Behavioral Lateralization Research Articles

Individual and population-level sex-dependent lateralization in yellow-legged gull (Larus michahellis) chicks

Behavioral lateralization at the population level is widespread across vertebrates, with considerable variation among species. However, evidence for individual-level and sex-dependent lateralization is sparse and inconsistent in fish, reptiles and birds. In addition, covariation of lateralization with position in the laying sequence, which is expected because the concentration of maternal egg hormones varies with laying order, has never been investigated. We analyzed lateralization of yellow-legged gull (Larus michahellis) chicks in reverting from supine to prone posture (‘RTP’ response) and in pecking at a dummy parental bill to solicit food provisioning (‘begging’ response). Chicks were lateralized both at the population and at the individual level in the RTP response and at the individual level in begging. Lateralization in the RTP was sex-dependent, as females showed a leftward preference. Lateralization in either motor task was not correlated within individuals. Lateralization did not differ among families, suggesting little additive genetic variation. Lateral preference in begging response varied according to laying order and matched variation in egg androgens concentration. Our study confirms previous findings on population-level lateralization and adds to the scant information on individual-level and heritable variation in lateralization in birds. Moreover, it hints at epigenetic components in lateralization depending on maternal effects.

Do right-biased boxers do it better? Population-level asymmetry of aggressive displays enhances fighting success in blowflies

Lateralisation (i.e. left-right asymmetries in brain and behaviour) of aggressive traits has been deeply studied in a number of vertebrates, while evidence for invertebrates is scarce. We investigated lateralisation of boxing behaviour in the blowfly Calliphora vomitoria (Diptera: Calliphoridae), where males fight for non-resource based spaces. We found a population-level lateralisation of aggressive displays: three repeated testing phases confirmed the preferential use of right legs over left ones. Duration of contests and number of boxing acts per fighting event were not different between males using left and right legs. The use of right legs for boxing acts lead to higher fighting success over males using left legs. Lateralised aggressive displays at population-level may be connected to the prolonged social interactions occurring among males searching for food and mates.

First report of behavioural lateralisation in mosquitoes: right-biased kicking behaviour against males in females of the Asian tiger mosquito, Aedes albopictus.

Lateralisation (i.e. functional and/or structural specialisations of left and right sides of the brain) of aggressive traits has been studied in a number of vertebrates, while evidence for invertebrates is scarce. Mosquito females display aggressive responses against undesired males, performing rejection kicks with the hind legs. In this research, we examined lateralisation of kicking behaviour in females of the Asian tiger mosquito, Aedes albopictus. We found a right-biased population-level lateralisation of kicking behaviour. Four repeated testing phases on mosquito females confirmed the preferential use of right legs. However, when left legs were used, the mean number of kicks per rejection event was not different to that performed with right legs. Both left and right kicking behaviour lead to successful displacement of undesired partners. This is the first report about behavioural lateralisation in mosquitoes.

Lateralization of behavior in dairy cows in response to conspecifics and novel persons

The right brain hemisphere, connected to the left eye, coordinates fight and flight behaviors in a wide variety of vertebrate species. We investigated whether left eye vision predominates in dairy cows’ interactions with other cows and humans, and whether dominance status affects the extent of visual lateralization. Although we found no overall lateralization of eye use to view other cows during interactions, cows that were submissive in an interaction were more likely to use their left eye to view a dominant animal. Both subordinate and older cows were more likely to use their left eye to view other cattle during interactions. Cows that predominantly used their left eye during aggressive interactions were more likely to use their left eye to view a person in unfamiliar clothing in the middle of a track by passing them on the right side. However, a person in familiar clothing was viewed predominantly with the right eye when they passed mainly on the left side. Cows predominantly using their left eyes in cow-to-cow interactions showed more overt responses to restraint in a crush compared with cows who predominantly used their right eyes during interactions (crush scores: left eye users 7.9, right eye users 6.4, standard error of the difference=0.72). Thus, interactions between 2 cows and between cows and people were visually lateralized, with losing and subordinate cows being more likely to use their left eyes to view winning and dominant cattle and unfamiliar humans.

