Ncuropsycho) c >gy 1994, Vol. 8, No.

2, 148-159

Copyright 1994 by the American Psychological Association. Inc. 0894-41 Or>/94/$3.(X)

Distributions of Hemispheric Asymmetry in Left-Handers and Right-Handers: Data From Perceptual Asymmetry Studies
Hongkeun Kim
Although hemispheric asymmetry among individuals is often treated as a categorical variable with 3 values (i.e., left hemisphere dominance, right hemisphere dominance, and bilateral dominance), it is best viewed as a continuously distributed variable ranging from strong asymmetry in favor of the left hemisphere through nearly equal asymmetry to strong asymmetry in favor of the right hemisphere. The present study compared distributions of hemispheric asymmetry in left-handers and right-handers, based on behavioral indexes of hemispheric asymmetry, such as visual field asymmetry on divided visual field tasks and ear asymmetry on dichotic listening tasks. Metaanalyses of prior studies using these indexes indicate that distributions of hemispheric asymmetry in left-handers and right-handers differ both in the mean and in the variance. Right-handers have greater mean hemispheric asymmetry than left-handers, whereas left-handers have greater variance in hemispheric asymmetry than right-handers. Within left-handers, those without sinistral relatives have greater variance in hemispheric asymmetry than those with sinistral relatives, suggesting that sinistral patterns of hemispheric asymmetry determined by environmental factors may be more variable than those determined by genetic factors.

Evidence indicates that in a majority of the population, the left hemisphere is superior to the right hemisphere for language functions, whereas the right hemisphere is superior to the left hemisphere for visuospatial functions (for a review, see Beaton, 1985). However, in a substantial minority of the population, hemispheric asymmetry does not follow this pattern (Annett, 1964; Bishop, 1990a; Geschwind & Galaburda, 1987; McManus & Bryden, 1991). The minority with anomalous types of hemispheric asymmetry may show a reversed direction of hemispheric asymmetry or various degrees of bilateralization of language and visuospatial functions. Individual variations in hemispheric asymmetry have been ascribed to a multitude of factors, such as heredity (e.g., Annett, 1964; Levy & Nagylaki, 1972), cytoplasmic left-right gradient (Morgan & Corballis, 1978), fetal testosterone levels (e.g., Geschwind & Galaburda, 1987), loss of callosal axons (Witelson & Nowakowski, 1991), birth stress (e.g., Bakan, 1971), early brain insult (e.g., Satz, 1973), chance factors during the course of development (e.g., Annett, 1972), and so forth. Clinical studies indicate that the incidence of anomalous types of hemispheric asymmetry is elevated in left-handers relative to right-handers (e.g., Bryden, Hecaen, & DeAgostini, 1983; Hecaen, DeAgostini, & Monzon-Montes, 1981). Thus, cases of aphasia following right hemisphere damage are more frequent in left-handers than in righthanders (for a review, see Carter, Hohenegger, & Satz, 1980; Segalowitz & Bryden, 1983). Rasmussen and Milner
I am grateful to Lucia A. French for improvement of the English text. Correspondence concerning this article should be addressed to Hongkeun Kim, Department of Psychotherapy, College of Rehabilitation Science, Taegu University, Nam-Taegu, P.O. Box 21, Taegu, South Korea.
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(1975) used sodium amytal testing to determine lateralization of speech in a group of right-handed epileptic patients and a group of left- and mixed-handed epileptic patients. Of 140 right-handed patients tested, 134 (96%) had speech in the left hemisphere, 6 (4%) had speech in the right hemisphere, and none had evidence of bilateral control of speech. Of 122 left- or mixed-handed patients tested, 86 (70%) had speech in the left hemisphere, 18 (15%) had speech in the right hemisphere, and another 18(15%) had bilateral control of speech. On the basis of the incidence of dysphasic symptoms following unilateral electroconvulsive therapy in severely depressed patients, Warrington and Pratt (1973) reported estimates of the incidence of left, right, and bilateral control of speech in left- and right-handers similar to those of Rasmussen and Milner (1975). The elevated incidence of anomalous types of hemispheric asymmetry in left-handers shows that handedness is associated, albeit imperfectly, with hemispheric asymmetry. This association presumably reflects common factors (e.g., genetic factors, early brain insult) affecting lateralization of both handedness and cerebral functions in at least some individuals. For example, genetic factors determining lateralization of hemispheric functions may also code for lateralization of handedness (e.g., Annett, 1964, 1972, 1982). Early brain insult, depending on lesion location and size, may lead to changes in both handedness and hemispheric asymmetry (Bishop, 1990a; Rasmussen & Milner, 1975). Clinical studies and, to a lesser extent, normal studies comparing hemispheric asymmetry in left- and right-handers have often treated hemispheric asymmetry among individuals as a categorical variable with three values: left hemisphere dominance, right hemisphere dominance, and bilateral dominance (Bryden et al., 1983; Rasmussen & Milner, 1975; Warrington & Pratt, 1973). However, as

