Behavioral Neuroscience 2003, Vol. 117, No. 6, 1448 –1452
Copyright 2003 by the American Psychological Association, Inc. 0735-7044/03/$12.00 DOI: 10.1037/0735-7044.117.6.1448
Opposite Turning Behavior in Right-Handers and Non-Right-Handers Suggests a Link Between Handedness and Cerebral Dopamine Asymmetries C. Mohr
T. Landis
University Hospital Geneva and University Hospital Zurich
University Hospital Geneva
H. S. Bracha
P. Brugger
Department of Veterans Affairs Spark M. Matsunaga Medical and Regional Office Center
University Hospital Zurich
The strong right hand preference in humans remains a riddle; no lateralized behavior other than fine finger dexterity relates to it. The relation between handedness and language dominance may be far weaker than currently judged; after all, both right-handers and non-right-handers utilize the left brain for speech. There is, however, a lateralized motor preference in animals, turning behavior, that is strongly associated with hemispheric dopamine (DA) asymmetries. Turning consistently occurs towards the side with less DA. The authors tested 69 right-handers and 24 non-right-handers with a device recording spontaneous turning behavior for 20 hr within 3 days. Findings indicate that right-handers preferred left-sided turning and non-right-handers preferred right-sided turning. This result suggests a link between handedness and DA asymmetries.
In vertebrates, however, there exists another stable intraindividual motor preference, turning behavior, which is strongly associated with hemispheric dopamine (DA) asymmetries. In animals, the direction is ipsilateral to the hemisphere with the less active DA system, or in other words, contralateral to the hemisphere with the more active DA system (Glick, 1983; Patino, Garcia-Munoz, & Freed, 1995). This relation is so well established that without quantitative DA measurements, turning behavior alone is taken as proof of DA asymmetries (Brunner & Gattaz, 1995; Lindemann, Lessenich, Ebert, & Loscher, 2001). In humans, there is one known pathological condition, asymmetric Parkinson’s disease, in which one hemisphere contains less DA than the other. Consistent with animal findings, such patients turn away from the hemisphere that is more intact (Bracha, Shults, Glick, & Kleinman, 1987). Because one motor side preference, turning behavior, is associated with asymmetries in the DA system, it was tempting to propose that another motor side preference, handedness, might depend upon this system as well. This DA– handedness hypothesis has a long history in animals and, to some extent, in humans (Bracha, Seitz, Otemaa, & Glick, 1987; de la Fuente-Fernandez, Kishore, Calne, Ruth, & Stoessl, 2000; Fitzgerald, Ratty, Teitler, Gross, & Glick, 1993; Glick, 1983; Kooistra & Heilman, 1988; Larson, Dodson, & Ward, 1989; Nielsen et al., 1997). Various asymmetries of the volume and DA content of different parts of the basal ganglia have been associated with handedness (Kooistra & Heilman, 1988). However, a direct functional support of this hypothesis, a relation of handedness and spontaneous turning behavior, has not been found in animals (Fitzgerald et al., 1993; Larson et al., 1989; Nielsen et al., 1997; Westergaard & Suomi, 1996), and the only study in humans did not yield a clear-cut picture (Bracha, Seitz, et al., 1987). These latter authors tested hemispheric dominance, a compound measure of hand–foot– eye
Across cultures, humans have a strong right-hand preference, reportedly manifest for at least the past 5,000 years of human history (Coren & Porac, 1977). However, there seems to be no clear phylogenetic root to this human right-bias since handedness— or “pawedness”—appears equally distributed in most of the highest primates (Hamilton & Vermeire, 1988; see Palmer, 2002 for a meta-analysis). The preponderance of human righthandedness has remained a riddle and is not known to be related to any motor or cognitive behavior, other than measures of fine finger dexterity (e.g., Bryden, Pryde, & Roy, 2000; Triggs, Calvanio, Levine, Heaton, & Heilman, 2000). In view of the fact that both right-handers and about 70% of non-right-handers utilize the left brain for speech (Knecht et al., 2000; Pujol, Deus, Losilla, & Capdevila, 1999; Signore, Chaoui, Nosten-Bertrand, Perez-Diaz, & Marchaland, 1991), a direct link between handedness and language appears to be overestimated.
