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Opposite Turning Behavior in Right-Handers and Non-Right-Handers Suggests a Link Between Handedness and Cerebral University Hospital Geneva and University Hospital Zurich Department of Veterans Affairs Spark M. Matsunaga Medical The strong right hand preference in humans remains a riddle; no lateralized behavior other than finefinger dexterity relates to it. The relation between handedness and language dominance may be farweaker than currently judged; after all, both right-handers and non-right-handers utilize the left brain forspeech. There is, however, a lateralized motor preference in animals, turning behavior, that is stronglyassociated with hemispheric dopamine (DA) asymmetries. Turning consistently occurs towards the sidewith less DA. The authors tested 69 right-handers and 24 non-right-handers with a device recordingspontaneous turning behavior for 20 hr within 3 days. Findings indicate that right-handers preferredleft-sided turning and non-right-handers preferred right-sided turning. This result suggests a link betweenhandedness and DA asymmetries.
Across cultures, humans have a strong right-hand preference, In vertebrates, however, there exists another stable intraindi- reportedly manifest for at least the past 5,000 years of human vidual motor preference, turning behavior, which is strongly asso- history (Coren & Porac, 1977). However, there seems to be no ciated with hemispheric dopamine (DA) asymmetries. In animals, clear phylogenetic root to this human right-bias since handed- the direction is ipsilateral to the hemisphere with the less active ness— or “pawedness”—appears equally distributed in most of the DA system, or in other words, contralateral to the hemisphere with highest primates (Hamilton & Vermeire, 1988; see Palmer, 2002 the more active DA system (Glick, 1983; Patino, Garcia-Munoz, & for a meta-analysis). The preponderance of human right- Freed, 1995). This relation is so well established that without handedness has remained a riddle and is not known to be related to quantitative DA measurements, turning behavior alone is taken as any motor or cognitive behavior, other than measures of fine finger proof of DA asymmetries (Brunner & Gattaz, 1995; Lindemann, dexterity (e.g., Bryden, Pryde, & Roy, 2000; Triggs, Calvanio, Lessenich, Ebert, & Loscher, 2001). In humans, there is one Levine, Heaton, & Heilman, 2000). In view of the fact that both known pathological condition, asymmetric Parkinson’s disease, in right-handers and about 70% of non-right-handers utilize the left which one hemisphere contains less DA than the other. Consistent brain for speech (Knecht et al., 2000; Pujol, Deus, Losilla, & with animal findings, such patients turn away from the hemisphere Capdevila, 1999; Signore, Chaoui, Nosten-Bertrand, Perez-Diaz, that is more intact (Bracha, Shults, Glick, & Kleinman, 1987).
& Marchaland, 1991), a direct link between handedness and lan- Because one motor side preference, turning behavior, is associ- ated with asymmetries in the DA system, it was tempting topropose that another motor side preference, handedness, mightdepend upon this system as well. This DA– handedness hypothesishas a long history in animals and, to some extent, in humans C. Mohr, Department of Rehabilitation, University Hospital Geneva, Ge- (Bracha, Seitz, Otemaa, & Glick, 1987; de la Fuente-Fernandez, neva, Switzerland, and Department of Neurology, University Hospital Zurich,Zurich, Switzerland; T. Landis, Department of Neurology, University Hospital Kishore, Calne, Ruth, & Stoessl, 2000; Fitzgerald, Ratty, Teitler, Geneva; H. S. Bracha, National Center for PTSD, Department of Veterans Gross, & Glick, 1993; Glick, 1983; Kooistra & Heilman, 1988; Affairs Spark M. Matsunaga Medical and Regional Office Center, Honolulu, Larson, Dodson, & Ward, 1989; Nielsen et al., 1997). Various Hawaii; P. Brugger, Department of Neurology, University Hospital Zurich.
asymmetries of the volume and DA content of different parts of the This research was supported by Grant 690610 from the Institut fu¨r basal ganglia have been associated with handedness (Kooistra & Grenzgebiete der Psychologie und Psychohygiene, Freiburg, Germany, Heilman, 1988). However, a direct functional support of this Grant 31-65096.01 from the Swiss National Science Foundation, and by hypothesis, a relation of handedness and spontaneous turning the Office of Research and Development, Medical Research Service, behavior, has not been found in animals (Fitzgerald et al., 1993; Larson et al., 1989; Nielsen et al., 1997; Westergaard & Suomi, Correspondence concerning this article should be addressed to C. Mohr, 1996), and the only study in humans did not yield a clear-cut Functional Brain Mapping Laboratory, University Hospital Geneva, RueMicheli-du-Crest 24, CH-1211 Geneva 14, Switzerland. E-mail: christine picture (Bracha, Seitz, et al., 1987). These latter authors tested hemispheric dominance, a compound measure of hand–foot– eye preference in relation to turning behavior. They found a complex case of removal, subjects were required to deposit the device in such a way interaction between hemispheric dominance, turning, and gender.
