Hand Motor Performance and Degree of Asymmetry in Monozygotic Twins

NOTE

HAND MOTOR PERFORMANCE AND DEGREE OF ASYMMETRY IN MONOZYGOTIC TWINS L. Jancke1 and H. Steinmetz2 eDepartment of General Psychology, Section Cybernetical Psychology and Psychobiology, Heinrich-Heine-University, Dusseldorf; 2Department of Neurology, Heinrich-HeineUniversity, Dusseldorf)

ABSTRACT

To determine whether the absolute degree of asymmetry of hand motor performance (irrespective of direction of this asymmetry) may have a heritable component we examined 20 pairs of monozygotic (MZ) twins of whom 10 pairs were concordantly right-handed (MZRR) and 10 pairs discordant for handedness (MZ-RL). The tests comprised measurements of the maximum left and right hand tapping rate as well as a paper-and-pencil test of left and right hand motor proficiency. Intraclass correlations within MZ-RR and MZ-RL for absolute degree of hand motor asymmetry were not significant. In contrast, significant intrapair correlations emerged for overall hand motor performance, a measure unrelated to laterality. These results demonstrate that at least in MZ twins the degree of hand motor asymmetry is mainly determined by non-genetic factors, whereas overall hand motor skill is more likely to be influenced by the genome. In addition, the lack of a difference in overall hand motor performance between MZ twins and 40 singletons studied as controls would not support hypotheses explaining behavioural asymmetry in twins, or their discordance for asymmetry, by developmental dysfunction.

INTRODUCTION

It is still a matter of dispute whether handedness is determined primarily by genetic or non-genetic factors. Thus, a number of conflicting theories have attributed important influences to social factors (Collins, 1975, 1977, 1991), other exogenic influences (Bakan, 1971, 1977; Satz, 1973; Harris, 1980), non-genetic biological left-right gradients (Corballis and Morgan, 1978; Morgan and Corballis, 1978), primarily genetic (Levy and Nagylaki, 1972) or a combination of genetic and random factors (Annett, 1978, 1994; McManus, 1985). Whereas twin studies have generally been perceived as a powerful tool to separate genetic from other determinants of human behavior (Bouchard, 1994), it is interesting to note that this is different in handedness research. Here, principle objections have been raised against using the frequent observation of handedness discordance in healthy monozygotic (MZ) twins (McManus, 1980) as an argument against genetic hypotheses. Such caution appears justified because twin-specific developmental factors may indeed play a role, such as increased likelihood of pre- or postnatal damage possibly resulting in pathological left-handedness (Wilson and Jones, 1932; Nagylaki and Levy, 1973), or the observed phenomenon of mirror imaging within MZ twin pairs (Newman, 1928; Carter-Saltzman, 1979; Bum, 1991; Steinmetz, Herzog, Schlaug et aI., 1995). Most of the large twin surveys used hand preference to define handedness (e.g. Wilson and Jones, 1932; Rife, 1940; Tambs, Magnus and Berg, 1987; Davis and Annett, 1994). It should be noted, however, that this measure is more likely than hand motor performance to be biased by social, statistical and questionnaire-specific factors (Bryden, 1982; Peters, 1992; Cortex, (1995) 31, 779-785

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L. Jiincke and H. Steinmetz

Peters and Murphy, 1992, 1993), and that it does not allow precise quantification of asymmetry on a continuous scale. Thus, an attractive experimental model prediction by Collins (1975, 1977, 1991), that degree but not direction of handedness may be genetically determined, has not been adequately tested in human MZ twins. We have quantified left and right hand motor performance in 20 MZ twin pairs and, thereby, attempted to answer the following questions: (i) Is the absolute degree of asymmetry of hand motor performance correlated within pairs of MZ twins concordant and discordant for handedness direction? (ii) Do MZ twins differ from singletons with respect to overall hand motor performance? MATERIALS AND METHODS

Subjects

The MZ twin pairs were recruited through announcements in the local Medical School and newspaper advertisement specifically calling for participation in a handedness study. Twenty consecutive MZ pairs reporting no birth complication, neurologic or psychiatric illness, learning disability or failure in elementary school were examined (32 women and eight men between 22 and 34 years of age). All pairs had been reared together. Monozygosity was ascertained by blood typing yielding a probability of >0.9996 for each pair to be MZ (Scheil and Koppatz, 1991; Steinmetz et aI., 1995). According to self-classification and writing hand, the twins were concordantly right-handed (group label: MZ-RR, n= 10 pairs) or discordant for handedness (group label: MZ-RL, n= 10 pairs). In addition, a control group of normal singletons carefully matched for age, sex and handedness (according to self-classification and writing hand) was included in the study (32 women and eight men between 21 and 36 years of age). This control group comprised 20 right- (C-RH) and 20 left-handers (C-LH). Hand Performance

