Behavioral Lateralization Research Articles

Night-migratory garden warblers can orient with their magnetic compass using the left, the right or both eyes

Several studies have suggested that the magnetic compass of birds is located only in the right eye. However, here we show that night-migrating garden warblers (Sylvia borin) are able to perform magnetic compass orientation with both eyes open, with only the left eye open and with only the right eye open. We did not observe any clear lateralization of magnetic compass orientation behaviour in this migratory songbird, and, therefore, it seems that the suggested all-or-none lateralization of magnetic compass orientation towards the right eye only cannot be generalized to all birds, and that the answer to the question of whether magnetic compass orientation in birds is lateralized is probably not as simple as suggested previously.

Behavioral correlates of corpus callosum size: Anatomical/behavioral relationships vary across sex/handedness groups

There are substantial individual differences in the size and shape of the corpus callosum and such differences are thought to relate to behavioral lateralization. We report findings from a large scale investigation of relationships between brain anatomy and behavioral asymmetry on a battery of visual word recognition tasks. A sample of 200 individuals was divided into groups on the basis of sex and consistency of handedness. We investigated differences between sex/handedness groups in callosal area and relationships between callosal area and behavioral predictors. Sex/handedness groups did not show systematic differences in callosal area or behavioral asymmetry. However, the groups differed in the relationships between area of the corpus callosum and behavioral asymmetry. Among consistent-handed males, callosal area was negatively related to behavioral laterality. Among mixed-handed males and consistent-handed females, behavioral laterality was not predictive of callosal area. The most robust relationship was observed in mixed-handed females, in whom behavioral asymmetry was positively related to callosal area. Our study demonstrates the importance of considering brain/behavior relationships within sub-populations, as relationships between behavioral asymmetry and callosal anatomy varied across subject groups.

The relationship between growth, brain asymmetry and behavioural lateralization in a cichlid fish

Cerebral lateralization, the partitioning of cognitive tasks to one cerebral hemisphere, is a widespread phenomenon among vertebrates. Despite this diversity, every species studied to date shows substantial individual variation in the strength of lateralization. The neural basis of this trait is unclear, although asymmetries in cerebral structures have been investigated for over a century. The habenular nuclei, for example, have been shown to present striking neuroanatomical and/or neurochemical asymmetries in species ranging from jawless fish to mammals. In teleost fish, these nuclei are relatively symmetrical in most species. Those teleosts that do have asymmetrical habenular nuclei, show varying patterns of asymmetry in different species. Here we investigate the relationship between individual variation of asymmetry in the habenula of a South American cichlid fish, Geophagus brasiliensis, and behaviour in a commonly used test for visual laterality in fish, the detour task. We show that the strength of asymmetry in the habenula is correlated with strength of behavioural lateralization in the detour task. Both the strength and direction of habenular asymmetry are correlated with individual differences in growth rate. We suggest that this relationship results from processes linking growth rate and sexual differentiation to frequency-dependent variation in life-history strategies. To our knowledge, this is the first study to demonstrate a relationship at the individual level between neural asymmetry and lateralized behaviour in a fish.

Sex and asymmetry in humans: what is the role of developmental instability?

Because asymmetric individuals are less attractive and may suffer from reduced fitness, bilateral asymmetry is widely believed to affect human sexual selection. Its evolutionary significance is based on the presumed relationship with developmental instability (DI). Yet, relationships between DI and bilateral asymmetry are often weak and possibly confounded by asymmetric mechanical loadings because of handedness. We related asymmetry in hands and faces to degrees of handedness and sexual behaviour in 100 humans. Handedness correlated to levels of asymmetry, thereby likely invalidating the use of asymmetry to estimate DI. For facial asymmetry, applying existing theoretical models refuted a link between asymmetry and DI. Explicit statistical modelling at the level of DI confirmed the absence of a link between DI and aspects of sexual behaviour. Nevertheless, asymmetries in both hands and face correlated significantly with sexual behaviour. We conclude that bilateral asymmetry per se, rather than its presumed link with DI, more likely relates to measures of human sexual behaviour. Because lateralization of behaviour appears widespread, evaluating the role of DI in evolution and ecology relies on a very critical selection of traits whose asymmetry can reliably reflect DI.

