A directional bias for studies of laterality

A directional bias for studies of laterality

CO28-3932/X9 $3.00+0.00 PergamonPress plc Neuropsychologlo, Vol. 27. No. 2, pp. 251-257, 1989 Prmtedm GreatBritain. NOTE A DIRECTIONAL BIAS FOR ST...

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CO28-3932/X9 $3.00+0.00 PergamonPress plc

Neuropsychologlo, Vol. 27. No. 2, pp. 251-257, 1989

Prmtedm GreatBritain.

NOTE A DIRECTIONAL

BIAS FOR STUDIES

OF LATERALITY

ISABELLE ALTER,* STEPHANIE REINt and ALFREDO TORO*

*Brain Research

Laboratories, Department of Psychiatry, NY 10016, U.S.A.; and tDalton

NYU Medical Center, 550 First Avenue, New York, School, New York, U.S.A.

(Received 22 May 1987; accepted

6 May 1988)

Abstract-We have shown that a directional bias (D), previously thought to be unrelated to cerebral lateralization, is, in fact, intimately associated with it. In a group of fully consistent dextrals without familial sinistrality, the direction of lateral asymmetries depended upon the direction of D. Leftdirected dextrals manifested the usual visual field advantages for linguistic and spatial material, while right-directed dextrals did not. D is therefore recommended as moderator variable for future studies of laterality.

INTRODUCTION SEKE HANDEDNESS, which is still our best non-invasive marker for speech representation, is an imperfect predictor of behavioral asymmetries, the search has persisted for “moderator” variables for handedness, that is, for subject characteristics that might reduce the observed variance. In this study, we introduce as moderator variable a directional bias whose population characteristics are described elsewhere [l-3]. These characteristics strongly suggest a relation between directionality (D) and cerebral lateralization. The present report is an initial attempt to demonstrate that the task we devised to assess directionality can enhance the predictive accuracy of existing subject variables, such as handedness and familial sinistrality. Toward that end, we administered standard laterality tasks, the tachistoscopic presentation of nonsense syllables and differing line orientations, to a group of strongly right-handed individuals with no known familial sinistrality: the major difference from the standard approach being that our right-handers were selected so that half were directionally biased towards the left (LD) and half toward the right (RD). Our dextral group was evenly divided between LD and RD so as to differentiate directionality from handedness; these are not the usual proportions of directional bias in a dextral population 131. Figure 1 shows what the distribution for D might look like for a random sample of consistent right-handers without familial sinistrality, drawn from the age group commonly used in laterality experiments. The graph tells us (when D scores are 1 IO.671 so as to include only strongly directional individuals) that approx. 70% of randomly selected dextrals are left-directed, with less than 20% being right-directed. Thus, if D were predictive ofperformance for a group of randomly selected dextrals in a standard laterality experiment, we should have a larger group of subjects displaying a preference for one visual field, while the remainder should show a different preference. It is the case that, on the average, 70% of dextrals display the expected visual field advantage [lo], while the remaining subjects do not. We shall argue that directionality contributes to the variance in laterality experiments by demonstrating that D is predictive of visual field advantage (VFA). Since a directional bias toward the left (LD) constitutes the “norm” among the right-handed [3], it might be anticipated that this group of right-handers would demonstrate the expected directional asymmetries-namely, a right VFA for linguistic, and a left VFA for spatial stimuli, while rightbiased (RD) individuals would not.

METHOD Subjects

Thirty-two undergraduate students from Bryn Mawr and Haverford Colleges, ranging in age from 17 to 23 yr, were tested. Subjects were selected so that there were eight females and eight males in each of two directionality 251

NOTE

252

60 1

--I.00-0.67 -0.33

0

to.33 i-O.67t1.00

D Score FIG. 1. The distribution

ofdirectionality (D) scores for 28 randomly selected dextral subjects, wlthout familial sinistrals. is shown by the curve connecting the dots. These subjects were extracted from the population described in the accompanying ariicle (ALTER, 131). In contrast, each hatched bar represents 50% of the 28 subjects used in the present study. These wire also dextrals without f.lmilial sinistrality but had been selected, in addition, for their strong directional tendencies. Negative and positive D scores refer to left- and right-directed individuals, respectively.