C. Mohr, Department of Rehabilitation, University Hospital Geneva, Geneva, Switzerland, and Department of Neurology, University Hospital Zurich, Zurich, Switzerland; T. Landis, Department of Neurology, University Hospital Geneva; H. S. Bracha, National Center for PTSD, Department of Veterans Affairs Spark M. Matsunaga Medical and Regional Office Center, Honolulu, Hawaii; P. Brugger, Department of Neurology, University Hospital Zurich. This research was supported by Grant 690610 from the Institut fu¨r Grenzgebiete der Psychologie und Psychohygiene, Freiburg, Germany, Grant 31-65096.01 from the Swiss National Science Foundation, and by the Office of Research and Development, Medical Research Service, Department of Veterans Affairs. Correspondence concerning this article should be addressed to C. Mohr, Functional Brain Mapping Laboratory, University Hospital Geneva, Rue Micheli-du-Crest 24, CH-1211 Geneva 14, Switzerland. E-mail: christine
[email protected] 1448
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preference in relation to turning behavior. They found a complex interaction between hemispheric dominance, turning, and gender. Unfortunately, the intercorrelation between hand, foot, and eye dominances is known to be low (Gabbard & Iteya, 1996; Graves, 1983). Thus, this study could not really answer the crucial question of a relationship between human handedness and turning behavior. We thus aimed to directly test human turning behavior in relation to handedness in a large sample of healthy right-handers and non-right-handers.
Method Subjects A total of 93 healthy subjects (48 women) with a mean age of 29.5 years (range ⫽ 21–59, see Table 1) were recruited by flyers and personal contact. The study protocol, in accordance with the Declaration of Helsinki, was approved by the local human research ethics committee, and all subjects gave signed consent before participation.
Handedness Handedness was assessed with the 13-item handedness questionnaire from Chapman and Chapman (1987) known for a high internal consistency and good test–retest reliability. For each item, subjects indicated whether they perform the action with the right hand, left hand, or both hands. The 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 items answered with “right”) to 39 (all items answered with “left”). According to the cut-off scores (Chapman & Chapman, 1987), the sample was subdivided into right-handers (scores 13–17, n ⫽ 69, 35 women) and non-righthanders (scores 18 –39, n ⫽ 24, 13 women, see Table 1).
Turning Behavior We used a lightweight, rechargeable, belt-mounted device comprising a position sensor and an electronic processing circuit that monitors changes 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 is used as an external reference and is tracked by a compass. With this device, partial turns (90°) in either direction are summed consecutively while the person moves in the same direction. When four 90° quadrants have been completed, a 360° turn is registered. If the subject suddenly moves in the other direction, a new measurement begins for the opposite direction. We assessed the number of full 360° turns to either side. Subjects were blind to the hypothesis and specific kind of measurement. They were required to wear the device during 20 hr for 3 consecutive days. At the first testing session, instructions were provided about the correct use of the device. Important instructions were that the device should be worn all day, removed only for sports, sleep, or activities damaging to the device. In the
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case of removal, subjects were required to deposit the device in such a way as to minimize any confounding non-body-related movements. At the end of the 20-hr test-time, the subjects had to fill out the handedness questionnaire.
Data Analysis We calculated a conventional laterality index score for the number of 360° turns: [(right turns minus left turns) ⫼ (right turns plus left turns)] ⫻ 100 (Marshall, Caplan, & Holmes, 1975). This laterality index is a measure independent 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 ⫽ 0.05, p ⬎ .20). Gender has been found to relate differently to hemispheric dominance and turning preference (Bracha, Seitz, et al., 1987). Thus, we performed a three-way analysis of variance (ANOVA) with gender (women vs. men) and handedness groups (right-handers vs. nonright-handers) as between-subject variables on laterality index scores. Previous studies on language lateralization and handedness found a linear relationship between increasing left-handedness and diminished lefthemisphere dominance for language (Knecht et al., 2000); thus, we also performed Pearson correlations between handedness raw scores and laterality index scores. Finally, we determined individuals’ preference to turn to either the left or right side by subtracting full turns to the right from full turns to the left. Thus, a positive value indicated a right-sided turning preference; and a negative value, a left-sided turning preference. If not stated otherwise, all reported p values are two-tailed, and only significant results will be reported.
