Strength of forelimb lateralization predicts motor errors in an insect

Lateralized behaviours are widespread in both vertebrates and invertebrates, suggesting that lateralization is advantageous. Yet evidence demonstrating proximate or ultimate advantages remains scarce, particularly in invertebrates or in species with individual-level lateralization. Desert locusts (Schistocerca gregaria) are biased in the forelimb they use to perform targeted reaching across a gap. The forelimb and strength of this bias differed among individuals, indicative of individual-level lateralization. Here we show that strongly biased locusts perform better during gap-crossing, making fewer errors with their preferred forelimb. The number of targeting errors locusts make negatively correlates with the strength of forelimb lateralization. This provides evidence that stronger lateralization confers an advantage in terms of improved motor control in an invertebrate with individual-level lateralization.     

Behavioral and neural lateralization of vision in courtship singing of the zebra finch

Along with human speech and language processing, birdsong has been one of the best-characterized model systems for understanding the relationship of lateralization of brain function to behavior. Lateralization of song production has been extensively characterized, and lateralization of song perception has begun to be studied. Here we have begun to examine whether behavior and brain function are lateralized in relation to communicative aspects of singing, as well. In order to monitor central brain function, we assayed the levels of several activity dependent immediate early genes after directed courtship singing. Consistent with a lateralization of visual processing during communication, there were higher levels of expression of both egr-1 and c-fos in the left optic tectum after directed singing. Because input from the eyes to the brain is almost completely contralateral in birds, these results suggest that visual input from the right eye should be favored during normal singing to females. Consistent with this, we further found that males sang more when they could use only their right eye compared to when they could use only their left eye. Normal levels of singing, though, required free use of both eyes to view the female. These results suggest that there is a preference for visual processing by the right eye and left brain hemisphere during courtship singing. This may reflect a proposed specialization of the avian left hemisphere in sustaining attention on stimuli toward which a motor response is planned.     

Identification, genomic organization, chromosomal mapping and mutation analysis of the human INV gene, the ortholog of a murine gene implicated in left-right axis development and biliary atresia

Determination of left-right axis is a precocious embryonic event, and all phenotypic anomalies resulting from disruption of the normal lateralization process are collectively referred to as the lateralization defect. A transgenic mouse with lateralization defect and hepatic, kidney, and pancreatic anomalies has resulted from disruption of the inv gene by insertion of a transgene. The human ortholog is thus a good candidate for lateralization defect in humans, in particular in cases with associated hepatic anomalies. Here, we have identified, mapped, and characterized the INV human gene and screened a series of heterotaxic patients (with or without biliary anomalies) for mutation in this gene. In a German family of Turkish origin, we have found that all available affected and unaffected individuals are heterozygous for a mutation in the splicing donor site of intron 12 in the INV gene resulting in two different aberrant splicing isoforms. This can be explained either by a randomization of lateralization defects or, as suggested earlier, di- or trigenic inheritance, although we have been unable to detect, in this family, a mutation in genes known to be involved in the human lateralization defect ( LEFTY1, LEFTY2, ACVR2B, NODAL, ZIC3, and CFC1). In contrast to the mouse, the affected individuals have no biliary anomalies, and the absence of mutation in a series of seven cases with lateralization defect and biliary anomalies demonstrates that INV is not frequently involved in such a phenotype in humans.     

Lateralization of olfaction in the honeybee Apis mellifera

Lateralization of function is a well-known phenomenon in humans. The two hemispheres of the human brain are functionally specialized such that certain cognitive skills, such as language or musical ability, conspecific recognition, and even emotional responses, are mediated by one hemisphere more than the other [1, 2]. Studies over the past 30 years suggest that lateralization occurs in other vertebrate species as well [3-11]. In general, lateralization is observed in different sensory modalities in humans as well as vertebrates, and there are interesting parallels (reviewed in [12]). However, little is known about functional asymmetry in invertebrates [13, 14] and there is only one investigation in insects [15]. Here we show, for the first time, that the honeybee Apis mellifera displays a clear laterality in responding to learned odors. By training honeybees on two different versions of the well-known proboscis extension reflex (PER) paradigm [16, 17], we demonstrate that bees respond to odors better when they are trained through their right antenna. To our knowledge, this is the first demonstration of asymmetrical learning performance in an insect.     

