Introduction. Functional interhemispheric asymmetry characterizes all elements of sensory systems and stages of the sensory process. Right-sided preference across all lateralization indices is a distinctive human characteristic. The majority of people (about 80%) exhibit right-sided dominance of the hand and foot, and nearly half prefer the right eye. Approximately 40% of people show consistent lateral hand preference (37% right and about 3% left), while the remaining 60% may use either the dominant or subdominant hand depending on the action—these individuals are considered inconsistent or partial right-handers/left-handers. Lateral preference of limbs and sensory organs depends on many factors.

Before modern radiological methods for studying the brain, some researchers believed that the formation of different lateralization patterns might be linked to hemodynamic factors. In particular, it was hypothesized that right-handedness results from the left carotid artery generally being larger in diameter than the right. In 2006, Cagnie et al., studying the correlation between dominant left carotid artery and right-handedness, found no relationship between carotid artery diameter and hand dominance. The hypothesis that a dominant left carotid artery leads to right-handedness, and vice versa, was not confirmed [1].

However, strong evidence supports the involvement of a genetic component in determining the leading hand. It is widely known that more left-handers appear in families with left-handed parents. As an alternative to the genetic theory of dominance, some authors proposed a model of left-handedness associated with birth trauma. They argued that brain damage during pathological childbirth could shift hand preference from right to left.

Consequently, one might find more left-handers in groups where the likelihood of birth trauma is higher. Since 1971, literature reviews have examined the relationship between birth conditions, birth trauma, and children’s lateral preferences. Bakan was the first to suggest that non-right-handedness observed in first-born and last-born children is a consequence of fetal birth trauma (Bakan P, 1971). When examining laterality not only of the hand but also of the foot, eye, and ear in more than 5,000 individuals, Coren and Porac found that prenatal or perinatal circumstances are more strongly associated with left-handedness than chromosomal factors (Coren S, Porac C, 1980).

This explains why a disproportionately high number of left-handers are observed among neurological patients. For example, among patients with athetoid cerebral palsy, 61% were left-handed, predominantly children with the most severe form of the disease due to perinatal asphyxia (PA) (Yokochi K et al., 1990). In 1987, Levine et al. found that in most cases, neonatal brain damage occurs in the left hemisphere. Later, Njiokiktjien confirmed radiologically that children and adults more often suffer left-hemisphere damage than right, regarding perinatal and postnatal unilateral strokes, hemiparesis, and epilepsy.

The primary pathogenetic factor is hemodynamic, responsible for insufficient blood supply to the left hemisphere via the left internal carotid artery. During childbirth, an open ductus arteriosus also plays an additional role [6]. Thus, enough evidence has accumulated in the literature to recognize pre- and perinatal damage to the left hemisphere as one cause of left-handedness. At the same time, there is no direct evidence linking birth trauma to partial or incomplete right-handedness/left-handedness, where a right-hander performs some actions with the non-dominant hand.

When assessing lateral preference, not only pure right-handers and left-handers are identified—people with dominance of right or left functions across all indices (leading right hand and foot, right ear and eye). The majority are individuals with not only various combinations of auditory and visual functions but also varying degrees of dominance of the leading hand, with right functions prevailing over left. To date, it remains unclear why pure right-handers and left-handers as well as predominantly right- or left-handed individuals coexist in the population. It is possible that deviations from consistent hand lateral preference may also be related to birth pathology. The present study was undertaken to investigate this.

Methods. Healthy children without neurological pathology (n=20), aged 5.5–6 years, with a history of perinatal asphyxia (PA) were selected. All wrote, drew, and held a spoon with their right hand—they were right-handers by primary criteria. They were asked to perform the following tasks requiring bimanual activity: 1) open a Russian doll (matryoshka); 2) open a tube with a screw cap; 3) assemble a pyramid; 4) build a structure from blocks; 5) take matches out of a box; 6) build a well from matches; 7) thread a needle; 8) string beads onto a thread; 9) untie a knot; 10) lace a shoe. Performance with right-hand dominance was scored as 1 point. The total score obtained by each child was compared with data from the same examination of 20 healthy right-handed children of the same age born without pathology. The results were processed using nonparametric statistics (Mann–Whitney test).

Results. Children from the control group used their right hand as the primary and left as the auxiliary hand when performing 9–10 out of 10 tests (mean score: 9.7). Children who had experienced PA demonstrated difficulties in all types of manual activity. They performed all tests more slowly, showing motor clumsiness, and used the right hand as the leading hand in 5–9 out of 10 cases (mean score: 6.5). When building a matchstick well, untying knots, or lacing shoes, 9 children used both hands without preference. In all children, lateral advantage was recorded as right-sided, but with varying degrees of left-hand involvement as the leading hand in some types of bimanual activity. The degree of right-hand dominance in children with a history of PA was lower than in children from the control group (p < 0.0001).