Results Subjects A three-way ANOVA with gender (women vs. men) and handedness groups (right handers vs. non-right-handers) on age revealed only a significant main effect for gender, F(1, 89) ⫽ 4.43, p ⫽ .04; men were older (31.1 ⫾ 7.6) than women (28.0 ⫾ 5.3; see Table 1).
Turning Magnitude of turning preference. The ANOVA on the laterality index revealed a significant main effect for handedness groups, F(1, 89) ⫽ 13.30, p ⫽ .0004; right-handers had a lower laterality index than non-right-handers (Table 1). As can be seen in Figure 1, right-handers turned more strongly to the left and nonright-handers more strongly to the right. The difference from zero (an equal preference to turn to either side) was significant for the right-handed group, t(68) ⫽ 4.24, p ⬍ .0001 (one-tailed), and was
Table 1 Demographic and Turning Measures of the Study Sample Total
Women
Men
Measure
RH
NRH
RH
NRH
RH
NRH
Age Handedness scores Laterality index Side preference (L/R)
29.9 ⫾ 7.5 13.97 ⫾ 1.30 ⫺11.0 ⫾ 21.6 (51/18)
28.3 ⫾ 3.1 34.50 ⫾ 5.40 7.6 ⫾ 21.6 (7/17)
28.5 ⫾ 5.9 13.74 ⫾ 1.30 ⫺11.6 ⫾ 21.6 (26/9)
26.6 ⫾ 3.1 35.70 ⫾ 2.60 4.8 ⫾ 20.4 (4/9)
31.3 ⫾ 8.7 14.20 ⫾ 1.30 ⫺10.3 ⫾ 21.9 (25/9)
30.3 ⫾ 1.6 33.10 ⫾ 7.40 10.9 ⫾ 23.3 (3/8)
Note. RH ⫽ right-handers; NRH ⫽ non-right-handers; (L/R) ⫽ number of subjects with a left-sided (L) or right-sided (R) turning preference.
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Figure 1. Magnitude and opposite turning preferences of the two handedness groups, as shown by the mean (⫾ SEM) turning indices.
also significant, although less pronounced, for the non-righthanded group, t(23) ⫽ 1.73, p ⫽ .048 (one-tailed). Relationship between handedness raw scores and turning index scores. Increasing handedness raw scores (elevated lefthandedness) were positively correlated to laterality index scores, that is, more pronounced right-sided turning (r ⫽ .33, p ⫽ .001).
Frequency Distribution The log-linear analysis revealed a significant main effect for handedness groups, 2(1, N ⫽ 93) ⫽ 22.72, p ⫽ .000002 (more subjects were right-handed than non-right-handed) and preferred turning side, 2(1, N ⫽ 93) ⫽ 5.75, p ⫽ .02 (more subjects preferred left turns to right turns), as well as a significant interaction between handedness groups and preferred turning side, 2(1, N ⫽ 93) ⫽ 15.02, p ⫽ .0001 (right-handed subjects preferred left turns and non-right-handed subjects preferred right turns; Table 1).