groups. LD and RD. All subjects were consistently right-handed. as determined recornmendzd by BKYDEY [7], and had no known familial sinistrals.

by a five-item

questionnaire

Subjects were selected on the basis of their directionality score. Six sketche.r were rcquircd ofa potential subject (of a bicycle, dog walking, bus. facial profile. airplane. pitcher), each drawn on a separate sheet of paper, as rapidly as possible. D (for directionality) was scored as (R-L),‘(R+L j, where R and t are the number of right- and leftoriented objects, respectively. Scores would thus range from - I .OO (consistent LD) to + 1.OO(consistent RD). Only those subjects demonstrating a consistent left- or rightward orientation were accepted for participation in the study. Subjects were retested for D just prior to experimental testing. Small shifts (from 6,‘6 to 5,‘6 drawmgs in one direction) wcrc observed in several subjects. The one subject who rcverscd direction was discarded.

A two-channel oriented lines.

Stoeitlng

tachistoscopc

was used to present

two sets of stimuli,

(a) nonsense

syliablzs

and (b!

(11) ~von.~e,s, S~/h/h. Subjects were required to identify a three-letter nonsense syllable prcscntcd to the left or right visual field. The syllables were of the CVC, or consonant vowel&consonant variety, selected from NotILt. [14] for their low association value. The CVC trigrams were constructed from 4X-point Helvetica Medium Lctraqct. SIxteen syllables were presented once in each field for a total of 32 trials. The syllables were prescntcd vertically, ccntcrcd at 2’ from the ccr,tral fixation point, and subtended a visual angle of approximately 2.8 (h) Line orimtufion. Subjects were required to match the line orientation exposed In the left or right visual field. Eight oriented lines were selected from the set provlaed by BENTOV er cd. [4] for judgment of lint orientation. Vertical and horizontal lines were omitted to minimize verbal encoding. The lines, drawn in black ink, were inclined at .!O. 35.55.75, 110. 125, 145, and 160 l&h line orientation was presented twice in each field for a totnl of 32 trial\. Line length subtended an angle of approx. 1.3 Each line was centered at 2 from fixation. A display of the X line orientations. 4 per row, was presented above the viewer for matching line orientation. A central fixation digit. randomly selected from 1 to 9. was used in conjunction with each stimulus, and sub:endcd a vertical angle of approx. 0.5’. A prc- an.I post-exposure field contamed a cenrered asterisk to provlde for visual fixation during intertrial intervals.

Eight practice stimuli. 4 ofcach type. were presenied prior to formal testing. The pre-exposure field was displayed for an average of 4 sec. after which it was replaced by the stimulus card containing both central digit and unilateral stimulus. Stimulus exposure duration centered on an average of 150 msec. All viewing was binocular. Subjcc:s were instructed to fixate the pre-exposure fixation design. and to report the central digit before identifying the stimulus itself. Responses following an incorrect (or missed) report of the fixation digit were not scored. Nor were trials with unreported fixation replaced. As a consequence, one subject with an excessive number of lost trials (I 3 of 16) was discarded. This being the second subject eliminated from two separate groups (one had been dropped earlier for a reversal of D), two other subjec::;, one from each of the remaining groups, were ehminated from the roster to simplify

253

NOTE

analysis: these were subjects with the worst overall performance in their respective groups. This resulted in a total n = 28,7 in each group. There were 64 trials per session, 32 CVCs and 32 line orientations. In order to prevent the development of taskrelated attentional or strategy effects, the CVC and line stimuli were randomly intermingled. They were presented in the same sequence to each subject. Trials were randomized so that no more than 4 trials appeared sequentially in the same visual field and no more than 4 trials were of the same stimulus type. Responses were scored for correctness of syllable and line orientation identification in each visual field. CVC trigrams were scored in all-or-none fashion, with no credit given for partially correct answers.

