З. Стоянов, П. Николова, Д. Ставрев
ЭПИДЕМИОЛОГИЯ ПРАВШЕСТВА-ЛЕВШЕСТВА В БОЛГАРИИ: ПОДТВЕРЖДЕНИЕ ГЕНЕТИЧЕСКОЙ МОДЕЛИ АННЕТТ И МАКМАНУС
Медицинский Университет имени профессора Стоянова, варна, Болгария
Zlatislav Stoyanov*, Piareta Nikolova*, Dimitar Stavrev**
Handedness Proportions in Bulgaria:
I. Evidence supporting the Genetic Models of Annett and McManus
*Department of Physiology and Pathophysiology
**Department of Anatomy, Histology and Embryology
Medical University “Prof. Paraskev Stoyanov”, Varna, BulgariaHANDEDNESS PROPORTIONS IN BULGARIA: EVIDENCE SUPPORTING THE GENETIC MODELS OF ANNETT AND MCMANUS Zlatislav Stoyanov*, Piareta Nikolova*, Dimitar Stavrev** The population proportions of handedness in Bulgaria have been explored twice with a 15-year interval between them. Two separate analyses have been carried out with different subdivisions of the studied persons: left-handed/right-handed and non-right-handed/right-handed. Statistically significant differences between the results of both surveys have not been found. Aggregated data show that: left-handed people in Bulgaria comprise 6.5% of the population; 11.5% of all Bulgarians fall in the broader category of non-right-handedness. The obtained results are discussed considering the genetic models of Annett and McManus. Key words: left-handedness, non-right-handedness, genetic models, Annett, McManus. Introduction. The term handedness (or manual dominance) is used to denote the hand skill asymmetry and the preferred use of one hand for performance of most manual tasks and fine manual activities (Medland et al., 2009; Corballis et al., 2012). Handedness as motor asymmetry is one of the manifestations of hemispheric lateralization of brain functions. Researchers are especially interested in left-handedness. The type of handedness, according to many authors, is a distinct marker for specificity in the cerebral organization, and handedness-related differences in hemispheric specialization are mentioned (Grabowska et al., 1994; Grimshaw, 1998; Toga and Thompson, 2003; Chuprikov and Volkov, 2006; Medland et al., 2009; Gutwinski et al., 2011).At individual level, the earliest signs of handedness may be visible in the 10th week of intrauterine development (Searleman et al., 1989; Hepper et al., 1998). At that age single movements of the arms may be observed, with 75% of the foetuses showing higher number of right hand movements. In 12.5% of the cases the number of left-hand movements of the arms is larger, and in the remaining 12.5% there is a balance between the movements of the left and right arms. Observations between the 12th and the 27th weeks give similar results which allow Hepper et al. (1990) to claim that at the end of the first trimester of the intrauterine development the asymmetric tendencies in the handedness proportions are already set and they are later found at the population level.The aggregated data for adults indicate that about 10% of the human population are left-handed but there exist ethnic, racial and geographical regional differences (McManus, 2002; Geuze et al., 2012). Data found in various sources present a wide range, e.g. 3.6% left-handers in some non-industrial communities in Papua, Indonesia, 5.6% in Algeria and up to 15-16% in some studies from the USA (see Bourassa et al., 1996; Porac, 1996; Schaafsma et al., 2012). In their summary Llaurens et al. (2009) point at an even wider range, between 3.35% and 26.9%, of established left-handedness incidence in various communities. Despite the variations, however, left-handers present a minority everywhere. It is interesting to note that the dominance of right-handers in the right-handers/left-handers proportion may be traced back as far as 35,000 years ago, and over 300,000 years according to some researchers (see Coren and Porac, 1977; Faurie and Raymond, 2004; Llaurens et al., 2009).Many theories have been proposed in the attempt to explain the causes of handedness and they often are a part of the bigger problem of what causes the cerebral lateralization. Some of the early concepts (those of the first decades of 20th century) accept that laterality and handedness are learned and therefore are a product exclusively of the social environment (for review see Elias, 1999). Other hypotheses strictly adhere to the biological and genetic perspective (Levy and Nagylaki, 1972; Annett, 1972; McManus, 1985; Klar, 1996. Francks et al., 2007). Still others are based on the genetics but also take into account the role of chance or environmental factors (such as the influence of the sex hormones on the development of the brain, see Geschwind and Galaburda, 1985 may, june).One of the most impressive genetic models is Annett’s Right Shift Theory (Annett, 1972). Annett favours the role of a single gene with two alleles (RS+ and RS–), where RS+ (Right Shift Factor) appears to be dominant and determining the development of a typical left hemisphere dominance for language (Annett, 1985; 1998; 2008). This gene is not directly determining but highly affecting handedness. If