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149

individuals may vary in degree as well as direction of hemispheric asymmetry, hemispheric asymmetry is best viewed as a continuum ranging from strong asymmetry in favor of the left hemisphere through nearly equal asymmetry to strong asymmetry in favor of the right hemisphere (Eling, 1981; Harshman & Lundy, 1988; McManus, 1983; Segalowitz, 1987; Shankweiler & Studdert-Kennedy, 1975). There are several sources of evidence for the notion of hemispheric asymmetry as a continuously distributed variable. First, handedness, a variable known to be associated with hemispheric asymmetry, is continuously distributed (e.g., Shankweiler & Studdert-Kennedy, 1975). Second, in commissurotomized patients, the level of skills in right hemisphere language varies considerably (e.g., Gazzaniga, 1983). Third, a proportion of variations in degrees of aphasic disturbance following unilateral brain damage has been ascribed "to the degree of dominance of one hemisphere in relation to lateralized processes such as speech production" (Luria, 1966, cited in Eling, 1981, p. 321). Finally, implicit in the construct of bilateral speech dominance is the notion that both hemispheres contribute in varying degrees to speech production (Snyder, Novelly, & Harris, 1990). Thus, despite the common practice of treating hemispheric asymmetry as a categorical variable, it is best viewed as a continuously distributed variable among individuals. If it is accepted that hemispheric asymmetry is a contin uously distributed variable, the most informative approach to comparing hemispheric asymmetry in left-handers and right-handers would be to compare their distribution characteristics, such as means and variances. Although there are a number of a priori possibilities in which distributions of hemispheric asymmetry in left-handers and right-handers might differ, four possibilities are considered here. They are illustrated in the four panels of Figure 1. Note that normal distributions are assumed in all cases and that illustrations were constructed to depict distributions of hemispheric asymmetry for a left-hemisphere specialized language task. First, distributions of hemispheric asymmetry in left- and right-handers may have the same mean and the same variance (see Figure 1 a). This possibility can be regarded as a null hypothesis to be tested against other alternative hypotheses. Second, the two distributions may have the same mean but different variances, with the variance for left-handers greater than the variance for right-handers (see Figure Ib). Third, the two distributions may have the same variance but different means, with the mean for right-handers greater than the mean for left-handers (see Figure Ic). Finally, the two distributions may have different means and different variances, with the mean for right-handers greater than the mean for left-handers and the variance for left-handers greater than the variance for right-handers (see Figure Id). The first of these four a priori possibilities, namely, that the two distributions have both the same mean and the same variance, is ruled out by clinical data indicating an elevated incidence of anomalous types of hemispheric asymmetry in left-handers relative to right-handers (e.g., Rasmussen & Milner, 1975). However, on the basis of the clinical data alone, it is not possible, or is at best difficult, to distinguish

LH

Figure I. Four hypothetical distributions of hemispheric asymmetry for a left hemisphere specialized task in left- and righthanders. For simplicity of presentation, the difference in population proportions between left- and right-handers is ignored. R = right-handers; L = left-handers; LH = left hemisphere superiority; RH = right hemisphere superiority; and f = frequency.

among the remaining three alternatives. What is needed to distinguish among the three alternatives is a continuously distributed index of hemispheric asymmetry, that is, an index reflecting individual variations in degree as well as direction of hemispheric asymmetry. A candidate for such an index is behavioral indexes of hemispheric asymmetry, such as visual field asymmetry on divided visual field tasks and ear asymmetry on dichotic listening. These indexes, computed as the difference between right- and left-sensoryfield scores or the transformations of such a difference (for a review, see Sprott & Bryden, 1983), are naturally continuously distributed and shown to be related, albeit not perfectly, to patterns of hemispheric asymmetry as measured by sodium amytal testing or other neurological procedures (e.g., Geffen & Caudrey, 1981; Hugdahl & Wester, 1992; Kimura, 1961; Strauss, 1988; Zatorre, 1989). However, there may be some objections to the use of behavioral indexes of hemispheric asymmetry in comparing distributions of hemispheric asymmetry in left- and righthanders because these indexes are not perfect indicators of hemispheric asymmetry (Colbourn, 1978; Efron, 1990; Richardson, 1976; Satz, 1977; Schwartz & Kirsner, 1984). Evidence indicates that perceptual asymmetry reflects not only hemispheric asymmetry but also other extraneous variables, such as attentional biases (e.g., Kim & Levine, 1992; Kim, Levine, & Kertesz, 1990; Levine, Banich, & KochWeser, 1984; Levy, Heller, Banich, & Burton, 1983a), sensory pathway dominance (e.g., Efron, 1990; Lauter, 1983; Sidtis, 1982), random errors in measurements (e.g., Chiarello, Dronkers, & Hardyck, 1984; Kim, in press; Teng, 1981), and so forth. However, it may be assumed, in the