as to minimize any confounding non-body-related movements. At the end Unfortunately, the intercorrelation between hand, foot, and eye of the 20-hr test-time, the subjects had to fill out the handedness dominances is known to be low (Gabbard & Iteya, 1996; Graves, 1983). Thus, this study could not really answer the crucial questionof a relationship between human handedness and turning behavior.
We thus aimed to directly test human turning behavior in We calculated a conventional laterality index score for the number of relation to handedness in a large sample of healthy right-handers 360° turns: [(right turns minus left turns) Ϭ (right turns plus left turns)] ϫ 100 (Marshall, Caplan, & Holmes, 1975). This laterality index is a measureindependent from the individual number of turns, whereby positive values indicate a preference to turn to the right; and negative values, to the left.
The laterality index was normally distributed (Kolmogorov–Smirnov Test d ϭ 0.05, p Ͼ .20). Gender has been found to relate differently tohemispheric dominance and turning preference (Bracha, Seitz, et al., 1987).
A total of 93 healthy subjects (48 women) with a mean age of 29.5 years Thus, we performed a three-way analysis of variance (ANOVA) with (range ϭ 21–59, see Table 1) were recruited by flyers and personal contact.
gender (women vs. men) and handedness groups (right-handers vs. non- The study protocol, in accordance with the Declaration of Helsinki, was right-handers) as between-subject variables on laterality index scores.
approved by the local human research ethics committee, and all subjects Previous studies on language lateralization and handedness found a linear gave signed consent before participation.
relationship between increasing left-handedness and diminished left-hemisphere dominance for language (Knecht et al., 2000); thus, we also performed Pearson correlations between handedness raw scores and later-ality index scores. Finally, we determined individuals’ preference to turn to Handedness was assessed with the 13-item handedness questionnaire either the left or right side by subtracting full turns to the right from full from Chapman and Chapman (1987) known for a high internal consistency turns to the left. Thus, a positive value indicated a right-sided turning and good test–retest reliability. For each item, subjects indicated whether preference; and a negative value, a left-sided turning preference. If not they perform the action with the right hand, left hand, or both hands. The stated otherwise, all reported p values are two-tailed, and only significant use of the right hand is given 1 point, of both hands 2 points, and of the left hand 3 points. Possible scores thus range continuously from 13 (all itemsanswered with “right”) to 39 (all items answered with “left”). According tothe cut-off scores (Chapman & Chapman, 1987), the sample was subdi- vided into right-handers (scores 13–17, n ϭ 69, 35 women) and non-right-handers (scores 18 –39, n ϭ 24, 13 women, see Table 1).
A three-way ANOVA with gender (women vs. men) and hand- edness groups (right handers vs. non-right-handers) on age re- We used a lightweight, rechargeable, belt-mounted device comprising a vealed only a significant main effect for gender, F(1, 89) ϭ 4.43, position sensor and an electronic processing circuit that monitors changes p ϭ .04; men were older (31.1 Ϯ 7.6) than women (28.0 Ϯ 5.3; see in the orientation of the dorsal–ventral axis (see Bracha, Seitz et al., 1987; Bracha, Shults et al., 1987, for further technical details). Magnetic north isused as an external reference and is tracked by a compass. With this device, partial turns (90°) in either direction are summed consecutively while theperson moves in the same direction. When four 90° quadrants have been completed, a 360° turn is registered. If the subject suddenly moves in the ality index revealed a significant main effect for handedness other direction, a new measurement begins for the opposite direction. We groups, F(1, 89) ϭ 13.30, p ϭ .0004; right-handers had a lower assessed the number of full 360° turns to either side. Subjects were blind laterality index than non-right-handers (Table 1). As can be seen in to the hypothesis and specific kind of measurement. They were required towear the device during 20 hr for 3 consecutive days. At the first testing Figure 1, right-handers turned more strongly to the left and non- session, instructions were provided about the correct use of the device.
right-handers more strongly to the right. The difference from zero Important instructions were that the device should be worn all day, re- (an equal preference to turn to either side) was significant for the moved only for sports, sleep, or activities damaging to the device. In the right-handed group, t(68) ϭ 4.24, p Ͻ .0001 (one-tailed), and was Table 1Demographic and Turning Measures of the Study Sample RH ϭ right-handers; NRH ϭ non-right-handers; (L/R) ϭ number of subjects with a left-sided (L) or right-sided (R) turning preference.