the Right Shift Factor is present in the individual, then the person is pre-determined to be with language functions lateralized in the left hemisphere and right-handed. If the factor is absent, the individual may be with typical or atypical cerebral dominance for language and right-handed or left-handed depending on the influence of random factors and circumstances. Annett’s theory takes into consideration that both alleles are found with equal frequency in the populations and are randomly paired. There follows that 50% of the population will be RS+/RS–, 25% will be RS+/RS+ and 25% will be RS–/RS–. In accordance with that, the individuals from the first two groups (RS+/RS– and RS+/RS+) will be right-handed with language functions lateralized in the left hemisphere. According to Annett, in the third group (RS–/RS–) where the factor of the right shift is absent, handedness is determined by factors of the environment on the random principle and it is to be expected that half of those 25% will be right-handed and the other half – left-handed. The theory predicts 12.5% left-handers in the populations. The specific point in Annett’s theory is that it understands handedness as a continuum ranging between far right and far left (i.e., it has varying degrees of left-/right-handedness) (Annett, 1985; 1998; 2008). Depending on where the discriminating threshold is placed, quite different proportions of manual dominance may be derived, especially if the category of non-right-handedness is taken into account.Another genetic model that predicts population proportions of handedness (left-handedness/right-handedness) is the model of McManus (1985). The researcher claims that handedness is also controlled by two alleles of the same gene. One allele “D” encodes dextrality, the other “C” does not code sinistrality but randomness in forming the manual preferences. According to this hypothesis, the incidence of right-handedness in the population is defined cumulatively depending on the variants in the model: 100% of the “DD” homozygotes, 75% of “DC” heterozygotes and 50% of the “CC” homozygotes will be right-handed. Following McManus’ quantitative analyses, about 15% of the population have the chance to be left-handed, namely those individuals with “C” expressed allele (2.4% “СС” genotypes and 13% “DC” genotypes). It is a 50:50 chance and therefore, according to the model, the frequency of left-handedness should normally be 7.75%. In contrast to Annett, the McManus model adopts the directional principle in defining handedness: the author views handedness as existing in two explicitly differentiated (“discrete”) variants, left-handedness and right-handedness. Each deviation from the value 7.75% of the proportion left-handed/right-handed is, according to McManus, a result of changed criteria (definition of left-handedness) and previously cultivated attitudes during the selection (the chosen discriminating threshold).A key moment in both genetic models is the explanation of the principles which form and support relatively stable the population proportions of handedness. As it has been pointed out, however, there exist significant ethnic, racial and geographic differences in handedness that suggest interaction of the genetic mechanisms with environmental factors. In this outlined context we carried out a study with the following aims: (1) to establish the proportions of handedness in the Bulgarian population; (2) to check whether the handedness proportions in the Bulgarian population are stable with the passage of time, and (3) to find out which genetic model (of Annett or McManus) corresponds with the handedness proportions among the Bulgarians. A study of this kind is carried out in Bulgaria for the first time. The data obtained would be useful for researchers who analyse the handedness proportions in countries with different or similar climatic/geographic and ethnic/cultural characteristics. Methods. Analyses of the survey are based on a contingent of total of 1,856 individuals (856 males and 1,000 females). The data were collected during two studies, the first of which was conducted in the period of 1991-1993, and the second – during 2006-2008. The first study covered 1,256 individuals (606 males and 650 females) and the second – 600 persons (250 males and 350 females). The surveyed individuals were between 17 and 25 years of age and were recruited on a volunteer basis from the secondary schools and universities in the city of Varna, Bulgaria. Recruitment was directed at obtaining an approximately equal proportions of males and females, but complete balance was not achieved. The evaluation of handedness was based on a handedness questionnaire, which was adapted for Bulgarian compilation from the questionnaires of Annett (the 12-item version) and of Oldfield (the 10-item version) (for details see Stoyanov, 1998; Stoyanov et al., 2010). A handedness quotient (HQ) was computed on the basis of the handedness questionnaire (Fedoruk and Dobrohotova, 1980). The handedness quotient varied between –100% (strong left-handers) and +100% (strong right-handers). The zero value of HQ was used as a threshold for distinguishing between left-handers and right-handers. As questionnaire studies by correspondence hold certain risks of inaccurate evaluation (see Leutin and Nikolaeva, 1988; McManus, 1985; Brito et al., 1989), we consider it pertinent in screening analyses to use also the categories non-right-handedness (HQ = –100% ¸ +35%) and right-handedness (HQ = +36% ¸ +100%). This approach corresponds with the recommendations of Klar (2003) and allows the inclusion of switched to right-handedness left-handers (see McManus, 1985), the larger part of whom are in the range HQ = 0% ¸ +35%.Fisher’s exact test was used for statistical evaluation of the data (GraphPad Prism 5 software). The differences were considered significant at p < 0.05.Results. Tables 1 and 2 show the results from both studies carried out at an interval of 15 years, in 1991-1993 and 2006-2008 respectively. It is evident that the percentage of left-handers in both researches is almost identical: 6.3% and 6.8% correspondingly. Fisher’s exact test did not find differences in the proportions left-handers/right-handers established by the two surveys (p = 0.687).TABLE 1. Population proportions of handedness in categories left-handedness (HQ = –100% ¸ –1%) and right-handedness (HQ = 0% ¸ +100%)
TABLE 2. Population proportions of handedness in categories non-right-handedness (HQ = –100% ¸ +35%) and right-handedness (HQ = +36% ¸ +100%)
Discussion. In two separate studies carried out with an interval of 15 years we established similar proportions of handedness in the Bulgarian population both in the categories left-handedness/right-handedness and in the categories non-right-handedness/right-handedness. That confirms the expectations of the genetic hypotheses about population proportions of the main types of manual dominance that remain, on principle, stable in time.
The percentage of left-handers in Bulgaria (6.5%) is close to that predicted by the McManus model (7.75%). In other observations we carried, about one fourth of individuals with values of HQ between 0% and +35% reported to have been under pressure in their childhood to switch from preferred use of left hand to use of right hand (Stoyanov, 2011). We consider those individuals to be left-handers by nature. If they are taken into account, the percentage of left-handers will get even closer to the predictions of the McManus model.
The proportions in the categories non-right-handedness and right-handedness correspond more with the claims of Annett’s hypothesis. The established percentage of non-right-handers in both our studies, between 10.7% and 13%, are about the same as those 12.5% predicted by the original version of the Right Shift Theory.
How do data about the Bulgarian population compare with data for other populations? The percentage of left-handers in Bulgaria (6.5%) is close to that of some South European and Mediterranean countries: Greece (6.3%), Italy (7.3%), Spain (6.2%), Algeria (5.6%) (Dargent-Pare et al., 1992; Bourassa et al., 1996). A similar percentage (5.8%) is also reported for the Finnish population (Vuoksimaa et al., 2009). A higher incidence of left-handedness is registered in Western Europe: in France it is 9.3%, in Belgium 9.4%, and in the United Kingdom 10% (Bourassa et al., 1996; Porac, 1996; Bradley, 1992). Our data for the percentage of non-right-handers in Bulgaria (11.1%) almost completely correspond with the 11.2% established by Vuoksimaa et al. (2009) in Finland.
The confirmed stability of the proportions of handedness in the Bulgarian population and their compliance with the frequencies predicted by the genetic models, are facts supporting the claims that genetic mechanisms are engaged in determining handedness. The similarity of proportions of handedness in Bulgaria with proportions from other populations supports McManus’ assumption (1985) that the frequencies of the respective alleles should be the same in the various populations. We think that both genetic models discussed here, Annett’s Right Shift Theory and the McManus model, are applicable in explaining the determination of the handedness proportions: the first exploiting handedness as a continuum and the second as a binary phenomenon. We, however, are inclined to support the view that, in its genesis, handedness is rather an epigenetic phenomenon born from the superimposition of environmental influences on genetic mechanisms. Additional research needs to be done to establish the concrete role of environmental factors such as climate, length of day, nutrition, morbidity, in forming the proportion left-handers/right-handers (non-right-handers/right-handers) in specific populations or regions.
Acknowledgements. The authors would like to thank Prof. Boris Gutnik, Department of Physiology, Russian State Medical University by Pyrogov, Moscow, Russian Federation, for his valuable comments on an earlier version of this text.
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