Discussion The results of the present study show a reliable categorization of groups of people with opposite handedness according to another dichotomous behavioral measure, spontaneous turning behavior toward the side opposite to the preferred hand. One might argue that this preference is simply an artifact of an overactive dominant hand (or foot). But if increased unilateral limb motor activity is associated with increased contralateral turning behavior, patients with asymmetrical Parkinson’s disease should turn toward the more rigid, symptomatic body side, which is opposite to what is actually found (Bracha, Shults, et al., 1987). Moreover, a study with healthy right-handers showed that they spontaneously made significantly more movements with the left than the right arm (Eaton, Rothman, McKeen, & Campbell, 1998). One more alternative might be considered, that is, the possibilities that righthanders organize their personal environments differently from the
way left-handers do. If the organizational principle were guided by preferred hand use, our results would constitute a simple artifact. Although future studies should address this possibility (e.g., by limiting measurements to “controlled” environments), we do not think that it accounts for the present findings, because (a) a great amount of data were collected in natural, outdoor environments and (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 strong right-side bias of human handedness is phylogenetically unique, as animals up to the highest primates have individual paw preferences, but these appear equally distributed on the population level as to the side used (Betancur, Neveu, & Le Moal, 1991; Hamilton & Vermeire, 1988; Palmer, 2002; Signore et al., 1991). Animal studies will thus not necessarily answer questions about human handedness. While turning behavior in animals is widely accepted to depend on an asymmetric DA system, the neurochemical and/or neuroanatomical basis of paw preference has received little attention. It was tempting to relate side of turning, and implicitly DA asymmetries, to pawedness. As early as 1974, Glick and Jerussi studied spatial lever press preferences in rats as a function of pawedness. These authors found spatial lever-press preference to be related to turning side. Unfortunately, the authors did not report preferred pawedness and turning preference. In subsequent studies by the Glick group, a direct link and thus support for this DA– handedness hypothesis could not be established in animals (Fitzgerald et al., 1993; Larson et al., 1989; Nielsen et al., 1997; see also Westergaard & Suomi, 1996). Some relation between these variables does exist, however, as these studies showed that, independent of side, the stronger the paw preference, the stronger the turning behavior (Nielsen et al., 1997). Note that such a relationship was not found in our data (correlation between absolute turning index score and handedness raw scores: r ⫽ ⫺.02, p ⫽ .84).
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Moreover, DA injections in the caudate in rats produced an increased use of the preferred paw when ipsilaterally injected, but a decreased use when contralaterally injected (Evenden & Robbins, 1984). Another way of approaching this question was used in unilateral striatal lesion studies and in studies measuring DA in different parts of the basal ganglia: The striatum has been found to play an important role in contralateral paw-reaching skills and ipsilateral turning behavior (Barne´ oud et al., 1995; Henderson et al., 1999), and paw preference has been related to an ipsilateral hemispheric dominance for dopamine in the nucleus accumbens in mice (Cabib et al., 1995). In humans, similar attempts to relate size and/or DA asymmetries of basal ganglia structures to handedness have been undertaken. The globus pallidus especially appears to be larger and to contain higher amounts of DA in the left hemisphere (Glick, Ross, & Hough, 1982; Kooistra & Heilman, 1988). Kooistra and Heilman, for example, analyzed the postmortem brains of 18 individuals who were healthy and found significantly larger left globus pallidus size. Assuming right-handedness in these individuals, they speculated about a causal link between DA asymmetries and turning behavior on the one hand and the development of limb motor asymmetries on the other hand. However, according to this line of reasoning, one would expect right-handers to have a rightsided, but not left-sided, turning preference. A recent study measured the unimanual and bimanual motor performance of 20 right-handed healthy subjects, and, independently, their at-rest (18F) Fluorodopa PET uptake (de la FuenteFernandez et al., 2000). The authors calculated left–right uptake asymmetries in the basal ganglia and statistically correlated them to the individual’s motor proficiency. They found right-hand performance to correlate with left putamen dominance, but unexpectedly bimanual performance to correlate with right caudate dominance. Because they did not test non-right-handers, the question of handedness could not be addressed with this study. However, their correlation of good bimanual performance in right-handers with a relative “dominance” of the right caudate is very interesting. Bimanual actions, by their inherent demand for interhemispheric connectivity, are closer physiologically to axial whole-body movements—such as turning behavior—than are the fine unilateral finger movements that usually determine handedness. If one accepts a link between bimanual action and axial motion, this study, because of the right-sided DA dominance, might better explain our left-sided turning behavior in right-handers. In conclusion, we found, in a large sample of right-handers and non-right-handers during a 20-hr spontaneous turning behavior study, that right-handers turn left and non-right-handers turn right. This finding, although indirect, constitutes the first experimental evidence of a link between human handedness and another dichotomous behavioral variable, other than fine finger dexterity. We also found that, primarily on the basis of animal studies, this turning behavior is likely to be due to DA asymmetries and may thus provide a link between the DA system and the development of human handedness.
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Received April 22, 2003 Revision received June 18, 2003 Accepted June 18, 2003 䡲