Assessment of Cerebral Lateralization in Children using Functional Transcranial Doppler Ultrasound (fTCD)

There are many unanswered questions about cerebral lateralization. In particular, it remains unclear which aspects of language and nonverbal ability are lateralized, whether there are any disadvantages associated with atypical patterns of cerebral lateralization, and whether cerebral lateralization develops with age. In the past, researchers interested in these questions tended to use handedness as a proxy measure for cerebral lateralization, but this is unsatisfactory because handedness is only a weak and indirect indicator of laterality of cognitive functions¹. Other methods, such as fMRI, are expensive for large-scale studies, and not always feasible with children².Here we will describe the use of functional transcranial Doppler ultrasound (fTCD) as a cost-effective, non-invasive and reliable method for assessing cerebral lateralization. The procedure involves measuring blood flow in the middle cerebral artery via an ultrasound probe placed just in front of the ear. Our work builds on work by Rune Aaslid, who co-introduced TCD in 1982, and Stefan Knecht, Michael Deppe and their colleagues at the University of Münster, who pioneered the use of simultaneous measurements of left- and right middle cerebral artery blood flow, and devised a method of correcting for heart beat activity. This made it possible to see a clear increase in left-sided blood flow during language generation, with lateralization agreeing well with that obtained using other methods³.The middle cerebral artery has a very wide vascular territory (see Figure 1) and the method does not provide useful information about localization within a hemisphere. Our experience suggests it is particularly sensitive to tasks that involve explicit or implicit speech production. The ''gold standard'' task is a word generation task (e.g. think of as many words as you can that begin with the letter ''B'') ⁴, but this is not suitable for young children and others with limited literacy skills. Compared with other brain imaging methods, fTCD is relatively unaffected by movement artefacts from speaking, and so we are able to get a reliable result from tasks that involve describing pictures aloud^5,6. Accordingly, we have developed a child-friendly task that involves looking at video-clips that tell a story, and then describing what was seen.     

Lateralization in monogamous pairs:wild geese prefer to keep their partner in the left hemifield except when disturbed

Behavioural lateralization, which reflects the functional specializations of the two brain hemispheres, is assumed to play an important role in cooperative intraspecific interactions. However, there are few studies focused on the lateralization in cooperative behaviours of individuals, especially in a natural setting. In the present study, we investigated lateralized spatial interactions between the partners in life-long monogamous pairs. The male-female pairs of two geese species (barnacle, Branta leucopsis, and white-fronted, Anser albifrons geese), were observed during different stages of the annual cycle in a variety of conditions. In geese flocks, we recorded which visual hemifield (left/right) the following partner used to monitor the leading partner relevant to the type of behaviour and the disturbance factors. In a significant majority of pairs, the following bird viewed the leading partner with the left eye during routine behaviours such as resting and feeding in undisturbed conditions. This behavioural lateralization, implicating the right hemisphere processing, was consistent across the different aggregation sites and years of the study. In contrast, no significant bias was found in a variety of geese behaviours associated with enhanced disturbance (when alert on water, flying or fleeing away when disturbed, feeding during the hunting period, in urban area feeding and during moulting). We hypothesize that the increased demands for right hemisphere processing to deal with stressful and emergency situations may interfere with the manifestation of lateralization in social interactions.     

Aggression, sex and individual differences in cerebral lateralization in a cichlid fish

Cerebral lateralization is an evolutionarily ancient adaptation, apparently ubiquitous among vertebrates. Despite demonstrated advantages of having a more lateralized brain, substantial variability in the strength of lateralization exists within most species. The underlying reasons for the maintenance of this variation are largely unknown. Here, we present evidence that the strength of lateralization is linked to a behavioural trait, aggressiveness, in the convict cichlid (Archocentrus nigrofasciatus), and that this relationship depends on the sex of the fish. This finding suggests that individual variation in behaviour may be linked to variation in cerebral lateralization, and must be studied with regard to the sex of the animal.     

