sex difference, which supports the previous interpretation that there is no strong sex difference in mouth asymmetry with a purely verbal task. Dichotic listenirzq. For a sample of dichotic listening studies, percentages of subjects with a

LANGUAGE

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LATERALlZATlOh

right ear advantage were, for right vs left handers, 65 vs 35% [S], 87 vs 69% [32], 90 vs 60% [40] and 72 vs 61% [22]. The present percentages, 77 vs 43x, appear representative. The sex difference in the present data (fewer females with a right ear advantage) was not significant, but a significant difference in the same direction has been reported [22]. Tachistoscopic reading. The present results with 78% of right handers showing a right visual field advantage appear to be typical, since percentages in the 70-80% range are common [3, 5, 14, 401, although 90% or higher has been reported [26, 271. While a significant effect of sex (weaker right visual field effects among females) has been reported [l, 21, one study [l] found that the sex effect disappeared when verbal report was used instead of lexical decision. The present study, using verbal report, is consistent in finding a small, non-significant sex difference. A handedness difference was not significant in the present data, consistent with previous studies [2,40]. Validity. Since the results for each individual measure were typical of previous results with these techniques, a comparison of their validities as indicators of language dominance was undertaken using the method of SATZ [31]. The simplest, and most common usage of laterality results as an indicator of language dominance just looks at the direction of the lateral difference. For example, any left ear advantage is taken as evidence for right hemisphere dominance. (This usage represents accepting laterality results at only the P< 0.5 level of significance.) With this approach, the three measures showed a “left hemisphere” pattern for 77-80x of the right handed subjects. The corresponding estimated validities were only 0.140.17, meaning that a prediction of right hemisphere language dominance for a right hander would be wrong five times out of six. Intercorrelations The three individual measures, even though each showed a “left hemisphere” bias, had quite low intercorrelations. The largest, and only significant, correlation was dichotic ear advantage with visual field advantage (f0.41). Previous studies [S, 12, 20, 21, 401 have found this correlation to be f0.39 or lower and seldom significant. On the basis of low intercorrelations between dichotic and tachistoscopic laterality measures, BRYDEN [S] and ELING [12] have suggested that cerebral dominance rather than being unitary, appears to be composed of several components. Alternative views have been presented [7, 331. Reliability

anul~xis und raliditl-

Recent articles [6, 9, 391 have argued for the utility of asking not just whether laterality data show any left vs right difference, but whether the difference is statistically significant for each subject. The percentages of subjects producing laterality results significant at the P~O.033 level ranged from 68% for mouth asymmetry to 35% for dichotic listening. The estimated validity based on results for right handers was 0.20 for mouth asymmetry (80% right side). Validity for 100% right side results in the dichotic and tachistoscopic data unfortunately cannot be estimated by Satz’ method. However, for the most meaningful evaluation of validity, it is necessary that all measures reliably classify a high percentage of subjects. The present results indicate that all three techniques must be improved to achieve this. Composite Results

measure with the composite

measure

were encouraging.

When data were accepted

at the

646

ROGERGRAVES

PcO.5 level, the composite measure predicted left hemisphere dominance for 87% of right handers, corresponding to an estimated validity of 0.28. This validity exceeds that of any individual measure. When the PC 0.033 criterion was used, a further large improvement in validity was made. The percentage of right handers with a “left hemisphere” result reached 95 % (18 of 19) closely approximating the 96 “/;, expected value. The estimated validity was 0.79, which is substantially higher than the 0.14-O. 17 found for the dichotomized individual measures. The relative percentages of right and left handers (95 vs 87%) showing “left hemisphere” results also looks more like the RASMUSSENand MILNER [29] results than do results from any of the three individual measures. Furthermore, the percentage of subjects with a reliable categorization (57%) was high given the poor sensitivity of two of the individual measures.