Lateralisation of trunk movements in captive Asian elephants (Elephas maximus)

Behavioural lateralisation has been widely investigated in vertebrates. Most studies in this area have focused on laterality in paired organs such as hands, limbs, and eyes. Fewer studies have explored side preferences in unpaired organs such as tails or trunks. We investigated laterality of trunk use among captive Asian elephants (Elephas maximus), quantifying side preference in four different trunk movements: feeding, sand spraying, self-touching, and swinging. We found evidence for significant side preference in all four movement categories. Variation in the occurrence and direction of side preference was seen both within and between individuals but no overall population-level side bias was seen for any of the four trunk movements. The strength of side preference in trunk use was significantly higher for feeding than for self-touching and swinging. This study adds to the very limited data on laterality in unpaired organs generally, and elephants’ trunks more specifically. In addition it provides novel information about directional lateralisation in trunk use across a range of functionally distinct contexts.

A large-scale investigation of lateralization in cortical anatomy and word reading: are there sex differences?

The authors report findings of a large-scale, multitask investigation of sex differences in both structural asymmetries and lateralization of word reading. Two hundred participants were tested in eight divided visual field lexical tasks, and each received a structural magnetic resonance imaging scan. The authors examined whether there was evidence for sex differences in overall measures of neuroanatomical and behavioral lateralization, in specific language tasks and brain regions, and in variation in asymmetry within and across tasks and brain regions. There was very little evidence for sex differences on any behavioral measure. The few indications of sex differences in the current report accounted for 2% or less of the individual variation in asymmetry and could not be replicated in independent subsamples. No sex differences were observed in the asymmetry of structures in Broca's and Wernicke's areas such as pars triangularis, pars opercularis, the planum temporale, planum parietale, or Heschl's gyrus. There were also no sex differences in the variability of neuroanatomical asymmetries within or between brain regions. However, a significant relationship between planum temporale and behavioral asymmetry was restricted to men.

Visual lateralization and development of spatial and social spacing behaviour of chicks (Gallus gallus domesticus)

We investigated whether the development of spatial behaviour of the domestic chicken is influenced by light exposure of the embryo, as is known to be the case for some other lateralized visual functions. Ninety-six chicks were incubated in the dark or exposed to light during the final days of incubation. Half of the chicks in each group had the experience of moving behind opaque screens from 10 to 12 days of age. The other half were given transparent screens as a control. Chicks were tested in a detour test and a rotated floor test and their dispersal in groups was observed in larger pens. In the rotated floor test, chicks that had had experience with opaque screens used distal cues significantly more often than chicks that had experience with transparent screens (P=0.042), regardless of whether they had been exposed to light before hatching or incubated in the dark. There were no significant differences between treatments in the detour test or in the dispersal behaviour. Hence, visual lateralization has no influence on the development of the spatial behaviour that we tested, whereas the occlusion experience is quite specific and results in shifted attention to distal spatial cues.

Epigenesis of behavioural lateralization in humans and other animals

Despite several decades of research, the epigenesis of behavioural and brain lateralization is still elusive, although its knowledge is important in understanding developmental plasticity, function and evolution of lateralization, and its relationship with developmental disorders. Over the last decades, it has become clear that behavioural lateralization is not restricted to humans, but a fundamental principle in the organization of behaviour in vertebrates. This has opened the possibility of extending descriptive studies on human lateralization with descriptive and experimental studies on other vertebrate species. In this review, we therefore explore the evidence for the role of genes and environment on behavioural lateralization in humans and other animals. First, we discuss the predominant genetic models for human handedness, and conclude that their explanatory power alone is not sufficient, leaving, together with ambiguous results from adoption studies and selection experiments in animals, ample opportunity for a role of environmental factors. Next, we discuss the potential influence of such factors, including perinatal asymmetrical perception induced by asymmetrical head position or parental care, and social modulation, both in humans and other vertebrates, presenting some evidence from our own work on the domestic chick. We conclude that both perinatal asymmetrical perception and later social modulation are likely candidates in influencing the degree or strength of lateralization in both humans and other vertebrates. However, in most cases unequivocal evidence for this is lacking and we will point out further avenues for research.