First record of limb preferences in monotremes (Zaglossus spp.)

Lateralisation in forelimb use at the population and/or individual level has been found in a wide variety of vertebrate species. However, some large taxa have not yet been investigated and that limits a proper evolutionary interpretation of forelimb preferences. Among mammals lateralised use of the forelimbs has been shown for both placentals and marsupials, but nothing is known about behavioural lateralisation in monotremes. Here we examined lateral preferences in forelimb use in four long-beaked echidnas (male and female Zaglossus bruijni, and male and female Z. bartoni) in captivity. Three individuals showed significant forelimb preferences in unimanual behaviours associated with feeding. When stepping on an eminence with one forelimb first, the lateralisation at the individual level was found only in males of both species. During male–female interactions, the male Z. bartoni significantly preferred to put one of the forelimbs on the female’s back. In both males, the direction of preferences was consistent across different types of behaviour. Our results confirm that manual lateralisation, at least at the individual level, is widespread among mammals. Further research is needed to investigate whether the monotremes display population-level lateralisation in forelimb use.

Behavioural responses to simulated bird attacks in marine three-spined sticklebacks after exposure to high CO2 levels

The rising partial pressure of CO2 (pCO2) in oceanic water, termed ocean acidification, is an impending threat to marine life and has previously been reported to affect several aspects of fish behaviour. We evaluated the behavioural response to a simulated avian predator attack and lateralisation in three-spined sticklebacks (Gasterosteus aculeatus) after 10 and 20 days of exposure to present day pCO2 (400μatm) or elevated pCO2 (1000μatm). We show that elevated pCO2 lead to reduced behavioural lateralisation. However, no major differences in the sheltering response after an overhead avian attack were observed; fish from both treatments exhibited similar and strong responses. Compared with fish exposed to high pCO2, the control fish took longer time to freeze (i.e. stop moving) after attack at Day 20 but not Day 10. The freezing duration was significantly reduced between Day 10 and Day 20 in elevated pCO2, whereas no such reduction was observed in the control-group. However, no significant differences between treatment groups were detected at Day 20. These results demonstrate that behaviour is indeed altered by high CO2 levels, although the general responses to avian predation stimuli remain similar to those of unexposed fish, indicating that some predator avoidance behaviours of three-spined sticklebacks are robust to environmental disturbance.

Aggression in Tephritidae Flies: Where, When, Why? Future Directions for Research in Integrated Pest Management.

True fruit flies (Diptera: Tephritidae) include over 4000 species, many of which constitute enormous threats to fruit and vegetable production worldwide. A number of Tephritidae are lekking species, forming aggregations in which males fight to defend a small territory where they court females and mate. Male-male contests also occur in non-lekking species, characterized by resource defense polygyny. Tephritidae females display agonistic behavior to maintain single oviposition sites and reduce larval competition for food. Here, how, where, when and why aggressive interactions occur in Tephritidae flies is reviewed. A number of neglected issues deserving further research are highlighted, with a special focus on diel periodicity of aggression, cues evoking aggressive behavior, the role of previous experience on fighting success and the evolution of behavioral lateralization of aggressive displays. In the final section, future directions to exploit this knowledge in Integrated Pest Management, with particular emphasis on enhancement of Sterile Insect Technique and interspecific competitive displacement in the field are suggested.

Ants show a leftward turning bias when exploring unknown nest sites

Behavioural lateralization in invertebrates is an important field of study because it may provide insights into the early origins of lateralization seen in a diversity of organisms. Here, we present evidence for a leftward turning bias in Temnothorax albipennis ants exploring nest cavities and in branching mazes, where the bias is initially obscured by thigmotaxis (wall-following) behaviour. Forward travel with a consistent turning bias in either direction is an effective nest exploration method, and a simple decision-making heuristic to employ when faced with multiple directional choices. Replication of the same bias at the colony level would also reduce individual predation risk through aggregation effects, and may lead to a faster attainment of a quorum threshold for nest migration. We suggest the turning bias may be the result of an evolutionary interplay between vision, exploration and migration factors, promoted by the ants' eusociality.