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HONGKEUN KIM standard deviation of .74 (cf. Segalowitz & Bryden, 1983). Thus, right-handers may have greater mean hemispheric asymmetry than left-handers, whereas left-handers may have greater variability in hemispheric asymmetry than right-handers. The primary goal of the present study was to investigate whether left-handers have a greater variance in perceptual asymmetry than right-handers, which would be consistent with the hypothesis that left-handers have a greater variance in hemispheric asymmetry than right-handers. A preliminary review of potentially relevant prior literature revealed that in a substantial number of these studies, variance data were either directly reported in the text (though not statistically tested) or could be calculated from other results listed. Thus, it was determined that the question of variance differences between left-handers and right-handers could be addressed by reanalyzing available data from prior studies rather than by performing another not-so-new experiment. Results obtained from reanalyzing prior studies were then integrated across studies through a quantitative meta-analytic procedure. In addition, mean differences reported in the literature were also tabulated and then integrated across studies, using quantitative meta-analysis. Although it is known that left-handers typically yield a weaker mean perceptual asymmetry than right-handers (for a review, see Annett, 1982), a meta-analysis of this finding has not yet been carried out. Finally, the present study addressed the possible relevance of familial sinistrality (FS), defined as the incidence of one or more left-handers among first-order (and sometimes second-order) relatives, in determining hemispheric asymmetry, especially in left-handers. On the premise that FS provides an index of the likelihood that a left-hander has a genetic predisposition to left-handedness and related patterns of sinistral hemispheric asymmetry, left-handers with left-handed relatives (FS + ) may include more cases whose hemispheric asymmetry was determined by genetic factors than will left-handers without left-handed relatives (FS-). Numerous studies have been conducted comparing the mean perceptual asymmetry of FS+ and FS- left-handers, with little agreement among studies (for a review, see Annett, 1982; Bryden, 1988b; McKeever & Van Deventer, 1977). Thus, there appear to be at best weak differences between FS+ and FS- left-handers in mean hemispheric asymmetry. However, it has not been determined whether the two subgroups differ in the variance of hemispheric asymmetry. Sinistral patterns of hemispheric asymmetry determined by environmental factors may be more variable than those determined by genetic factors, reflecting a multitude of environmental factors that could potentially affect lateralization of cerebral functions, for example, high fetal testosterone levels, birth stress, early brain insult, chance factors during the course of development, and so forth. If this is the case, FS- left-handers may have greater variance in hemispheric asymmetry than FS+ left-handers. The present study made use of quantitative meta-analytic procedures. In a quantitative meta-analysis, statistical procedures are applied to a collection of empirical findings from individual studies for the purpose of integrating them

absence of evidence to the contrary, that these extraneous variables do not differentially involve left-handers and right-handers (Harshman & Lundy, 1988; Kim, 1992; Kim & Levine, 199la, 1991b; Segalowitz, 1987). With this assumption, influences of extraneous factors, even if they are robust, do not invalidate an attempt to compare distributions of hemispheric asymmetry in left- and right-handers on the basis of perceptual asymmetry. Instead, they indicate only that high statistical power (e.g., a large sample size) is necessary to show a statistical difference between left- and right-handers (Berenbaum & Harshman, 1980; Harshman & Lundy, 1988; Segalowitz & Bryden, 1983). A number of studies have compared perceptual asymmetry in left-handers and right-handers (for reviews, see Annett, 1982; Bryden, 1987, 1988b). These studies have typically reported that left-handers yield a reduced mean perceptual asymmetry relative to right-handers. That is, left-handers typically show a smaller mean right-sensoryfield advantage on verbal tasks and a smaller mean leftsensory-field advantage on spatial tasks. These results are consistent with the hypothesis that left-handers have a weaker mean hemispheric asymmetry than right-handers. Of the four possibilities depicted in Figure 1, these results rule out the second alternative as well as the first one, which suggest that distributions of hemispheric asymmetry in lefthanders and right-handers have the same mean (see Figure l a & Ib). Unfortunately, nearly all prior studies comparing perceptual asymmetry in left-handers and right-handers have only compared means, failing to test variance differences (for an exception, see Bryden, 1965). Thus, despite a large number of potentially relevant existing studies, it is not yet known whether left-handers have a greater variance in perceptual asymmetry than right-handers, which would be consistent with the hypothesis that left-handers have a greater variability in hemispheric asymmetry than right-handers. Of the four possibilities depicted in Figure 1, it is not yet possible to decide between the third alternative (that the two distributions for left- and right-handers have different means but the same variance; see Figure Ic) and the fourth alternative (that the two distributions have both different means and different variances; see Figure Id). To my knowledge, there has been only one study, reported by Bryden (1965), that compared variances of perceptual asymmetry in left- and right-handers. This study, using a verbal dichotic listening task, found a significantly greater variance for left-handers than for right-handers, consistent with the hypothesis that left-handers have greater variability in hemispheric asymmetry than right-handers. Thus, preliminary evidence indicates that distributions of hemispheric asymmetry in left- and right-handers have not only different means but also different variances. This is also suggested by the following theoretical illustration offered by Segalowitz and Bryden (1983). If we arbitrarily assign values of 1 to left hemisphere, -1 to right hemisphere, and 0 to bilateral control of speech to, for example, Rasmussen and Milner's (1975) findings, right-handers will yield a mean value of .92, with a standard deviation of .39, and left-handers will yield a mean value of .55, with a

HEMISPHERIC ASYMMETRY IN LEFT- AND RIGHT-HANDERS (Wolf, 1986). Glass, McGaw, and Smith (1981) noted that the findings of multiple studies should be regarded as a complex data set, no more comprehensible without statistical analysis than hundreds of data points in one study. Quantitative meta-analysis is becoming increasingly popular as a technique for evaluating studies within a given area of research, including laterality studies (e.g., Boles, 1984; Bryden, 1987, 1988b; Kim & Levine, 199Ib; Marzi, Bisiacchi, & Nicoletti, 1991). An important feature of metaanalysis is its high statistical power relative to individual tests of significance, which is, roughly speaking, due to the increased sample size. This feature of a meta-analytic procedure is particularly relevant for the present purpose. As discussed, evidence indicates that perceptual asymmetry reflects not only hemispheric asymmetry but also other extraneous variables, such as attentional biases, sensory pathway dominance, random errors, and so forth (for reviews, see Kim & Levine, 1991b; Segalowitz, 1987; Tzeng & Hung, 1985). Thus, a proportion of between-subjects variance in perceptual asymmetry stems from factors other than individual variations in hemispheric asymmetry. Moreover, patterns of hemispheric asymmetry in the majority of left-handers do not differ from those of a typical righthander (e.g., Rasmussen & Milner, 1975), suggesting an extensive overlap between distributions of hemispheric asymmetry in the two groups. Thus, to find a statistical difference between left- and right-handers, especially on the basis of perceptual asymmetry, high statistical power is necessary (Berenbaum & Harshman, 1980; Harshman & Lundy, 1988; McManus, 1984; Segalowitz & Bryden, 1983). Insofar as nonsignificant differences between lefthanders and right-handers in individual studies may be attributable to Type II errors (i.e., errors of incorrectly retaining a false null hypothesis) because of low statistical power, a meta-analysis may provide an opportunity to examine the differences with sufficient statistical power. F ratio:

151

(1)

where S\ is the variance for left-handers and 5r is the variance for right-handers. The F ratio also was used as an effect size estimator for the variance differences. Thus, an F ratio value of, say, 2, would indicate that sf is two times greater than sf The mean differences between left-handers and right-handers in perceptual asymmetry were tested with the following / ratio:

Mr-M,

(2)

where Mr is the mean for right-handers, M, is the mean for left-handers, nr is the number of right-handers, n, is the number of left-handers, and the other terms are as defined for Equation 1. Note that the standard error of differences is estimated differently from the usual / ratio. This adjustment was made because the present review indicated that S| and Sf are unequal and the usual standard error of difference is biased with unequal variances. The degrees of freedom used to test the t ratio also were adjusted for unequal variances (for specifics of this procedure, see Hinkle, Wiersma, & Jurs, 1988, p. 251). The effect size estimator for the mean differences, d, was defined as follows:

d=

Mr - M,

SDr

(3)

where SDr is the standard deviation for right-handers and the other terms are as previously defined. Thus, a d value of, say, 1, would indicate that the means for right-handers and left-handers are one standard deviation of the right-handers' distribution apart in the direction of the expected difference (i.e., a greater mean for righthanders than for left-handers).

Method Data Set

Included in the present review were those prior studies that compared the perceptual asymmetry of left-handers and righthanders under identical conditions and in which the variance data for each handedness group were either directly reported in the text or could be calculated from other results listed. A total of 22 studies meeting these criteria were located from the issues of the following journals published from 1965 to 1992: Brain and Cognition, Brain and Language, Cortex, and Neuropsvchologia. These studies provided 28 experiments, which constituted the data set for the present review. A total of 2,192 subjects ( 1 , 1 1 2 right-handers and 1,080 left-handers) participated in the experiments. Because data for male and female subjects could not be calculated separately for most experiments, the data were collapsed over sex.

Meta-Analyses
The meta-analytic procedure used in the present study was Stouffer's Z method. This method requires adding the standard normal deviates (zs) associated with the one-tailed ps obtained for each study and dividing that sum by the square root of the number of studies (N) being combined:

z=

(4)

Analyses of Individual Studies

The variance differences between left-handers and righthanders in perceptual asymmetry were tested with the following

The resulting Z is referred to the standard normal table for onetailed significance testing (Rosenthal, 1984). Meta-analyses were run separately for the following categories of studies: verbal divided visual field studies, verbal dichotic listening studies, and free-vision face studies. There were too few nonverbal divided visual studies or nonverbal dichotic listening studies to apply a meta-analytic procedure. For these studies, individual results only are considered. Including multiple results from the same subjects in a metaanalysis could inflate the sample size of statistical tests and effects beyond the number of independent studies (Rosenthal, 1984). In the present meta-analyses, six studies reported more than one set of

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HONGKEUN KIM

results relevant to the present meta-analyses by administering multiple laterality tasks to the same subjects. These studies were handled by first averaging the multiple results and entering the averaged value into the meta-analysis. However, some multiple results from the same subjects are included in two or more different meta-analyses. For example, two sets of results from the same subjects, one for a verbal divided visual field task and the other for a verbal dichotic listening task, are included in those two separate meta-analyses.

Results Divided Visual Field Studies

Nine studies included in the meta-analyses of verbal divided visual field studies are listed in chronological order in Table 1. These studies used letters, nonsense syllables, or words as stimuli. For each study, Table 1 lists numbers, standard deviations, and means for right-handers and lefthanders, respectively, with one-tailed ps for the variance difference and one-tailed ps for the mean difference. Left-handers showed a greater variance in visual field asymmetry than right-handers in eight of nine studies (89%). Reflecting this difference, the Stouffer's Z for the variance difference was significantly positive (Z = 3.815, p < .0001). The median value of F was 1.634; that is, on average, the variance of left-handers was about 1.6 times greater than the variance of right-handers. Right-handers had a greater mean visual field asymmetry (i.e., a greater mean right visual field advantage) than lefthanders in seven of nine studies (78%). Reflecting this difference, the Stouffer's Z for the mean difference was significantly positive (Z = 2.140, p < .05). The median value of d was .225; that is, on average, the means for left-handers and right-handers were about one-fourth of a standard deviation of the right-handers' distribution apart. In summary, meta-analyses of verbal divided visual field studies indicate that distributions of visual field asymmetry for verbal tasks in left-handers and right-handers have both different means and different variances. Right-handers have a greater mean right visual field advantage than left-

handers, whereas left-handers have a greater variance than right-handers. This pattern is illustrated in Figure Id. Only two nonverbal divided visual field studies (Heller & Levy, 1981; Kim et al., 1990) were available. Both studies used photographs of faces as stimuli. In Heller and Levy's (1981) study, left-handers had a greater variance than righthanders, whereas in Kim et al.'s (1990) study, the reverse was true. In neither case, however, was the variance difference statistically significant. In both studies, right-handers had a greater mean than left-handers (i.e., a greater left visual field advantage for right-handers). The mean difference was statistically significant only in Kirn et al.'s (1990) study (p < .05).