GENERAL

DISCUSSION

The results with the individual measures were representative of studies in the literature. When only the direction of lateral asymmetry was used, the three measures appeared to have equal but poor validity as indicators of language dominance. Requiring significant data for classifications resulted in some improvement and demonstrated the necessity of improved methodology. Results with the composite measure were surprisingly good. The number of reliable classifications (57 y;) was higher than for two of the component individual measures. Most importantly, the estimated validity (0.79) was very high for an experimental, non-invasive, measure. Why did the individual measures not find a right side bias for 96% of right handers? This is the percentage of left hemisphere dominant right handers found by RASMUSSENand MILNER [29] in their widely quoted report of results with the Wada procedure. There are at least three reasons why the individual measures could have low validity (and low intercorrelations) and why a composite measure may be more valid. While all three may act together, they will be described separately. The first possible reason for low validity is simply that the individual measures contain excess random “noise”, i.e. are unreliable. Demonstrating statistically reliable data [6,9, 391 will rule out this problem. Indeed, some studies have reported a high percentage of right ear advantage right handers when dichotic tests with high test-retest reliability [33] or with reliable classifications [39] were used. Increasing the number of trials is the simplest way to address this problem and a composite measure would be superior simply because it is based on more trials. The second possible reason for low validity is that there may be systematic error in each measure for a particular subject. For example, dichotic listening may be influenced by constant peripheral sensory system imbalance or attentional strategies, and improving the reliability of the data would not improve the measure’s validity. There are dichotic and tachistoscopic studies with good test-retest reliability which still obtained low percentages of right side advantage or, as in this study, a relatively low percentage of significant classifications [7, 8, 16, 391. Such results suggest that reliable cluss$‘cations (i.e. an asymmetry reliably different from zero) may not be possible for a substantial number of subjects even if the asymmetry itself is reliable. Innovations in methodology [e.g. 161 may overcome this problem. A composite measure would also tend to overcome this problem by “averaging out” the biases of each individual measure.

LANGUAGE

LATERALIZATION

647

The third possible reason for low validity is that the individual measures may not directly measure “language dominance” at all. If language dominance is not unitary [S, 121, it may be an emergent quality based on many underlying component functions, each of which is only weakly or inconsistently lateralized. Individual laterality techniques may most directly measure only one of these components. If this view is correct, even if each individual measure were reliable and valid for its specific function, it would not be a valid index for lateralization of overall language dominance. A composite score would be a better measure of language dominance because it would average over several of these functions. Clinical and anatomical results offer some support for this view. “Language dominance” is a construct which is based on observations that almost every aspect of language can be disrupted by extensive damage to the left side of the brain, but extensive damage to the right side results in little disruption of any aspect. One cannot conclude from this, however, that each of these aspects of language is strongly lateralized. The early locahzationists relied on the principle stemming from BOUILLAUD [35] that one could infer the existence of separate anatomical substrates and distinguish several “functions” only when each function could be observed to disappear in isolation following a different lesion. It is most interesting that in 150 years only three such major language functions have been distinguished and associated with distinct anatomical regions. These are: speech articulation associated with the posterior third frontal gyrus [4], word discrimination associated with the posterior first temporal gyrus [38] and reading/writing associated with the angular gyrus [IO]. The strength of the lateralization of these functions is not well established. For example, from the time of Broca and Wernicke to the present, cases of right handers with small lesions involving Broca’s or Wernicke’s area without the expected impairments have been found. In such cases duplication of function in the right hemisphere has been postulated [ 173. Recent observations of split-brain patients also demonstrate that the right hemisphere can have some word discrimination and reading ability [ 15, 241. It is remarkable that experimental psychology has discovered only three major types of language-related lateral asymmetries, mouth asymmetry, dichotic listening ear asymmetry and tachistoscopic visual field asymmetry, and that these asymmetries arise with the clinically defined functions, namely speech articulation, word discrimination and reading. It would appear then that the three laterality measures are most direct/y reflecting lateralization of the corresponding specific language functions. These specific functions (which concern “distal” input and output channels) may have independent degrees of lateralization within an individual. None of these may correspond well with “language dominance” (which presumably involves in addition more “central” aspects of language). Recent anatomical findings also appear to bear on this issue. The planum temporale in the human temporal lobe, which is assumed to serve auditory receptive language functions, has been found to be larger on the left side for 65582 0, of the cases [ 18, 371. If dichotic listening ear advantage depended on such an asymmetry, then a right ear advantage would be observed for only 65-82”; of subjects and ear advantage would have low validity as an index for “language dominance”. Another study [13] has measured both the planum and an area in the frontal lobe, approximately Broca’s region, which is assumed to serve expressive speech functions. This latter area was also found to be larger on the left in only about 75 Y,,of cases. Mouth asymmetry might depend on such an underlying anatomical asymmetry. Most interestingly, if one calculates the correlation between the reported anatomical asymmetries (expressed as percentages), the result is r= - 0.19. That is, a relatively large left Broca’s area did not imply a relatively large planum temporale. Anatomical effects like this could underly

648

ROGER GRAVES

the low correlations between different laterality indices found in the present data and in other studies [S, 12, 20, 21,401. At present, no local anatomical difference has been found which shows a hemispheric difference for 96 ‘A of right handers. It is noteworthy that none of the cases [13] had both speech regions larger on the right, which suggests that a measure of overall language dominance may have to be sensitive to both perceptual and expressive functions. If language dominance results from a summation of many small and uncorrelated asymmetries, then performance measures of language dominance would also require sensitivity to a range of underlying functions. Acknowle~~emenrs~This study was supported by faculty research Grant No. l-45835 from the University of Victoria. Portions of this work were presented to the Eleventh Annual Meeting of the International Neuropsychological Society, February 1983.

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