Lateralization and cognitive systems.

Lateralization and cognitive systems.

The contribution of cortical thickness and surface area to gray matter asymmetries in the healthy human brain.

Human cortical gray matter (GM) is structurally asymmetrical and this asymmetry has been discussed to be partly responsible for functional lateralization of human cognition and behavior. Past studies on brain asymmetry have shown mixed results so far, with some studies focusing on the global shapes of the brain's surface, such as gyrification patterns, while others focused on regional brain volumes. In this study, we investigated cortical GM asymmetries in a large sample of right-handed healthy volunteers (n = 101), using a surface-based method which allows to analyze brain cortical thickness and surface area separately. As a result, substantially different patterns of symmetry emerged between cortical thickness and surface area measures. In general, asymmetry is more prominent in the measure of surface compared to that of thickness. Such a detailed investigation of structural asymmetries in the normal brain contributes largely to our knowledge of normal brain development and also offers insights into the neurodevelopmental basis of psychiatric disorders, such as schizophrenia.

Testing for Behavioral Lateralization in Observational Data: a Monte Carlo Approach Applied to Neck-looping in American Flamingos

Abstract We applied a Monte Carlo approach to test for both individual and group level laterality preferences in neck looping by American Flamingos (Phoenicopterus ruber ruber) at rest. We found no evidence of individual or group-level preferences, contrary to the results of previous studies. In the present data, the appearance of bias tended to decrease as the number of observations increased, suggesting that apparent lateral bias may be largely because of stochastic error. Pair members tended to loop the neck to the same side on the same day to a greater extent than expected by chance, implying that social factors can act contrary to any individual lateral preference that may exist in this species.

Hemispheric side of damage influences sex-related differences in smoking cessation in neurological patients

Patterns of smoking behavior vary between the sexes. There is evidence that decision making, which is one of the key “executive functions” necessary for making life-style modifications such as smoking cessation, is relatively lateralized to the right hemisphere in males and left hemisphere in females. In the current study, we examined whether the side of brain lesion has a differential effect on smoking behavior between the sexes. We hypothesized sex differences in smoking cessation based on lesion side. Participants were 49 males and 50 females who were smoking at the time of lesion onset. The outcome variable was abstinence from smoking (quit rate) at least one year post lesion. We found that in patients with left-hemisphere damage, quit rates were significantly higher in males than in females; however, in patients with right-hemisphere damage, quit rates were not statistically different. The findings support previous cognitive neuroscience literature showing that components of behavior responsible for maintaining addiction tend to be more strongly lateralized in males, whereas in females there is a more bilateral distribution. Our study provides further evidence for differences in lateralization of complex behavior between the sexes, which has significant implications for differences in treatment strategies between the sexes.

Behavioral Lateralization and Optimal Route Choice in Flying Budgerigars

Birds flying through a cluttered environment require the ability to choose routes that will take them through the environment safely and quickly. We have investigated some of the strategies by which they achieve this. We trained budgerigars to fly through a tunnel in which they encountered a barrier that offered two passages, positioned side by side, at the halfway point. When one of the passages was substantially wider than the other, the birds tended to fly through the wider passage to continue their transit to the end of the tunnel, regardless of whether this passage was on the right or the left. Evidently, the birds were selecting the safest and quickest route. However, when the two passages were of equal or nearly equal width, some individuals consistently preferred the left-hand passage, while others consistently preferred the passage on the right. Thus, the birds displayed idiosyncratic biases when choosing between alternative routes. Surprisingly - and unlike most of the instances in which behavioral lateralization has previously been discovered - the bias was found to vary from individual to individual, in its direction as well as its magnitude. This is very different from handedness in humans, where the majority of humans are right-handed, giving rise to a so-called ‘population’ bias. Our experimental results and mathematical model of this behavior suggest that individually varying lateralization, working in concert with a tendency to choose the wider aperture, can expedite the passage of a flock of birds through a cluttered environment.