RESULTS A MANOVA was performed on lambda (A), the laterality metric based on the log odds ratio, proposed by BRYDEN and SPROT~ [9].* Independent variables were directionality and gender, and dependent variables were measures on the two laterality tasks, CVC syllables and judgment of line orientation. The MANOVA yielded a significant overall effect for (D) directionality (F(2, 23)=6.5, P
Table 1. Performance

of LD and RD dextrals

on CVC identification

LD Subject

RD

(%) LVF

(%) RVF

46 82 50 62.5 43 64 44 56

56 100 73 75 86 85 53 75

n Females 0.4055 0.7985 1.0116 0.5878 2.0794 1.1451 0.3848 0.7904*

Subject

(%) LVF

(X) RVF

i.

I5 16 17 18 19 20 21 x

62.5 79 57 67 62.5 50 87.5 67

50 87.5 64 57 69 33 69 61

-0.5108 0.6466 0.3001 -0.4055 0.2776 -0.6931 -1.1575 -0.2179*

22 23 24 25 26 27 28 x

71 77 45 87 75 87.5 87.5 76

69 60 43 87 69 92 85 72

-0.1278 -0.7985 -0.1054 0 -0.2877 0.5390 -0.2412 -0.2257*

Males 8 9 10 II I2 13 14 Jz *Overall

38 50 93 53 70 47 60 59 1 for the group

50 94 87.5 44 93 62.5 67 71

0.4700 1.6094 - -0.6931 _ -0.3848 1.7918 0.6444 0.2877 0.4001*

[9].

The table shows that all 7 females and 5 of 7 males in the LD groups displayed a right VFA (86% of LD subjects). In contrast, only 3 out of 7 females and 1 of 7 males in the RD groups (28%) displayed a right VFA. For the combined performance of males and females, all consistent dextrals, only 57% displayed the anticipated direction of asymmetry.

*MANOVA was performed square criterion [9].

once homogeneity

of lambda

had been established

for each subgroup,

using the Chi

254

NOTE

Line orientation. The ANOVA on i., performed forjudgment of line orientation, yielded no significant main effects of directionality or gender.* However, the directionality by gender interaction fell just short of significance (F (1, 24)=3.10, 0.05 < P
of LD and RD dextrals

on judgement

of line orientation

LD Subject

RD 1

(X) LVF

(%) RVF

53 57 69 67 37.5 62.5 44 56

81 67 69 60 31 81 94 69

Females 1.3328 0.4055 0 -0.2877 -0.2776 0.9555 2.9594 0.4987*

71 78.5 41 75 78.5 75 94 74

94 87.5 62.5 61 62.5 67 50 70

1.7918 0.6466 0.6444 -0.4055 -0.7885 -0.4055 -2.7081 -0.1519*

(%) LVF

(X) RVF

i

15 16 17 18 19 20 21 x

37.5 75 69 77 87.5 75 80 72

69 61 62.5 75 81 67 62.5 69

1.2993 -0.4055 -0.2176 -0.1054 -0.4796 -0.4055 -0.8755 -0.1287*

22 23 24 25 26 27 28 x

67 75 75 56 31 50 69 60

75 69 73 81 37.5 80 53 67

0.4055 -0.3102 -0.0870 1.2150 0.2776 1.3863 -0.6549 0.2812*

Subject

Males 8 9 10 11 12 13 14 x *Overall

Measuring

1 for the group

[9]