Dichotic Listening Studies

Thirteen studies included in the meta-analyses of verbal dichotic listening studies are listed in chronological order in Table 2, with associated statistics for each study. These studies used digits, nonsense syllables, or words as stimuli. Left-handers showed a greater variance in ear asymmetry than right-handers in 10 of 13 studies (77%). Reflecting this difference, the Stouffer's Z for the variance difference was significantly positive (Z = 3.900, p < .0001). The median value of F was 1.243. Right-handers had a greater mean ear asymmetry (i.e., a greater right ear advantage) than left-handers in 13 of 13 studies (100%). Reflecting this difference, the Stouffer's Z for the mean difference was significantly positive (Z = 9.114, p < .0001). The median value of d was .503. In summary, consistent with results of meta-analyses of verbal divided visual field studies, meta-analyses of verbal dichotic listening studies indicate that right-handers have a greater mean right ear advantage than left-handers, whereas left-handers have greater variance than right-handers (see Figure Id). Only one nonverbal dichotic listening study (Curry, 1967) was available. In this study, in which environmental sounds were used as stimuli, right-handers had both greater variance and a greater mean (i.e., a greater left ear advantage)

Table 1 Verbal Divided Visual Field Studies: Mean Perceptual Asymmetries and Standard Deviations for Right-Handers (RH) and Left-Handers (LH)
n
Study Bryden (1965) Orbach (1967) McKeever, Van Deventer, & Suberi (1973) McKeever & Van Deventer (1977) Bradshaw, Gates, & Nettleton (1977) Haun (1978) Bradshaw & Taylor (1979) Dagenbach (1986) Kim, Levine, & Kertesz (1990)

SD

M P P 0.725 -0.200 .146 3.160 1.095 .024 1.290 .136 3.000

2.613 2.127 .347

RH LH 20 25 48 80 24 12 24 50 31 20 21 24 71

RH
2.500 3.070 7.603 7.059

LH

RH

LH

2.950 .239 3.700 .190 5.300 .968

7.941 .155 .000

24 19.202 46.847

13.000

8.000 .316 8.930 15.500 2.540 3.060

.402 .018 .649 .705

9.800 12 6.207 10.238 .056 48 23.328 33.321 .033 30.000 124 1.290 2.450 1.650 .026 32 4.530 5.790 .091 2.350

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153

Table 2 Verbal Dichotic Listening Studies: Mean Perceptual Asymmetries and Standard
Deviations for Right-Handers (RH) and Left-Handers
n

(LH)

SD

M P
RH LH

P 20 20 0.210 0.450 .001 0.110 -0.090 .041 Bryden (1965) 2.400 .040 25 25 5.645 5.600 .515 5.240 Curry (1967) 4.530 .000 12 12 2.210 2.500 .345 10.280 Curry & Rutherford (1967) 52 41 22.279 22.296 .493 23.480 12.640 .011 Satz, Achenbach, Pattishall, &Fennell (1967) 11 8.300 8.100 .530 54.228 47.257 .030 11 Knox & Boone (1970) 0.750 .055 Briggs&Nebes(1976) 40 40 7.002 6.994 .503 3.275 3.645 .019 McKeever & Van Deventer 80 71 9.770 10.216 .349 7.080 (1977) 14.400 .245 Fennell, Satz, Van Den Abell, 26 42 10.200 12.150 .178 16.300 Bowers, & Thomas (1978) Hugdahl & Andersson (1984) 20 20 20.753 23.052 .326 20.000 -10.000 .000 0.125 .002 215 257 0.217 0.244 .036 0.187 Orsini, Satz, Soper, & Light (1985) 1.860 .011 1.200 0.580 .009 Dagenbach (1986) 50 124 1.390 0.134 .000 Bryden (I988a) 219 78 0.789 0.880 .113 0.554 Obrzut, Conrad, Bryden, 15 15 0.240 0.684 .000 0.363 -0.452 .000 & Boliek (1988)
Study

RH LH

RH

LH

than left-handers. However, neither of these differences was statistically significant. Free-Vision Laterality Studies The three studies included in the meta-analyses of freevision laterality studies are listed in chronological order in Table 3, with associated statistics for each study. These studies used the free-vision chimeric face task developed by Levy, Heller, Banich, and Burton (1983b) or a similar face-processing task. This task involves judging which of the two mirror-imaged chimeric faces, one with a smile to the subject's left or one with a smile to the subject's right, looks happier. Subjects as a group show a strong bias to choose the face with the smile to their left as looking happier (for details of this task, see Levy et al., 1983b). Left-handers showed a greater variance in perceptual asymmetry for this task than right-handers in all studies. Reflecting this difference, the Stouffer's Z for the variance difference was significantly positive (Z = 1.809, p < .05). The median value of F was 1.360. Right-handers had a greater mean perceptual asymmetry (i.e., a greater leftward bias) for this task than left-handers

in all three studies. Reflecting this difference, the Stouffer's Z for the mean difference was significantly positive (Z = 3.494, p < .0001). The median value of d was .384. In summary, consistent with the results of the metaanalyses of verbal divided visual field studies as well as of verbal dichotic listening studies, the meta-analyses of nonverbal free-vision face studies indicate that right-handers have a greater mean leftward bias than left-handers, whereas left-handers have greater variance than right-handers (see Figure Id). Familial Sinistrality
In 6 of 22 studies, it was possible to compare means and variances in visual field or ear asymmetries for FS+ righthanders and FS- right-handers, and in 8 of 22 studies, it was possible to compare means and variances for FS+ lefthanders and FS- left-handers. These studies are listed in Table 4, with associated statistics for each study. Half of these studies were verbal divided visual field studies and the other half were verbal dichotic listening studies. Because of the relatively small number of studies available, divided visual field and dichotic listening studies were analyzed