When right differs from left: Human limb directional asymmetry emerges during very early development

The often observed directional asymmetry (DA) in human limb bones may have a genetic/developmental basis and/or could emerge from different mechanical loadings across sides due to handedness. Because behavioural lateralization in itself has a genetic basis, it has been suggested that DA in limbs could develop prenatally as a pre-adaptation to adult life. However, the presence of consistent differences in the size of left and right limb bones in early development is understudied. We study asymmetry in limb bones during early development (10–20 weeks of gestation) in a sample of 178 aborted foetuses. Statistically significant DA was found in several upper and lower limb bones, where the right-hand side was consistently larger than the left. We argue that this pattern is probably the consequence of developmental processes related to internal asymmetric positioning of organs.

Shifting from Right to Left: The Combined Effect of Elevated CO2 and Temperature on Behavioural Lateralization in a Coral Reef Fish

Recent studies have shown that elevated CO2 can affect the behaviour of larval and juvenile fishes. In particular, behavioural lateralization, an expression of brain functional asymmetries, is affected by elevated CO2 in both coral reef and temperate fishes. However, the potentially interacting effects of rising temperatures and CO2 on lateralization are unknown. Here, we tested the combined effect of near-future elevated-CO2 concentrations (930 µatm) and temperature variation on behavioural lateralization of a marine damselfish, Pomacentrus wardi. Individuals exposed to one of four treatments (two CO2 levels and two temperatures) were observed in a detour test where they made repeated decisions about turning left or right. Individuals exposed to current CO2 and ambient temperature levels showed a significant right-turning bias at the population level. This biased was reversed (i.e. to the left side) in fish exposed to the elevated-CO2 treatment. Increased temperature attenuated this effect, resulting in lower values of relative lateralization. Consequently, rising temperature and elevated CO2 may have different and interactive effects on behavioural lateralization and therefore future studies on the effect of climate change on brain functions need to consider both these critical variables in order to assess the potential consequences for the ecological interactions of marine fishes.

Loss of molars early in life develops behavioral lateralization and impairs hippocampus-dependent recognition memory

BackgroundUsing senescence-accelerated mouse prone 8 (SAMP8), we examined whether reduced mastication from a young age affects hippocampal-dependent cognitive function. We anesthetized male SAMP8 mice at 8 weeks of age and extracted all maxillary molar teeth of half the animals. The other animals were treated similarly, except that molar teeth were not extracted. At 12 and 24 weeks of age, their general behavior and their ability to recognize novel objects were tested using the open-field test (OFT) and the object-recognition test (ORT), respectively.ResultsThe body weight of molarless mice was reduced significantly compared to that of molar-intact mice after the extraction and did not recover to the weight of age-matched molar-intact mice throughout the experimental period. At 12 weeks of age, molarless mice showed significantly greater locomotor activity in the OFT than molar-intact mice. However, the ability of molarless mice to discriminate a novel object in the ORT was impaired compared to that of molar-intact mice. The ability of both molarless and molar-intact SAMP8 mice to recognize objects was impaired at 24 weeks of age. These results suggest that molarless SAMP8 mice develop a deficit of cognitive function earlier than molar-intact SAMP8 mice. Interestingly, both at 12 and 24 weeks of age, molarless mice showed a lateralized preference of object location in the encoding session of the ORT, in which two identical objects were presented. Their lateralized preference of object location was positively correlated with the rightward turning-direction preference, which reached statistical significance at 24 weeks of age.ConclusionsLoss of masticatory function in early life causes malnutrition and chronic stress and impairs the ability to recognize novel objects. Hyperactivation and lateralized rotational behavior are commonly observed with dysfunction of the dopaminergic system, therefore, reduced masticatory function may deplete the mesolimbic and mesocorticolimbic dopaminergic systems to impair the cognitive functions of selective attention and recognition memory in the prefrontal cortex and the hippocampus.

Severe hypoxia impairs lateralization in a marine teleost fish.