Does testosterone affect lateralization of brain and behaviour? A meta-analysis in humans and other animal species

Lateralization of brain and behaviour has been the topic of research for many years in neuropsychology, but the factors guiding its development remain elusive. Based on sex differences in human lateralization, four hypotheses have been postulated that suggest a role for androgens, specifically testosterone. With the discovery that lateralization is a fundamental principle in the organization of brain and behaviour among vertebrates, it has now become possible to experimentally test such hypotheses in animal models. The use of different taxa, humans, other mammalian species and birds (with oestradiol and not testosterone involved in sexual differentiation in birds) facilitates to differentiate between the hypotheses. We used meta-analyses for analysing papers that provided sufficient information, and a semi-quantitative approach based on all relevant studies that we extracted from the literature. We tested the predictions of these hypotheses regarding strength and direction of lateralization for motor output, language and visuospatial cognition in these three taxa. We tested for sex differences and early organizational effects of testosterone (both correlative and experimental studies). We found sex differences in the direction of lateralization for non-human mammals (motor biases similar to humans) and in direction and strength in birds (visual cognitive tasks). However, the prediction that prenatal testosterone exposure affects the direction of lateralization was not supported for humans. In birds and non-human mammals, opposite trends were found, with the effect in non-human mammals being opposite to the expectation based on sex differences. None of the four hypotheses was sufficiently supported and more studies, testing a wider array of functions in different taxa while reporting the data more completely are needed.

Mechanisms and functions of brain and behavioural asymmetries

For almost a century the field of brain and behavioural asymmetries has been dominated by studies on humans, resting on the evidence that the anatomical structures underlying language functions are asymmetrical, and that human handedness is lateralized at the population level. Today, there is not only evidence of population-level lateralization of brain and behaviour across a variety of vertebrate and invertebrate species, but also a growing consensus that the comparative analysis of the environmental and developmental factors that give origin to neural and behavioural laterality in animal models, together with theoretical analyses of their costs and benefits, will be crucial for understanding the evolutionary pathways that led to such a multifaceted phenomenon. The present theme issue provides a survey of theoretical, review and research work cutting across the biological and the cognitive sciences, focusing on various species of fishes, birds and primates (including humans) and emphasizing an integrative approach to the study of lateralization encompassing neural, behavioural, cognitive, developmental and environmental aspects.

Escape behaviour elicited by a visual stimulus. A comparison between lateralised and non-lateralised female topminnows

Studies over the past 30 years suggest that functional lateralisation occurs in many animal species. Preferential eye use is ubiquitous among fish, and recently some advantages of being lateralised have been reported in the golden topminnow, Girardinus falcatus, using fish from lines selected for high or low degrees of behavioural lateralisation. In the present paper we investigated whether non-lateralised fish differed from lateralised fish in escape behaviour elicited by a potentially dangerous stimulus. A total of 56 female topminnows were observed when swimming in an unknown environment in which the shape of a predator was presented on either the right or the left side of the visual field. We found no side differences in latency and efficiency of escape reaction and on the whole non-lateralised fish escaped as quickly as lateralised individuals. We discuss our results in the light of recent findings suggesting that the development of lateralisation in the fast escape response in fish may be controlled by a mechanism distinct from that controlling the asymmetric placement of most other cognitive functions.

Lines of Danio rerio selected for opposite behavioural lateralization show differences in anatomical left–right asymmetries

Previous studies suggest that laterality of the viscera, morphological asymmetries of the brain, and lateralization of cognitive functions have a common genetic origin. To test this hypothesis, we conducted an artificial selection experiment for behavioural lateralization of eye use in two strains (TL and GT) of zebrafish ( Danio rerio), maintaining one selected line in each strain for five generations. In addition, we investigated, using molecular markers, whether there was any correlation among directionality in eye preference, diencephalic left–right asymmetries in the brain and positioning of the viscera. After one generation of selection, the right- and left-eye lines of both strains showed a significant difference in the behavioural trait. This difference was maintained for all the five generations even though we observed a progressive decline in the response to artificial selection in subsequent generations for both strains. Overall, anatomical evidence suggests that selection for right-eye use significantly increased the frequency of reversed asymmetry in the epithalamus while selection for left-eye use decreased it. However, the response was irregular since not all samples conformed to this pattern. The association between the direction of behavioural selection and pancreas position was less clear-cut, although the concordance between visceral and brain asymmetries exceeded 90% in both strains.

Behavioral lateralization and prenatal exposure to antiepileptic drugs: Evidence for increased non-right hand preference

Behavioral lateralization and prenatal exposure to antiepileptic drugs: Evidence for increased non-right hand preference

Effects of early adverse experiences on behavioural lateralisation in rhesus monkeys (Macaca mulatta)

In the past 15 to 20 years, evidence of population-level handedness in non-human primates has emerged from a plethora of studies, although considerable inconsistency is also apparent. The study reported here examined two factors that may contribute to the expression of hand preference: early rearing history and sex differences. Handedness was assessed in rhesus monkeys (Macaca mulatta) using a task that measures coordinated bimanual actions and is referred to as the TUBE task. Nursery-reared monkeys demonstrated greater left-hand bias in the TUBE task when compared to their mother-reared counterparts. Females showed greater right-hand preference and stronger bias on the TUBE task compared to males. These results provide evidence that early rearing experiences significantly influence the development of lateralisation in nonhuman primates.