relative dominance

Although probabilities for the two dependent variables differed-the CVC task depending upon recall and the line-orientation task depending upon recognition; the sign, or laterality, ofthe results (for LD groups) accorded with earlier findings for linguistic vs spatial tasks. Therefore, the suitability of relative measures of lateralization, as suggested by SEGALOWITZ and ORR 1163, was assessed for the analysis of D. When difference scores between 1. for CVCs and line orientation were computed, the mean i scores for a spatial-linguistic difference were these: for LD females= -0.1893, LD males= -0.7072, RD females= +0.0418, and RD males= +0.6520. Thus, when relative measures were taken, there was complete concordance between the direction of D and the direction of the relative advantage for spatial-linguistic differences. LD was associated with a greater magnitude ofleft spatial advantage (for both males and females), while RD was associated with a larger right spatial advantage (also, for both males and females). This was the case despite the fact that males, as a group, generated opposite (complementary) scores for CVCs vs lines, while females did not. The measure of relative dominance, however, may cause differential laterality effects for individuals with noncomplementary specialization to disappear altogether. With this measure, LD and RD females did not differ significantly (t =0.33, df= 13, n.s.), whereas males did (t =2.04, df= 13, P <0.05, one-tailed). The absence of effect for D, in females, who had earlier shown the largest performance asymmetries (see Tables 1 and 2), is principally due to their homolateral advantages for linguistic and spatial tasks. That is, even where the actual visual field asymmetry

*It has been pointed out that shorter exposure durations are more likely to produce significant asymmetries for the judgment of line orientation [ 111. The longer duration (150 msec) used here was forced by technical limitations arising from the intermingling of stimulus types: all had to be exposed at the same duration.

NOTE

255

may be substantial for each of the linguistic and spatial tasks, but where they are of the same sign, the relative dominance measure reveals only the existence of non-complementarity. For the kinds of tasks here examined, females may rely more heavily upon the operation of a single hemisphere, but LD and RD females may rely upon opposite hemispheres. This fact is obscured by the relative dominance measure. Error

patterns

Although it was established, by means of ANOVA, that overall performance accuracy did not differ significantly for the 4 CVC groups (the means ranging from 63 to 75%), the central fixation digits were nevertheless missed in systematic fashion. More fixation digits were missed when the stimulus was presented in the left visual field, for all groups, whether given alphanumeric or spatial stimuli. Yet this bias did not apparently affect performance asymmetries, as described above. In an analysis of missed fixation digits for CVC identification, with visual fields as the within-subjects factor, ANOVA generated an F (1,28) = 21.23, P < 0.01, for visual fields, and F (1,27) = 4.60, P < 0.05, for the directionality by gender interaction. LD females and RD males missed the largest number of fixation digits when CVCs were in the LVF, yet these were the very groups which most consistently displayed a right and left VFA, respectively, for CVCs. Similarly, although only 3% of fixation digits were missed for judgments of line orientation, there were still twice as many omitted on the left as on the right (PC 0.05, binomial test). The systematic masking of the central digit by stimuli in the left visual field has not, as far as we know, been previously reported in the laterality literature. It may warrant further study, to determine whether it was an artifact of the apparatus used in the present study, or whether it represents an additional leftward bias, unrelated to D. However, since it was uniformly present for all dextral subgroups, which did differ significantly on the experimental factors, we do not view it as in any way undermining the principal finding-that the right VFA for CVCs was largely confined to leftdirected (LD)right-handers.

DISCUSSION A highly significant difference was seen between dextrals who were left-directed (LD)and those who were rightdirected (RD):the former displayed the expected right VFA for CVCs, the latter did not. This study therefore confirms that a directional bias (D)plays a significant part in affecting the outcome of visual laterality experiments. It also counters the notion that “any contamination from directional scanning is likely to be at most small” in laterality studies 161. The directional scanning to which BRADSHAWet al. [6] refer would very likely possess some of the general characteristics of D [3]. Whether the contamination by D was small or large should depend entirely upon the distribution of D,that is, on the proportion of RD individuals in the sample at issue. In our sample, where 50% of subjects were RD, the influence of D was made particularly evident by the fact that only 57% of the entire dextral sample displayed the anticipated right VFA for the linguistic task. Without D as moderator variable, this would have constituted one of the failed laterality experiments. When one considers that D ostensibly reflects visuomotor (or spatial) rather than linguistic processing,* the results are all the more intriguing because D-LD, in particular-was specifically predictive for the laterality of the alphanumeric or linguistic task. In view of this, what might the findings for RD imply-given that they do not conform at all to the performance expected of dextrals without familial sinistrality? The most obvious implications are: (1) that RD individuals are associated with a different cerebral organization; or (2) that they employ different strategies that do not reflect a difference in cerebral organization. That cerebral organization might differ for RD individuals is actually a plausible notion when we consider the following: First, RD individuals are a minority among dextrals (constituting approx. 12% of the dextral population, including familial sinistrals). Still, that proportion exceeds conventional estimates of speech representation in the right hemisphere 1151. The point has repeatedly been made, however, that, tachistoscopic studies provide access to the receptive, rather than the productive, aspects of linguistic processing. And receptive aspects of linguistic analysis may not be confined to the left hemisphere, even among consistent dextrals (e.g. 157). It is possible that RD individuals process this type of input differently from LD individuals, despite their having in common a left hemisphere governance of speech. It is not obvious how differences in strategy could account for the fact that left directionality (LD)generates the expected findings and right directionality (RD)does not, particularly since strategy effects due to task demands were