In intertidal environments, the recurring hypoxic condition at low tide is one of the main factors affecting fish behaviour, causing broad effects on ecological interactions. We assessed the effects of hypoxia on lateralization (e.g. the tendency to turn left or right), a behaviour related to brain functional asymmetry, which is thought to play a key role in several life history aspects of fish. Using staghorn sculpin (Leptocottus armatus), a benthic fish that typically inhabits the intertidal zone, we found that hypoxia affects behavioural lateralization at the population level. On average, staghorn sculpins showed a distinct preference for right turns under normoxic conditions (>90% oxygen saturation), but an equal probability of turning right or left after exposure to hypoxia for 2 h (20% oxygen saturation). The specific turning preference observed in the staghorn sculpin control population is likely to have an adaptive value, for example in predator-prey interactions by enhancing attack success or survival from predatory attacks. Therefore the alteration of lateralization expressed by staghorn sculpins under hypoxic conditions may have far-reaching implications for species ecology and trophic interactions. Moreover, our work raises the need to study this effect in other species, in which a hypoxia-driven disruption of lateralization could affect a wider range of behaviours, such as social interactions and schooling.

Catecholamine plasma levels, IFN-γ serum levels and antibodies production induced by rabies vaccine in dogs selected for their paw preference

To explore the possible role of the sympathetic nervous activity in the asymmetrical crosstalk between the brain and immune system, catecholamine (E, NE) plasma levels, Interferon-γ (IFN-γ) serum levels and production of antibodies induced by rabies vaccine in dogs selected for their paw preference were measured. The results showed that the direction of behavioural lateralization influenced both epinephrine levels and immune response in dogs. A different kinetic of epinephrine levels after immunization was observed in left-pawed dogs compared to both right-pawed and ambidextrous dogs. The titers of antirabies antibodies were lower in left-pawed dogs than in right-pawed and ambidextrous dogs. Similarly, the IFN-γ serum levels were lower in left-pawed dogs than in the other two groups. Taken together, these findings showed that the left-pawed group appeared to be consistently the different group stressing the fundamental role played by the sympathetic nervous system as a mechanistic basis for the crosstalk between the brain and the immune system.

Behavioural Lateralization in Budgerigars Varies with the Task and the Individual

Handedness/footedness and side biases are a well-known phenomenon in many animals, including humans. However, these so-called biases have mostly been studied at the population level - individual biases have received less attention, especially with regard to consistency over different tasks. Here we investigate behavioral lateralization in 12 male Budgerigars, Melopsittacus undulatus, a social parrot inhabiting the Australian bushlands. We performed 5 types of experiments to investigate lateralization, in tasks that involved climbing onto a perch, or landing on perches arranged in various configurations. The birds displayed highly significant, individually varying biases. The bias displayed by any particular individual varied with the task, in strength as well as polarity. Analysis of the data revealed that the preferred foot used for climbing did not coincide with the foot that was used while landing. Thus, landing choices are probably not determined by foot bias. Furthermore, these individual preferences were overridden completely when a bird had to perform a task simultaneously with another bird.

Heritabilities of directional asymmetry in the fore- and hindlimbs of rabbit fetuses.

Directional asymmetry (DA), where at the population level symmetry differs from zero, has been reported in a wide range of traits and taxa, even for traits in which symmetry is expected to be the target of selection such as limbs or wings. In invertebrates, DA has been suggested to be non-adaptive. In vertebrates, there has been a wealth of research linking morphological asymmetry to behavioural lateralisation. On the other hand, the prenatal expression of DA and evidences for quantitative genetic variation for asymmetry may suggest it is not solely induced by differences in mechanic loading between sides. We estimate quantitative genetic variation of fetal limb asymmetry in a large dataset of rabbits. Our results showed a low but highly significant level of DA that is partially under genetic control for all traits, with forelimbs displaying higher levels of asymmetry. Genetic correlations were positive within limbs, but negative across bones of fore and hind limbs. Environmental correlations were positive for all, but smaller across fore and hind limbs. We discuss our results in light of the existence and maintenance of DA in locomotory traits.