The development and lateralization of prey delivery in a bill load-holding bird

Laterality or the preferential use of one or the other side of the body is associated with differential brain activity and increased specialization of brain function. Right or left biases are widespread among vertebrates and have been documented among some birds. Bill load holding or the delivery of whole prey in a bird's beak is common among terns (Charadriiformes) and many other birds. We recorded more than 2000 Caspian tern, Hydroprogne caspia, chick-feeding events for analysis of lateralization of prey within the bills of adult birds, size and shape of prey items delivered to chicks in relation to chick age, and the development of prey-handling skills among chicks. No initial lateralization of prey head position was found as adults flew into the colony, but head position of successful feeds was found to be significantly lateralized with a bias to the right side. Adults switched prey orientation significantly more often from left to right than from right to left without dropping the prey item, suggesting an adult bias. Adults appeared to adjust the length but not the shape of prey delivered according to chick age. Ability of chicks to manipulate prey items increased with age. Lateralization was most obvious in the first week of a tern's life, and adults modified their delivery behaviour to respond to these changes. Bill load-holding birds are excellent subjects to study lateralization of feeding behaviour in the wild and they may allow integration of lateralization with developmental changes.

Correlation of the shoulder girdle asymmetry with the limb skeleton asymmetry in Xenopus laevis

Cartilaginous epicoracoid plates in the arcipheral pectoral girdle of modern amphibians intersect ventrally along the body midline and overlap so that either the right or the left plate is located dorsal to the other [1, 2]. The ratio between the left and right variants in amphibian populations is species-specific; in different species, the left epicoracoid is in the dorsal position 3‐ 20 times more often than the right one [3‐6]. There is a hypothesis [4] that the asymmetric structure of the shoulder girdle is determined by the difference in the muscle tone between the sides of the body, which is, in turn, related to the functional asymmetry of the nervous system: differences in muscle tone lead to the shift of one epicoracoid away from the midline. Indeed, there is an association between the directions of the asymmetry of the shoulder girdle and the lateralization of the use of forelimbs by Bombina bombina in the snout-wiping test [5]. On the other hand, no significant correlation between the shoulder girdle asymmetry and preferential use of the right or left forelimb in the underwater righting test has been found in Bufo marinus [7]. We believe that this discrepancy between the results of the two tests appears because the asymmetric structure of the girdle affects the results of a more difficult test (performed by a semiaquatic toad species outside the water), but not the results of an easier test (performed by a terrestrial toad species underwater) [1]. Although the African smooth clawed frog ( Xenopus laevis ) is a traditional embryological object, and the asymmetry of its internal organs is being intensely studied [8], little is known about behavioral lateralization and the asymmetry of the postcranial skeleton in this species. Our preliminary data demonstrated that, in contrast to toads of the genus Bufo , X. laevis has a low ratio of the left variants of the shoulder girdle to the right ones [3], which increases the probability of finding the rarer (right) phenotype in a sample. Therefore, we used representatives of this species to study the correlation between the functional and morphological asymmetries of the locomotor system. To estimate preferences in the use of the limbs, we performed two experiments. In one of them, the tested animal was put into a Y-maze through a hole at the top (Fig. 1). First, the frog sank to the bottom of the maze; 10‐20 min later, it surfaced to breathe, faced an obstacle (the hole had been plugged by that time) and had to turn to the right or left arm of the maze. We recorded the first 10 turns. In the second experiment, the tested animal was put into a nontransparent plastic cylinder filled with water and evenly illuminated from the top. The frogs’ behavior was recorded for 3‐4 h by means of an autonomous video camera. After surfacing to breathe, the frogs made a stroke with the left or the right hindlimb before diving, thus turning to the side opposite to the stroking limb. When analyzing video recordings in the slow-motion mode, the first 10 turns were scored. In both experiments, the animal was considered to be “right-handed” or “left-handed” if the number of turns to one side was larger than 8. The significance of the trend toward one of the sides was tested using the G -test.

