Evolutionary origins of human handedness: evaluating contrasting hypotheses

Variation in methods and measures, resulting in past dispute over the existence of population handedness in nonhuman great apes, has impeded progress into the origins of human right-handedness and how it relates to the human hallmark of language. Pooling evidence from behavioral studies, neuroimaging and neuroanatomy, we evaluate data on manual and cerebral laterality in humans and other apes engaged in a range of manipulative tasks and in gestural communication. A simplistic human/animal partition is no longer tenable, and we review four (nonexclusive) possible drivers for the origin of population-level right-handedness: skilled manipulative activity, as in tool use; communicative gestures; organizational complexity of action, in particular hierarchical structure; and the role of intentionality in goal-directed action. Fully testing these hypotheses will require developmental and evolutionary evidence as well as modern neuroimaging data.     

Genetic influence on the expression of hand preferences in chimpanzees (Pan troglodytes): evidence in support of the right-shift theory and developmental instability

Genetic mechanisms have been proposed to explain the pervasive representation of right-handedness in humans, whereas random, nongenetic factors have been posited to explain the lack of population-level right-handedness in nonhuman primates. We report evidence that hand preferences in chimpanzees are heritable, even among related individuals raised in different environments. Furthermore, we report that the degree of heritability is modified by factors associated with developmental instability, notably, offspring parity. The data are interpreted to reconcile both genetic models for handedness and hypotheses suggesting that developmental instability influences variation in handedness.     

Sex differences and handedness in hemispheric lateralization of tactile-spatial functions

Sex differences in spatial processing and handedness were studied with a tactile-spatial task in 27 male and 29 female right-handed undergraduate students in psychology. Subjects were asked to identify amorphous shapes to investigate possible male right-hemisphere specialization for spatial functions and bilateral representation among the women. The Annett handedness questionnaire estimated extent of right-handedness. Subjects were classified by major, and women by phase of menstrual cycle. Analysis shows significantly more right-handedness in women and ambidexterity in men. Over-all, men do not perform significantly better than women, although men outperform women with their left hands when handedness is covaried. Within sex, no difference is seen between left and right hand scores for men, but women perform significantly better with right than left hands. Further analyses suggest men appear right-hemisphere dominant for this task whereas women show left-hemisphere dominance. Analyses of hormonal data support recent research, in that for women on the pill there is a trend to perform worse than all other groups. Engineering students perform significantly better than all other majors.     

Is there atypical handedness in schizophrenia?

Ninety-three schizophrenic patients and 105 normal controls were tested in a single session on an 8-item repeat-administration handedness test. The schizophrenic group, in contrast to the normal controls, showed a shift in the distribution away from right-handedness, which was due to an increase in the proportion of mixed-handers. Additional analyses revealed that the increase in mixed-handedness was largely due to an increase of within-item variability in the schizophrenic group, which we refer to as ambiguous handedness. Nearly 20% of the schizophrenic patients were inconsistent on 3 or more items compared with 3.8% of the normal controls. This increased incidence of atypical handedness is discussed within the context of disorders of attention and neurodevelopment.     

EEG correlates of behavioural laterality: right-handedness

Among right-handers, the magnitude of differences in proficiency between the left and right hands varies considerably. Yet significance of the extent of right-handedness is still a controversial issue. To examine whether individual differences in asymmetry of hand skill can partly be attributed to individual differences in asymmetrical hemispheric activation, handedness and electroencephalographic (EEG) laterality were correlated in two large samples (ns = 60 and 128). Analysis indicated that part of the variability in right-handedness may arise from activation asymmetries in the cortex, but whether this relation becomes apparent depends on the cortical area examined and on the experimental condition under which the EEG measures are taken.     

Chimpanzee (Pan troglodytes) handedness: variability across multiple measures of hand use

This study examined intertask consistency in handedness across multiple measures of hand use in a sample of 187 chimpanzees (Pan troglodytes). Hand preferences for 2 to 6 measures were collected from the sample, and hand preference scores were derived on the basis of the individual hand preferences for each measure. Seven of 15 possible intratask correlations were significant, with some degree of clustering depending on the motor demands of the tasks. Two overall measures of handedness revealed population-level right-handedness in the chimpanzees, although the degree of bias was reduced for chimpanzees tested on more than 3 measures of hand use. The results are interpreted in the context of several recent studies that proposed theoretical models of handedness in nonhuman primates.     

Maternal cradling bias in baboons: The first environmental factor affecting early infant handedness development?