Lateralized behaviour of a non-social cichlid fish (Amatitlania nigrofasciata) in a social and a non-social environment

Cerebral lateralization, the partitioning of cognitive function preferentially into one hemisphere of the brain, is a trait ubiquitous among vertebrates. Some species exhibit population level lateralization, where the pattern of cerebral lateralization is the same for most members of that species; however, other species show only individual level lateralization, where each member of the species has a unique pattern of lateralized brain function. The pattern of cerebral lateralization within a population and an individual has been shown to differ based on the stimulus being processed. It has been hypothesized that sociality within a species, such as shoaling behaviour in fish, may have led to the development and persistence of population level lateralization. Here we assessed cerebral lateralization in convict cichlids (Amatitlania nigrofasciata), a species that does not shoal as adults but that shoals briefly as juveniles. We show that both male and female convict cichlids display population level lateralization when in a solitary environment but only females show population level lateralization when in a perceived social environment. We also show that the pattern of lateralization differs between these two tasks and that strength of lateralization in one task is not predictive of strength of lateralization in the other task.     

Yolk testosterone affects growth and promotes individual-level consistency in behavioral lateralization of yellow-legged gull chicks

Behavioral lateralization is common in animals and may be expressed at the individual- and at the population-level. The ontogenetic processes that control lateralization, however, are largely unknown. Well-established sex-dependence in androgen physiology and sex-dependent variation in lateralization have led to the hypothesis that testosterone (T) has organizational effects on lateralization. The effects of T exposure in early life on lateralization can be efficiently investigated by manipulating T levels in the cleidoic eggs of birds, because the embryo is isolated from maternal and sibling physiological interference, but this approach has been adopted very rarely. In the yellow-legged gull (Larus michahellis) we increased yolk T concentration within the physiological limits and tested the effects on the direction of lateralization in two functionally fundamental behaviors (begging for parental care and escape to cover) of molecularly sexed hatchlings. We also speculated that T may intervene in regulating consistency, rather than direction of lateralization, and therefore tested if T affected the ‘repeatability’ of lateral preference in consecutive behavioral trials. T treatment had no effect on the direction of lateralization, but enhanced the consistency of lateral preference in escape responses. Sex did not predict lateralization. Neither behavior was lateralized at the population-level. We therefore showed for the first time in any species an effect of egg T on consistency in lateralization. The implications of the effect of T for the evolution of trade-offs in maternal allocation of egg hormones, and the evolutionary interpretations of findings from our studies on lateralization among unmanipulated birds are discussed.     

Night-Migratory Songbirds Possess a Magnetic Compass in Both Eyes

Previous studies on European robins, Erithacus rubecula, and Australian silvereyes, Zosterops lateralis, had suggested that magnetic compass information is being processed only in the right eye and left brain hemisphere of migratory birds. However, recently it was demonstrated that both garden warblers, Sylvia borin, and European robins have a magnetic compass in both eyes. These results raise the question if the strong lateralization effect observed in earlier experiments might have arisen from artifacts or from differences in experimental conditions rather than reflecting a true all-or-none lateralization of the magnetic compass in European robins. Here we show that (1) European robins having only their left eye open can orient in their seasonally appropriate direction both during autumn and spring, i.e. there are no strong lateralization differences between the outward journey and the way home, that (2) their directional choices are based on the standard inclination compass as they are turned 180° when the inclination is reversed, and that (3) the capability to use the magnetic compass does not depend on monocular learning or intraocular transfer as it is already present in the first tests of the birds with only one eye open.     

Lateralization in response to social stimuli in a cooperatively breeding cichlid fish

Cerebral lateralization, an evolutionarily ancient and widespread phenomenon among vertebrates, is thought to bestow cognitive advantages. The advantages of lateralization at the individual-level do not necessarily require that the entire population share the same pattern of lateralization. In fact, directional bias in lateralization may lead to behavioural predictability and enhanced predator success or prey evasion. Recent theory has suggested that population-level lateralization may be favored if individuals are better able to perform coordinated behaviours, providing a distinct advantage in cooperative contexts. Here we test whether the highly social, cooperatively breeding cichlid fish Neolamprologus pulcher shows lateralized responses to a social stimulus. We found population-level biases in males; on average male N. pulcher use their right eye/left hemisphere to view their mirror image. Individual females had a preferred hemisphere, but these preferences appeared not to be directionally aligned among females. We discuss these results in the context of coordinated social behaviour and suggest future research directions.     