Magnitude and opposite turning preferences of the two handedness groups, as shown by the mean also significant, although less pronounced, for the non-right- way left-handers do. If the organizational principle were guided by handed group, t(23) ϭ 1.73, p ϭ .048 (one-tailed).
preferred hand use, our results would constitute a simple artifact.
Relationship between handedness raw scores and turning index Although future studies should address this possibility (e.g., by limiting measurements to “controlled” environments), we do not handedness) were positively correlated to laterality index scores, think that it accounts for the present findings, because (a) a great that is, more pronounced right-sided turning (r ϭ .33, p ϭ .001).
amount of data were collected in natural, outdoor environmentsand (b) the animal literature found that DA asymmetry is the final common pathway of circling behavior (for overviews, see Glick &Ross, 1981; Pycock, 1983).
The log-linear analysis revealed a significant main effect for The strong right-side bias of human handedness is phylogeneti- handedness groups, 2(1, N ϭ 93) ϭ 22.72, p ϭ .000002 (more cally unique, as animals up to the highest primates have individual subjects were right-handed than non-right-handed) and preferred paw preferences, but these appear equally distributed on the pop- turning side, 2(1, N ϭ 93) ϭ 5.75, p ϭ .02 (more subjects ulation level as to the side used (Betancur, Neveu, & Le Moal, preferred left turns to right turns), as well as a significant interac- 1991; Hamilton & Vermeire, 1988; Palmer, 2002; Signore et al., tion between handedness groups and preferred turning side, 2(1, 1991). Animal studies will thus not necessarily answer questions N ϭ 93) ϭ 15.02, p ϭ .0001 (right-handed subjects preferred left about human handedness. While turning behavior in animals is turns and non-right-handed subjects preferred right turns; Table 1).
widely accepted to depend on an asymmetric DA system, theneurochemical and/or neuroanatomical basis of paw preference has received little attention. It was tempting to relate side of The results of the present study show a reliable categorization of turning, and implicitly DA asymmetries, to pawedness. As early as groups of people with opposite handedness according to another 1974, Glick and Jerussi studied spatial lever press preferences in dichotomous behavioral measure, spontaneous turning behavior rats as a function of pawedness. These authors found spatial toward the side opposite to the preferred hand. One might argue lever-press preference to be related to turning side. Unfortunately, that this preference is simply an artifact of an overactive dominant the authors did not report preferred pawedness and turning pref- hand (or foot). But if increased unilateral limb motor activity is erence. In subsequent studies by the Glick group, a direct link and associated with increased contralateral turning behavior, patients thus support for this DA– handedness hypothesis could not be with asymmetrical Parkinson’s disease should turn toward the established in animals (Fitzgerald et al., 1993; Larson et al., 1989; more rigid, symptomatic body side, which is opposite to what is Nielsen et al., 1997; see also Westergaard & Suomi, 1996). Some actually found (Bracha, Shults, et al., 1987). Moreover, a study relation between these variables does exist, however, as these with healthy right-handers showed that they spontaneously made studies showed that, independent of side, the stronger the paw significantly more movements with the left than the right arm preference, the stronger the turning behavior (Nielsen et al., 1997).
(Eaton, Rothman, McKeen, & Campbell, 1998). One more alter- Note that such a relationship was not found in our data (correlation native might be considered, that is, the possibilities that right- between absolute turning index score and handedness raw scores: handers organize their personal environments differently from the r ϭ Ϫ.02, p ϭ .84).
Moreover, DA injections in the caudate in rats produced an Betancur, C., Neveu, P. J., & Le Moal, M. (1991). Strain and sex differ- increased use of the preferred paw when ipsilaterally injected, but ences in the degree of paw preference in mice. Behavioural Brain a decreased use when contralaterally injected (Evenden & Rob- bins, 1984). Another way of approaching this question was used in Bracha, H. S., Seitz, D. J., Otemaa, J., & Glick, S. D. (1987). Rotational unilateral striatal lesion studies and in studies measuring DA in movement (circling) in normal humans: Sex difference and relationshipto hand, foot and eye preference. Brain Research, 411, 231–235.
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