Table 3 Free-Vision Face Studies: Mean Perceptual Asymmetries and Standard Deviations for Right-Handers (RH) and Left-Handers (LH)
n

SD

M P
.094 .163 .201

Study Levy, Heller, Banich, & Burton (1983b) Hoptman & Levy (1988) Kim, Levine, & Kertesz (1990)

RH
111 40 31

LH
111 40 32

RH
.440 .558 .548

LH
.499 .654 .639

RH
.303 .354 .259

LH
.134 -.027 .157

P
.004 .003 .249

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HONGKEUN KIM Table 4 Mean Perceptual Asymmetries and Standard Deviations for Subjects With No Familv History of Sinistratify (FS-) and Subjects With Such History (FS+)

n
Study
FS- FS + FS-

SD
FS +

M P
FSFS +

Right-handers Verbal divided visual field studies McKeever, Van Deventer, 24 & Suberi (1973) 44 McKeever & Van Deventer (1977) Kim, Levine, & Kertesz (1990) 22 Verbal dichotic listening studies 44 McKeever & Van Deventer (1977) Orsini, Satz, Soper, 145 & Light (1985) 143 Bryden (!988a)
24 36 9 36 70 76

7.951

7.240 .328
6.711 .281

4.090
3.130 1.364

1 .910 .837 1 .980 .766 4 .778 .048 7.300 .429 0.200 .235
0.619 .186

7.388 4.007

5.069 .816

9.360 10.379 .742 0.240 0.800

0.160 .000

6.900
0.180

0.770 .361

0.520

Left-handers Verbal divided visual field studies Bryden (1965) 16 4 2.500 0.900 .059 0.440 -1 .750 .994 34 McKeever & Van Deventer 37 7.027 8.507 .865 0.470 3.650 .045 (1977) 24 24 39.192 26.954 .035 1 2.000 19 .000 .237 Bradshaw & Taylor (1979) 19 Kim, Levine, & Kertesz (1990) 13 6.780 4.130 .042 3.420 2,.530 .676 Verbal dichotic listening studies 16 4 0.370 0.720 .967 0.010 -0 .360 .808 Bryden (1965) 34 37 1 1 .662 8.587 .037 5.000 2.400 .854 McKeever & Van Deventer (1977) 141 116 0.270 0.210 .003 0.120 0 .130 .369 Orsini, Satz, Soper, & Light (1985) 143 76 0.800 0.770 .361 0.520 0 .619 .186 Bryden (1988a) together in the first meta-analyses. When significant effects emerged in the first analyses, the effects were then separately analyzed for divided visual field studies and dichotic listening studies. Meta-analyses of right-handers showed that FS+ and FSright-handers did not significantly differ either in mean perceptual asymmetry (Z = .714, ns) or in the variance of perceptual asymmetry (Z = 1.427, ns). Meta-analyses of left-handers showed that FS+ and FS- left-handers did not significantly differ in mean perceptual asymmetry (Z = 1.236, ns). However, FS- left-handers had a significantly greater variance of perceptual asymmetry than FS+ lefthanders (Z = 2.504, p < .01). In six of eight studies (75%), the variance for FS- left-handers was greater than the variance for FS+ left-handers. When divided visual field studies and dichotic listening studies were analyzed separately, the effect was significant for divided visual studies (Z = 2.002, p < .05) and approached statistical significance for dichotic listening studies (Z = 1.539, p < .10). The greater variance for FS- than FS + left-handers suggests that the greater variance found for left- than for right-handers may involve FS- left-handers more than FS + left-handers. Consistent with this hypothesis, FS- lefthanders had a significantly greater variance than righthanders (Z = 3.904, p < .0001), whereas no significant difference in variance emerged between FS+ left-handers and right-handers (Z = .811, ns).

Discussion
The present study addressed the question of whether distributions of perceptual asymmetry in left-handers and right-handers differ in the mean or in the variance or both. Meta-analyses of 28 experiments collected from the literature support the hypothesis that distributions of perceptual asymmetry in left- and right-handers differ both in the mean and in the variance. Whereas right-handers had greater mean perceptual asymmetry than left-handers, left-handers had greater variance around the mean than right-handers. This was true for a variety of laterality tasks: divided visual field tasks, dichotic listening tasks, and a free-vision face task. Of the 28 experiments considered, 26 (93%) yielded greater mean asymmetry for right-handers, 22 (79%) yielded greater variance for left-handers, and 20 (71%) yielded both a greater mean for right-handers and greater variance for left-handers. Perceptual asymmetry has been shown to be related, albeit not perfectly, to patterns of hemispheric asymmetry as measured by sodium amytal testing or other neurological procedures (e.g., Geffen & Caudrey, 1981; Hugdahl & Wester, 1992; Kimura, 1961; Strauss, 1988; Zatorre, 1989). Although evidence indicates that perceptual asymmetry reflects not only hemispheric asymmetry but also other extraneous variables, such as attentional biases, sensory pathway dominance, random errors, and so forth (Hellige, Bloch, &