The most emblematic behavioral manifestation of human brain asymmetries is handedness. While the precise mechanisms behind the development of handedness are still widely debated, empirical evidences highlight that besides genetic factors, environmental factors may play a crucial role. As one of these factors, maternal cradling behavior may play a key role in the emergence of early handedness in the offspring. In the present study we followed 41 Papio anubis infants living in social groups with their mother for which direction (e.g., left- or right-arm) and degree of maternal cradling-side bias were available from a previous published study. We assessed hand preferences for an unimanual grasping task at three developmental stages: (A) 0–4, (B) 4—6, and (C) 9–10 months of age. We found that individual hand preferences for grasping exist as soon as the first months of age, with a population-level left-handedness predominance, being stable until 6 months; to wit the period during which juveniles are mainly carried by their mothers. More importantly, this early postnatal handedness is positively correlated with maternal cradling lateralization. Interestingly, hand preferences assessed later in the development, once juveniles are no longer carried (i.e., from 9 to 10 months of age), are less dependent from the maternal cradling bias and less consistent with the earlier developmental stages, especially in infants initially cradled on the right maternal side. Our findings suggest that the ontogenetic dynamics of the infant's hand preference and its changes might ultimately rely on the degree of infant dependence from the mother across development.     

How sensitive are handedness prevalence figures to differences in questionnaire classification procedures?

Questionnaire data from 572 subjects show that the proportion of right-handers to nonright-handers varies greatly (from 1:100 to 92:8) as a function of questionnaire length, graded or forced response to items, and cut-off criteria. For this reason, the right-handed/nonright-hander dichotomy is singularly unsuited as a basis for classification when handedness is to be related to some other neuropsychological factor as an independent variable. This is especially the case when very strict cut-off criteria are used to define right-handedness (e.g., only those individuals who prefer the right hand for all activities listed).     

Handedness incidence in a population of black university students

A modified version of the Edinburgh Handedness Inventory was used to assess degrees of left-, mixed-, and right-handedness in USA and Caribbean black university students. The distributional pattern of handedness in men and women was significantly different, largely due to a higher incidence of left- and mixed-handed men. Sinistral incidence in men of this population was significantly higher than that reported in some other studies on Anglo-Saxon populations.     

The influence of vestibular system and fetal presentation on handedness,cognitive and motor development: A comparison between cephalic and breech presentation

Genetics are undoubtedly implicated in the ontogenesis of laterality. Nonetheless, environmental factors, such as the intrauterine environment, may also play a role in the development of functional and behavioral lateralization. The aim of this study was to test the Left-Otolithic Dominance Theory (LODT; Previc, 1991) by investigating a hypothetical developmental pattern where it is assumed that a breech presentation, which is putatively associated with a dysfunctional and weakly lateralized vestibular system, can lead to weak handedness and atypical development associated with language and motor difficulties. We used the ALSPAC cohort of children from 7 to 10 years of age to conduct our investigation. Our results failed to show an association between the vestibular system and fetal presentation, nor any influence of the latter on hand preference, hand performance, or language and motor development. Bayesian statistical analyses supported these findings. Contrary to our LODT-derived hypotheses, this study offers evidence that fetal presentation does not influence the vestibular system's lateralization and seems to be a poor indicator for handedness. Nonetheless, we found that another non-genetic factor, prematurity, could lead to atypical development of handedness.     

The role of locomotor posture and experience on handedness and footedness in infancy

This research examined the development of handedness and footedness in infancy. We measured footedness by documenting the limb infants used to "lead-out" as they crawled or walked down a path several times. We measured handedness by documenting the hand infants used to reach for a goal at the end of each trial. Study 1 showed that locomotor skill affects limb lateralization preferences and that most 13-month-old infants demonstrated a side preference for reaching and leading out "in the moment." Study 2 longitudinally examined the developmental trajectories of handedness and footedness as they related to locomotor posture and experience. The findings suggest high variability in the developmental trajectory of footedness, with frequent fluctuation between side preferences. The developmental trajectory of handedness was more stable over the transition between locomotor milestones. The transition between crawling and walking decreased the proportion of infants demonstrating side preferences for leading out and the onset of walking decreased the proportion of infants demonstrating side preferences for reaching. These findings demonstrate the importance of making behavioral observations at multiple time scales to understand underlying developmental trajectories, specifically the stability or instability of the motor system associated with the acquisition of new motor abilities.     

Cerebral asymmetry: motoring on

I argue that the phylogenetic and neurobiological bases for cerebral asymmetry in humans are likely to be found in motor systems rather than in perceptual systems. Current genetic models of human laterality suggest that a `dextral' allele might be responsible for right-handedness and left-cerebral dominance for speech in the majority of humans. The linking of handedness with language lateralization might reflect the early evolution of language as predominantly a system of manual gestures, perhaps switching to a mainly vocal system only with the emergence of Homo sapiens. So-called `mirror neurons' in the prefrontal cortex of the monkey, which fire both when the animal makes a grasping response and when it sees the same response performed by others, might be part of a circuit that is the precursor to language circuits in the brain. This circuit appears to be bilateral in monkeys, but left-hemispheric in humans.     