Discussion. The primary brain damage in PA in full-term children includes acute and subacute hemorrhages in the cerebral cortex, basal ganglia, hippocampus, diencephalic region of the brainstem, cerebellum, and white matter. The most sensitive and vulnerable neurons to asphyxia are pyramidal neurons in the hippocampus, Purkinje cells in the cerebellum, neurons of the caudate nucleus and putamen; destructive changes are most pronounced in hippocampal pyramidal cells and neurons of the third and fifth layers of the motor cortex, which apparently leads to motor impairments in children. Cortical hemorrhages in the frontal and somatosensory areas without involvement of periventricular and basal regions do not lead to significant neurological deficits but may manifest during the formation of post-traumatic interhemispheric redistribution of functions.

The consequences of birth trauma influence the formation of physical health and the child’s nervous system from birth. In children with brain damage due to asphyxia or hypoxia, hyper-, hypo-, or dystonic disorders usually appear from the first weeks of life. Subsequently, these children show neurological complications consisting mainly of motor insufficiency. Limited motor activity of the dominant hand proves insufficient for performing complex movements, and children use the subdominant hand to a greater extent than their healthy peers.

The immature human brain is characterized by plasticity, i.e., the ability for global functional reorganization in response to internal and external stimuli. Children who suffer extensive unilateral brain damage in early childhood can show a remarkable degree of residual sensorimotor function. For example, a child up to 7–8 years of age recovers language skills after extensive stroke in speech areas or even after removal of the dominant hemisphere. Children with extensive unilateral brain damage can grasp objects and walk, albeit with a limp. In children with hemiparesis, hand movements are often accompanied by mirror movements of the other hand (Levine S et al., 1987; Woods B & Teuber H, 1978). This implies that with early brain damage, motor functions may be represented in the hemisphere ipsilateral to the paretic hand. This is supported by results of hemispherectomy experiments in rodents. After hemispherectomy, the remaining hemisphere creates a new uncrossed corticospinal tract in addition to the usual crossed tract [2]. Moreover, the neurons involved in forming the uncrossed tract are found both in areas where typical crossed tract neurons reside and in adjacent areas [4].

In epilepsy patients after hemispherectomy, passive movements of the contralateral and ipsilateral hands elicit activation in the sensorimotor cortex of the remaining hemisphere, with a larger activation area for the contralateral hand, although in healthy right-handers the left hemisphere shows weak ipsilateral sensorimotor activation [3]. In patients with neonatal hemiparesis, the intact hemisphere is far more involved with the ipsilateral hand than in healthy individuals. Although most ipsilateral activation encompasses the Rolandic sulcus region of the intact hemisphere, in some hemiparetic patients finger movements activate zones distant from the central gyrus, mainly parietal cortex [7]. This indicates the potential involvement of non-specific cortical neurons in compensatory activity.

Thus, the mechanisms of brain plasticity following lesions of dominant hand representation areas may involve both motor analyzer neurons of the opposite hemisphere and nerve cells from adjacent brain regions, possibly including a limited number of multipotent polymodal neurons. The mechanisms of ultrastructural neuronal reorganization in the brain are not fully understood but may include competition for synaptic space, axonal migration, and sprouting along chemical gradients [5].

Conclusion. In focal or lesional damage to the motor cortex in the area representing the dominant hand, functional compensation of the developing brain may consist of redistribution of functions between intact regions of both hemispheres. The motor function of the dominant hand may be provided not only by specific areas of both hemispheres but also by adjacent cortical regions. Such brain reorganization leads to the result that both the dominant and subdominant hands of subjects after PA exhibit a lower degree of lateralization compared to healthy individuals. Therefore, it can be assumed that cases of incomplete or partial hand dominance may be associated with a history of birth trauma. Perinatal complications not only increase the probability of left-handedness but may also delay the establishment of the leading hand; early brain damage not only affects the formation of laterality but also contributes to the formation of partial hand dominance.

Literature:

1. Cagnie B, Petrovic M, Voet D, Barbaix E, Cambier D. Man Ther. 2006;11(2):153-6.

2. Hicks, S. P. & D'Amato, J. C. Exp. Neurol. 1970; 29, 416-438.

3. Holloway V, Gadian D, Vargha-Khadem F, Porter D, Boyd S. Brain. 2000;123;12:2432-44.

4. Huttenlocher, P. R. & Raichelson, R. Dev. Brain Res. 1989; 47, 59-69.

5. Letourneau, P. C. Trends Neurosci. 1983: 6, 451-455.

6. Njiokiktjien Ch. Fiziol Cheloveka. 2006;32(1):45-50.

7. Yue C, Vikingstad E, Huttenlocher P, Vernon L. Proc. Natl. Acad. Sci. USA 1994;91:9612-9616.