Hand motor performance was assessed using two paper-and-pencil performance tests. The 'hand-dominance test' (HDT; Steingrtiber, 1971) comprised three dexterity tasks, each to be performed with maximal speed and precision over 15 seconds, separately for the right (R) and left (L) hand (tracing lines, dotting circles and squares). Performance was scored for each hand. Total performance scores (R + L) and asymmetry coefficients (R - L)/(R + L) were determined for each task. According to previous experiments, HDT scores of the dominant hand are strongly correlated with writing and drawing speed (writing: r=0.65, n= 120, p0.05; drawing: r=.l1, n=120, p>0.05; own unpublished data). For all statistical tests specified in the following, a significance level of p
For the purpose of the following analyses, five subgroups of right-handed (RH) or lefthanded (LH) twin or control (C) subjects were formed: MZ-RR-RH (n = 20), MZ-RL-RH (n = 10), MZ-RL-LH (n = 10), C-RH (n = 20), C-LH (n = 20). Because this handedness classification had been based on self-description, we examined whether the five groups revealed significant asymmetry on hand performance testing (deviation from zero of asymmetry coefficients determined with t-tests for dependent samples). All RH subjects (twins

Hand motor performance in twins

781

TABLE I

lntraclass Correlations (according to the formula of Fuller and Thompson, 1960) for Absolute Asymmetry Coefficients and Total Accuracy Scores within Monozygotic Twin Pairs Concordant (MZRR, n = 10 pairs) or Discordant for Handedness (MZ-RL, n= 10 pairs) MZ-RR

MZ-RL

HDT

TAP

HDT

TAP

Absolute asymmetry coefficient

+0.06

+0.39

+0.16

+0.08

Total score

+0.67*

+0.58*

+0.78*

+0.77*

HDT: hand-dominance-test; TAP: tapping test. *: p< O.O) , two-tailed.

and controls) exhibited positive HDT and TAP asymmetry coefficients, whereas the LH subjects did not show significant asymmetry. Further analyses revealed no differences (all p-values >0.20) between RH twins and RH controls (three-way ANOVA) or LH twins and LH controls (t-test for independent samples). Intraclass correlations calculated according to the formula of Fuller and Thompson (1960) for absolute asymmetry coefficients in the 20 MZ twin pairs ·were not significant (Table I and Figure 1). To investigate whether the five subgroups differed in total HDT or TAP scores, one-way analyses of variances (ANOV As) with a five level grouping factor were calculated for each dependent variable. No significant result emerged (HDT: F = 1.89; dJ. = 4, 75 ; p=0.12; TAP: F=0.88; d.f .=4, 75; p=O.88). In contrast, we found a significant result for absolute asymmetry coefficients at HDT or TAP (HDT: F=4.69, dJ.=4,75 ; p=O.OO2; TABLE II

Means and Standard Deviations (in brackets) of Absolute Asymmetry Coefficients and Total Performance Scores for Right-handed Controls (C-RH: n=20), Left-handed Controls (C-LH, n=20); Monozygotic Twins from Concordant Pairs (MZ-RR-RH, n=20 right-handers) and Monozygotic Twins from Discordant Pairs (MZ-RL-RH, n = 10 right-handers; MZ-RL-LH, n = 10 left-handers). MZ-RR-RH

MZ-RL-RH

MZ-RL-LH

C-RH

C-LH

HDT absolute asymmetry coefficient

0.13 (0.06)

0.12 (0.03)

0.11 (0.04)

0.11 (0.04)

0.05 (0.05)

HDT total score

216.60 (15.69) 0.Q7 (0.06)

212.70 (25.20)

2 18.00 (21.06)

216.17 (23.63)

235.20 (17.07)

0.05 (0.04)

0.02 (0.04)

0.05 (0.02)

0.02 (0.0l)

111.15 (3.76)

109.60 (6.77)

112.20 (4.92)

109.23 (5.98)

108.90 (5.70)

TAP absolute asymmetry coefficient TAP total score

HDT: hand-dominance-test; TAP: tapping test.