The use of bouts and frequencies in the evaluation of hand preferences for a coordinated bimanual task in chimpanzees (Pan troglodytes): an empirical study comparing two different indices of laterality

Hand preferences for a coordinated bimanual task were assessed in 109 chimpanzees (Pan troglodytes). Hand preference was evaluated for 4 test sessions using bouts and frequencies of hand use to compare the sensitivity of each level of analysis in evaluating individual variation in handedness. Overall, significant population-level right-handedness was found using several different measures of hand use. Handedness indices based on bouts and frequencies were highly and significantly correlated. Moreover, hand preferences were consistent across tests despite efforts to situationally bias preference during each test. Taken together, these data do not support the view that bouts are a better level of analysis for evaluating hand preference. The results further suggest that hand preferences for coordinated bimanual actions are not influenced by situational factors and may reflect an inherent specialization of the left hemisphere for motor skill.     

Handedness, emotional problems, and schizotypy

The purpose of this study was to analyse the relationship between emotional or behavioural problems and schizotypy. An assessment of handedness and schizotypal personality traits were also performed by means of the Thinking and Perceptual Style Questionnaire, the Multidimensional Schizotypal Traits Questionnaire, the Edinburgh Handedness Inventory, and the Youth Self-Report. The sample comprised 296 participants with a mean age of 13.8 and a standard deviation of 1.34. Data indicate that adolescents with high scores on psychometric factors of schizotypy displayed higher patterns of problem behaviours as well as a significant difference in all the core factors of the Youth Self-Report, compared to those who scored low on these measures. Discriminant analysis showed that the core factors of the Youth Self-Report correctly classified 84% of the adolescents with high or low scores on psychometric schizotypy. Lastly, no significant association between the factors of schizotypy and left-handedness, right-handedness, or mixed-handedness was found.     

Unimanual and bimanual tasks and the assessment of handedness in toddlers

The goal of this study was to examine the relations between three different measures of handedness: unimanual reaching, bimanual manipulation and unimanual manipulation. The appropriateness of the task chosen to evaluate handedness was also explored by contrasting different bimanual manipulation tasks for the more or less differentiated (passive\active) roles assigned to each hand. Forty children, between 18 and 36 months of age, were tested in the three conditions. The results show that the degree of bimanual handedness is greater on the bimanual tasks with a strong role differentiation than on the tasks with less differentiation. Bimanual tasks with a strong role differentiation elicited more right‐handedness than unimanual reaching. Among the children who showed handedness in reaching, the correlation between unimanual and bimanual handedness was high, especially for right‐handers. For some tasks, bimanual handedness appeared at the earliest age studied here (18 months), and there was little relationship between bimanual handedness and bimanual skill. In contrast with unimanual reaching, there was no age‐related change in the degree of handedness for either bimanual or unimanual manipulation. There was a bias toward the use of the right hand for unimanual manipulation. It was concluded that grasping is not the best task to employ to look for robust evidence of handedness, and that bimanual tasks offer a better way to estimate handedness in children, as long as the tasks are carefully chosen.     

Dyslexia and brain morphology

Although the neurological basis of dyslexia has long been assumed, little direct evidence documents a relation between deviations in brain morphology and behavioral correlates of dyslexia. This article reviews two sources of evidence. Results of CT/MRI studies suggest that in the brains of dyslexics there is an increased incidence of symmetry in the region of the planum temporale and parietooccipital cortex that may be associated with language delay and handedness. Postmortem/cytoarchitectonic studies document symmetry of the plana, provide evidence of thalamic involvement, and chart widely distributed focal dysplasias preferentially involving the left frontal, left temporal, and right frontal regions. Methodological deficiencies characterize this literature, however, particularly regarding the diagnosis of dyslexia, appraisal of handedness and neurolinguistic deficits, and a failure to provide evidence that this pattern of involvement is unique to the dyslexic syndrome. These findings are discussed as they relate to neurobiological theory.     

Motor planning and execution in left- and right-handed individuals during a bimanual grasping and placing task

The issue of handedness has been the topic of great interest for researchers in a number of scientific domains. It is typically observed that the dominant hand yields numerous behavioral advantages over the non-dominant hand during unimanual tasks, which provides evidence of hemispheric specialization. In contrast to advantages for the dominant hand during motor execution, recent research has demonstrated that the right hand has advantages during motor planning (regardless of handedness), indicating that motor planning is a specialized function of the left hemisphere. In the present study we explored hemispheric advantages in motor planning and execution in left- and right-handed individuals during a bimanual grasping and placing task. Replicating previous findings, both motor planning and execution was influenced by object end-orientation congruency. In addition, although motor planning (i.e., end-state comfort) was not influenced by hand or handedness, motor execution differed between left and right hand, with shorter object transport times observed for the left hand, regardless of handedness. These results demonstrate that the hemispheric advantages often observed in unimanual tasks do not extend to discrete bimanual tasks. We propose that the differences in object transport time between the two hands arise from overt shifting visual fixation between the two hands/objects.     

Theoretical Speculations on the Evolutionary Origins of Hemispheric Specialization

ABSTRACT— Hemispheric specialization has long been considered a uniquely human trait associated with the evolution of language and handedness. Recent studies in a host of vertebrate species have reported evidence of population-level behavioral and brain asymmetries, challenging the claims for the uniqueness of hemispheric specialization to the human species. Here we summarize the findings in nonhuman species and discuss the adaptive significance and potential costs of lateralization of function.