HEMISPHERIC ASYMMETRY IN LEFT- AND RIGHT-HANDERS

155

Taylor, 1988; Kim & Levine, 1991b; Segalowitz, 1987; Tzeng & Hung, 1985), these extraneous variables may not differentially involve left-handers and right-handers (Harshman & Lundy, 1988; Kim et al, 1990; Segalowitz, 1987). Thus, the present pattern of results, that is, the greater mean perceptual asymmetry for right-handers and greater variance for left-handers, is consistent with the hypothesis that right-handers have greater mean hemispheric asymmetry than left-handers, whereas left-handers have greater variability in hemispheric asymmetry around the mean than right-handers. Another important finding in the present review is that FS- left-handers had greater variance in perceptual asymmetry than FS+ right-handers, suggesting a greater variability in hemispheric asymmetry for FS- left-handers. Also, the greater variance in perceptual asymmetry for leftthan for right-handers was due more to FS- left-handers than to FS+ right-handers. Relative to FS + right-handers, FS- left-handers may have included more cases in which handedness and sinistral patterns of hemispheric asymmetry were determined by environmental factors. On the basis of this premise, the greater variability in hemispheric asymmetry for FS- left-handers suggests that, at least within left-handers, patterns of hemispheric asymmetry determined by environmental factors are more variable than those determined by genetic factors. The greater heterogeneity in patterns of hemispheric asymmetry among FS- left-handers may reflect a multitude of environmental factors that could potentially induce sinistral patterns of hemispheric asymmetry, such as high fetal testosterone levels (e.g., Geschwind & Galaburda, 1987), birth stress (e.g., Bakan, 1971), early brain insult (e.g., Satz, 1973), chance factors during the course of development (e.g., Annett, 1972), and so forth. Bishop (1990a, 1990b) recently argued that it may be futile to subclassify left-handers into FS+ and FS types because familial sinistrality is an extremely weak indicator of whether or not a person's handedness or hemispheric asymmetry is influenced by genetic factors. However, the greater variance for FS- than FS+ left-handers shows that her conclusions may be premature. Although familial sinistrality may not be a perfect, or even strong, indicator of a left-hander's genetic predisposition to left-handedness, according to the present findings, the difference between FS 4and FS- left-handers in the proportion of so-called genetic left-handers is large enough to be statistically significant. Furthermore, the current genetic models of handedness and hemispheric asymmetry often postulate equal variance for distributions with and without a genetic bias (cf. Bishop, 1990a). This assumption may be in error given that FS + and FS- distributions differ in variance. Although the greater variance in perceptual asymmetry for left-handers is interpreted here as reflecting greater variability in hemispheric asymmetry, alternative interpretations are, of course, possible. For instance, it is often the case that subjects classified as right-handers typically include only strong right-handers, whereas subjects classified as left-handers include not only strong left-handers but also weak or mixed left-handers. According to this view, the

greater variance in perceptual asymmetry for left- than for right-handers may also reflect this factor. However, this view would predict equal variances in perceptual asymmetry for left- and right-handers in studies testing only strong left-handers and strong right-handers. In the present review, there were 11 experiments that tested only strong lefthanders and strong right-handers, and of these, 9 (82%) yielded greater variance for left-handers. Thus, the greater variance for left- than for right-handers is independent of some samples of left-handers that include both strong and weak left-handers. Another explanation for the greater variance for lefthanders may be that it is a methodological nuisance. From this point of view, the heterogeneity of variance should be eliminated by data transformation (e.g., log transformation) rather than be a subject of systematic investigation. However, in a great majority of studies reviewed, the variance differences were in the expected direction, that is, greater variance for left-handers, and in no case was the variance for right-handers significantly greater than the variance for left-handers. These systematic variance differences across studies are inconsistent with the view that they stem from methodological nuisance. As Bryk and Raudenbush (1988, p. 402) cogently argued, "The practice of routinely searching for data transformation that will eliminate heterogeneity is misguided, because it could lead to a failure to recognize the substantive significance of heterogeneity." The substantive significance of the present heterogeneity of variance is that it reflects greater variability in hemispheric asymmetry for left- than for right-handers. In passing, prior studies have routinely violated the assumption of homogeneity of variance in their testing of mean perceptual asymmetry differences between lefthanders and right-handers. Technically, unless the variance difference between two groups reaches statistical significance, it may not be a serious error to test the mean difference in a usual manner (for statistical means of testing mean differences with unequal variances, see, for example, Hinkle et al., 1988, p. 251). However, the present meta-analysis showed that the variances for leftand right-handers are significantly different, presumably reflecting greater variability in hemispheric asymmetry for left- than for right-handers. Thus, it may be safer not to assume equal variances, even when the variance difference between the two groups does not reach statistical significance. Although the present review was intended to examine distributions of hemispheric asymmetry for both lefthemisphere specialized verbal tasks and right-hemisphere specialized nonverbal tasks, there were too few nonverbal studies, except for free-vision studies, to apply a meta-analytical procedure. As Bryden (1987) noted, it is easy to assume, but not necessarily true, that "the functions of the right hemisphere are related to handedness in much the same way that language functions are, but in reverse" (p. 62). Thus, the present finding that distributions of hemispheric asymmetry in left- and right-handers differ in both mean and variance is generalizable more to