TAP: F = 4.83, d.f. = 4,75 ; p= 0.001). Subsequently performed S cheffe tests revealed lesser absolute asymmetry among LH controls (for HDT and TAP) and LH twins (for TAP), without differences between both of these subgroups . DISCUSSION

Our data indicate that there is no relationship between the absolute degree of asymmetry of hand motor performance within MZ twin pairs. This accords with the study of Tambs et a1. (1987) who also failed to demonstrate intrapair similarities using a composite hand preference score derived from a multi-item questionnaire. Although the exact quantification of variance due to heritability would require intraclass correlations for MZ and dizygotic

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Fig. 1 - Distribution of absolute asymmetry coefficients (Y-axis) for two hand motor performance tests (HDT and TAP) in twenty pairs of monozygotic (MZ) twins. Co-twins are connected by vertical lines. In each figure part, the twin pairs are ranked according to intrapair difference. continued

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twins, the low and nonsignificant intraclass correlations for MZ twins obtained in the present study argue against a strong genetic influence on the degree of asymmetry of motor performance. Thus, the results do not support the model of Collins (1975,1977,1991) which implies that degree but not direction is the heritable factor in human laterality. Instead, at least in MZ twins, neither degree nor direction of asymmetry follow a simple genetic rule, a conclusion very similar to that of a study of brain structural asymmetry in the same sample (Steinmetz et a!., 1995). Why do degree and direction of handedness diverge within MZ pairs? Of course, the findings could be explained by prenatal or postnatal environmental factors affecting MZ twins differentially, such as fetal position (Previc, 1991), fetal blood supply (Kaelber and Pugh, 1969), infant position in mother's arm, or chance (Annett, 1978, 1994; McManus, 1985), to mention just a few. Considering the fact that the twins studied here were healthy individuals with normal motor performance (Table II) and normal brain anatomy (Steinmetz et al., 1995), we exclude the possibility that any such hypothetical factor may have acted pathogenically in our cohort. . It is worth mentioning that the intraclass correlation of 0.39 for tapping laterality in MZRR twins, although nonsignificant, is in agreement with results obtained in familial studies using a similar performance test (dot-filling test, Tapley and Bryden, 1985). In these studies parent-child and sib-sib correlations ranged from .21 to .33 (Bryden, 1982; Carlier, Beau, Marchaland et a!., 1994). However, the moderate twin resemblance in our study was only found in MZ-RR twins and only for the tapping test, not for the HDT. Thus, it cannot be ruled out that sampling biases or task-specific factors might have influenced our results. In contrast to direction and degree of asymmetry, overall hand motor performance was very similar among the MZ co-twins (intraclass correlations for HDT or TAP: r=0.58-0.78; see Table I). This accords with the results of McNemar (1933) and Brody (1937) who reported strong intraclass correlations in MZ twin pairs for performance of other hand motor skills (pursuit rotor test: r=0.87-0.88, spool packing: r=0.54-0.56, card sorting: r=0.71-75). The McNemar study (1933) also comprised dizygotic twin pairs, who revealed much weaker intraclass correlations for these tasks (pursuit rotor test: r = 0.44-0.60, spool packing: r = 0.380.55, card sorting: r = 0.49-0.56). Regarding possible environmental explanations ("identical" training experience of MZ co-twins), it is interesting to note that auditory lateralization, a less overlearned feature of laterality, apparently follows the same rule as handedness. Thus, two dichotic listening studies of MZ twins showed no intrapair correlations for degree of asymmetry, but strong correlations for overall test scores (Springer and Searleman, 1978; Hncke and Steinmetz, 1994). Taken together, the data indicate that at least in MZ twins overall performance (R + L) but not asymmetry of performance of behavioral tasks is influenced by genetic factors. Acknowledgements. This study was supported by grants of the Deutsche Forschungsgemeinschaft (SFB 1941A7) and the Hermann und Lilly Schilling Stiftung, Essen, Germany (H.S.). The authors also thank Dr. Hans-Georg Scheil, Institute of Human Genetics and Anthropology, Heinrich-Heine-University Dusseldorf, for the haemogenetic studies, and Axel Herzog, Department of Neurology, Heinrich-Heine-University Dusseldorf, for technical assistance. REFERENCES

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