*If the analyticPholistic dichotomy of hemispheric processing were invoked instead, it might be contended that the directionality task, dealing as it does with complex configurations, actually requires analytic resources for its implementation. Since these are characteristic of left hemisphere processing, it would not be surprising to find that LD were predictive of a right VFA on a linguistic task. While contrary findings for RD could be ascribed to a more holistic approach to the directionality task, an explication of RD performance on the linguistic task would remain problematic. Finally, a description of the same task as dependent upon either analytic or holistic modes is tautological, unless independent evidence of a difference in strategies is brought to bear on the matter (and see below).

256

NOTE

minimized in this study through intermingling of linguistic and spatial stimuli. If the results on the spatial task were confirmed upon replication, we should be obliged to postulate that RD individuals actually reversed the usual processing strategies for hoth linguistic and spatial inputs. While LD males, for example, would apply the usual strategies so as to generate a right VFA for linguistic stimuli and a left VFA for spatial stimuli, RD males would have to reverse both strategies so as to produce a left VFA for linguistic stimuli and a right VFA for the spatial-a dubious proposition. This issue can be illuminated only through further study. The results of the judgment of line orientation task fell just short of statistical significance. The observed trends nonetheless indicate that it might be reasonable to expect that, for males, LD should be predictive of the canonical left VFA for the spatial task and right VFA for the linguistic task. For females, in contrast, LD should predict a right VFA for both spatial and linguistic tasks. Our findings tend to corroborate the suggestion of BRYDENrt al. [S] that complementary specialization may be more evident in men than in women. The sex difference, moreover was introduced by the spatial task-an observation consistent with the view that sex differences are seen principally in the spatial domain (e.g. [12], but see 1131). The fact that lef directionality (LD) might be associated with right VFAs for both spatial and linguistic tasks in females, would suggest that the particular direction for D (LD or RD) does not point, in a literal sense, to a preferred visual field, when the influence of D is examined in the context of conventional laterality tasks. The direction of D does, however, accord with the direction of the spatial asymmetry for males. It is also wholly concordant with the direction of spatial preference when a relative measure of dominance is used. It may nevertheless be useful to emphasize that the lack of directional correspondence poses no problem if we grasp the two distinct aspects of n: (I ) its predictive value for studies of laterality, as here examined, i.e. D as “moderator” variable; and (2) its reflection ofa lateralized directional bias in the perceptuo-motor domain [3], i.e. D as “independent” variable. While the present study provides strong supporting evidence of a cerebral basis for D, the conventional laterality task cannot serve adequately to evaluate whether D reflects an actual directional component in cerebral processing. This would have to be accomplished with stimuli whose spatial location and orientation were systematically varied, and not held constant, or balanced, as they are in the standard laterality task. We have shown that LD and RD dextrals differ as markedly as right- and left-handers in their performance asymmetries on visual laterality tasks. A comparison between handedness and directionality across a spectrum of tasks is an obvious corollary to the present work, as a means to establish their individual and joint associations with different patterns of cerebral organization. Acknowledgements-This report is based on an honours thesis done by Stephanie Rein at Bryn Mawr. We thank Drs Sidney Diamond, Lucia Kellar, and an anonymous reviewer, for their valuable comments on the manuscript.

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