156

HONGKEUN KIM viewing that literature. For example, on average, about 82% of right-handers but only 64% of left-handers showed an expected right ear advantage for verbal dichotic listening tasks (Bryden, 1987). This finding presumably reflects differences in cerebral organization between the two groups. However, in essence, by dichotomizing an essentially continuous variable, this approach does not take full advantage of information about hemispheric asymmetry contained in perceptual asymmetry. Moreover, as Bryden (1987) was aware, classification of subjects according to their direction of sensory field advantage could give a false implication that subjects are being classified according to their direction of hemispheric dominance. In reality, a left ear advantage, for example, is not an index of right hemisphere dominance but merely increases the likelihood of right hemispheric dominance relative to a right ear advantage (Satz, 1977; Speaks, 1988). My final comments concern why nearly all previous laterality studies have failed to address the question of variance differences between left-handers and right-handers. This question is rather curious, particularly because one of the earlier studies, reported by Bryden (1965), specifically addressed the question and found significantly greater variance for left-handers. However, neglect of questions regarding variance differences or, more broadly, individual differences is not limited to the laterality literature but occurs in many other areas in experimental psychology (Bryk & Raudenbush, 1988). Historically, there have been two traditions in psychologyone that has the goal of characterizing the modal human being and the other that has the goal of characterizing individual differences (Cronbach, 1957). In the former, nomothetic tradition, individual differences have often been viewed "as a methodological nuisance or an unwelcome obstacle in the pursuit of inferences about the effects of treatments on means" (Bryk & Raudenbush, 1988, p. 396). The neglect of questions regarding variance differences between left- and right-handers may be an unfortunate legacy of this tradition (see Kim & Levine, in press). In conclusion, in reading the laterality literature, one often encounters such statements as "Left-handers are less lateralized than right-handers." This statement is highly ambiguous because it could mean that each individual left-handed person has less differentiated patterns of hemispheric asymmetry than each individual right-handed person, or it could mean that left-handers are more variable in their lateralization than right-handers, or it could mean something else (Annett, 1982; Colbourn, 1978; Harshman, 1988; McManus, 1983). In fact, when hemispheric asymmetry is conceptualized as a continuously distributed variable, as it should be, it does not make a great deal of sense to ask whether one group of individuals is more or less lateralized than another group. Instead, one should be asking whether distributions of hemispheric asymmetry in the two groups differ in the mean, in the variance, or in both. The present study allows specific answers to such questions regarding left-handers and right-handers. That is, right-handers have greater mean hemispheric asymmetry than left-handers, whereas left-handers have greater variance in hemispheric

distributions of hemispheric asymmetry for verbal functions than to distributions of hemispheric asymmetry for nonverbal functions. Nonetheless, it is notable that the present meta-analyses of nonverbal free-vision studies yielded results comparable to those of the verbal laterality studies. That is, on the nonverbal face-processing task, right-handers showed greater mean perceptual asymmetry (i.e., a greater leftward bias) than left-handers, and left-handers showed greater variance than righthanders. Although free-vision modality is not a common type of laterality task, it has been shown that perceptual asymmetries on free-vision tasks are significantly correlated with those on divided visual field tasks (Kim & Levine, 1991b; Kim et al., 1990; Levy et al., 1983a). Thus, further studies may indicate that distributions of hemispheric asymmetry in left- and right-handers differ in both mean and variance not only for verbal functions but also for nonverbal functions. Although the majority of experiments included in the present review yielded the expected patterns of results (i.e., greater mean perceptual asymmetry for right-handers and greater variance for left-handers), the number of experiments in which these results reached statistical significance was relatively small. In particular, only 16 of 28 experiments (57%) showed a significantly greater mean for righthanders at the p < .05 level (one-tailed), and only 8 of 28 experiments (29%) showed significantly greater variance for left-handers at the same p level. This is not surprising because high statistical power or a large sample may be necessary to show a statistical difference between lefthanders and right-handers (Berenbaum & Harshman, 1980; Harshman, 1988; Segalowitz & Bryden, 1983). In fact, analyses of sample size showed that, on average, those experiments yielding significant differences had larger samples (M = 55.5 right-handers and 58.2 left-handers) than those yielding nonsignificant differences (M = 32.6 right-handers and 30.8 left-handers), suggesting that a small sample contributes to a lack of statistically significant effects. It also is of some interest that more significant mean differences were found than significant variance differences. One possibility may be that higher statistical power is necessary to demonstrate significant variance differences than significant mean differences. Alternatively, and perhaps more parsimoniously, this pattern may be related to the fact that studies supporting the null hypothesis are less likely to be published (Rosenthal, 1979). Because prior studies have reported only mean differences between leftand right-handers, failing to test variance differences, this publishing bias, if it exists, may also have biased the present sample of studies with respect to mean differences but not with respect to variance differences. As a result, the present sample of studies may include more cases of significant mean differences than significant variance differences. In an alternative approach to the present review, Bryden (1987, 1988b) used the fact that many studies report how many left-handers or right-handers show a left or right ear advantage on dichotic listening tasks as the basis for re-

HEMISPHERIC ASYMMETRY IN LEFT- AND RIGHT-HANDERS asymmetry than right-handers. FS- left-handers have greater variance in hemispheric asymmetry than FS+ lefthanders, suggesting that sinistral patterns of hemispheric asymmetry determined by environmental factors may be more variable than those determined by genetic factors. To the extent that meta-analyses are less subject to sampling error, measurement error, low statistical power, and other artifacts than are individual studies (Schmidt, 1992), the present findings represent a reliable characterization of distributions of hemispheric asymmetry in left- and righthanders.

157

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Received June 21, 1993

Accepted August 19, 1993

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