Consistency of hand preference across low‐level and high‐level tasks in Capuchin monkeys (Cebus apella)

Numerous studies investigating behavioral lateralization in capuchins have been published. Although some research groups have reported a population-level hand preference, other researchers have argued that capuchins do not show hand preference at the population level. As task complexity influences the expression of handedness in other primate species, the purpose of this study was to collect hand preference data across a variety of high- and low-level tasks to evaluate how task complexity influences the expression of hand preference in capuchins. We tested eleven captive brown capuchin monkeys (Cebus apella) to determine if they show consistent hand preferences across multiple high- and low-level tasks. Capuchins were expected to display high intertask consistency across the high-level tasks but not the low-level tasks. Although most individuals showed significant hand preferences for each task, only two of the high-level tasks that involved similar hand motions were significantly positively correlated, indicating consistency of hand preference across these tasks only. None of the tasks elicited a group-level hand preference. High-level tasks elicited a greater strength of hand preference than did low-level tasks. No sex differences were found for the direction or strength of hand preference for any task. These results contribute to the growing database of primate laterality and provide additional evidence that capuchins do not display group-level hand preferences.

Influence of behavioural lateralization on interleukin-2 and interleukin-6 gene expression in dogs before and after immunization with rabies vaccine

Evidence in several species, including dogs, has been collected demonstrating that the brain hemispheres modulate the immune system in an asymmetrical way. To study the interactions between immune response and lateralization, three groups of mixed breed dogs were selected on the basis of their performance in a paw preference test involving removal of a piece of sticky tape from the snout. The expression of interleukin-2 (IL-2) and interleukin-6 (IL-6) genes was measured in left-pawed, right-pawed and ambidextrous dogs before and after immunization treatment with a rabies vaccine. The results revealed a relationship between the mRNA expression of IL-2 and IL-6 genes and the direction of behavioural lateralization. Under basal conditions, IL-2 and IL-6 gene expression was higher in left-pawed dogs than in right-pawed and ambidextrous dogs. After the vaccine administration, decreasing levels of IL-2 and IL-6 gene expression were observed in left-pawed and right-pawed dogs, but not in ambidextrous dogs. These findings represent the first evidence that brain lateralization may influence the immune system in dogs by the modulation of mRNA gene expression of cytokines such as IL-2 and IL-6, which have been recognized as key immune-regulatory proteins.

Behavioural lateralization in sheep ( Ovis aries)

This study investigates behavioural lateralization in sheep and lambs of different ages. A flock was tested in a task in which the animals were facing an obstacle and should avoid it on either the right or left side to rejoin flock-mates (adult sheep) or their mothers (lambs). A bias for avoiding the obstacle on the right side was observed, with lambs apparently being more lateralized than sheep. This right bias was tentatively associated with the left-hemifield laterality in familiar faces recognition which has been documented in this species. Differences between adult sheep and lambs were likely to be due to differences in social reinstatement motivation elicited by different stimuli (flock-mates or mothers) at different ages. Preferential use of the forelegs to step on a wood-board and direction of jaw movement during rumination was also tested in adult animals. No population bias nor individual-level lateralization was observed for use of the forelegs. At the same time, however, there was a large number of animals showing individual-level lateralization for the direction of jaw movement during rumination even though there was no population bias. These findings highlight that within the same species individual- and population-level lateralization can be observed in different tasks. Moreover, the results fit the general hypothesis that population-level asymmetries are more likely to occur in tasks that require social coordination among behaviourally asymmetric individuals.

Histological asymmetries of primary motor cortex predict handedness in chimpanzees (Pan troglodytes)

Like humans, chimpanzees display robust and consistent hand preferences during the performance of certain tasks. Although correlations have been demonstrated between gross anatomic measures of primary motor cortex asymmetry and handedness in captive chimpanzees, the relationship between histological architecture and behavioral lateralization has not yet been investigated. Therefore, we examined interhemispheric asymmetry of several different microstructural characteristics of the primary motor cortex in the region of hand representation from 18 chimpanzees tested on a coordinated bimanual task before death. At the population level our data showed leftward bias for higher layer II/III neuron density. Of note, however, there was no population-level asymmetry in the areal fraction of Nissl-stained cell bodies, a finding that differs from previous studies of this cortical region in humans. Nonetheless, we found that asymmetry in the density of layer II/III parvalbumin-immunoreactive interneurons was the best predictor of individual hand preference. These results suggest that histological asymmetries are related to handedness in chimpanzees, while overall patterns of asymmetry at the population level might differ from humans.