额叶EEG偏侧化预测情绪灵活性

随着社会竞争的日益加剧,人们在生活、学习、工作中都可能遇到各种与情绪有关的事件,如何根据情境的要求和个人的需要对情绪进行灵活性的反应,对每个人而言都至关重要.情绪灵活性的研究已成为情绪心理学、临床心理学、健康心理学等多个领域热衷讨论的课题.研究发现,左侧和右侧前额叶皮层半球不同程度地涉及加工和调节对情绪刺激的情绪反应,因此,额叶脑电图(EEG)偏侧化与情绪灵活性存在密切关系.但是,额叶EEG偏侧化是否是情绪灵活性的一个客观指标,以及额叶EEG偏侧化怎样预测情绪灵活性,至今仍不清楚.本研究测量了通过情绪电影范式诱发被试产生高兴、悲伤、愤怒、恐惧、厌恶等情绪过程中的额叶EEG活动.结果显示,情绪灵活性的激活模式反映的是情绪的动机维度,而不是情绪的效价维度.在静息状态下,对于与接近动机相关的情绪,额叶EEG左侧化的个体的左侧化程度增加;对于与回避动机相关的情绪,其左侧化程度降低.与之相对,静息状态额叶EEG右侧化的个体,无论对于与趋近动机相关的情绪还是与回避动机相关的情绪,额叶EEG偏侧化的程度没有发生改变.研究表明,额叶EEG偏侧化模式能够预测情绪灵活性,额叶EEG左侧化的个体有更灵活的情绪反应,额叶EEG右侧化的个体则有相对不灵活的情绪反应.     

Embryonic exposure to predator odour modulates visual lateralization in cuttlefish

Predation pressure acts on the behaviour and morphology of prey species. In fish, the degree of lateralization varies between high- and low-predation populations. While lateralization appears to be widespread in invertebrates, we do not know whether heredity and early experience interact during development as in vertebrates. Here we show, for the first time, that an exposure to predator odour prior to hatching modulates visual lateralization in newly hatched cuttlefish. Only cuttlefish that have been exposed to predator odour display a left-turning bias when tested with blank seawater in a T-shaped apparatus. Exposure to predator odour all the incubation long could appear as an acute predictor of a high-predation surrounding environment. In addition, cuttlefish of all groups display a left-turning preference when tested with predator odour in the apparatus. This suggests the ability of cuttlefish to innately recognize predator odour. To our knowledge, this is the first clear demonstration that lateralization is vulnerable to ecological challenges encountered during embryonic life, and that environmental stimulation of the embryo through the olfactory system could influence the development of subsequent visual lateralization.     

The evolution of brain lateralization: a game-theoretical analysis of population structure

In recent years, it has become apparent that behavioural and brain lateralization at the population level is the rule rather than the exception among vertebrates. The study of these phenomena has so far been the province of neurology and neuropsychology. Here, we show how such research can be integrated with evolutionary biology to understand lateralization more fully. In particular, we address the fact that, within a species, left- and right-type individuals often occur in proportions different from one-half (e.g. hand use in humans). The traditional explanations offered for lateralization of brain function (that it may avoid unnecessary duplication of neural circuitry and reduce interference between functions) cannot account for this fact, because increased individual efficiency is unrelated to the alignment of lateralization at the population level. A further puzzle is that such an alignment may even be disadvantageous, as it makes individual behaviour more predictable to other organisms. Here, we show that alignment of the direction of behavioural asymmetries in a population can arise as an evolutionarily stable strategy when individual asymmetrical organisms must coordinate their behaviour with that of other asymmetrical organisms. Brain and behavioural lateralization, as we know it in humans and other vertebrates, may have evolved under basically 'social' selection pressures.     

Behavioural asymmetry affects escape performance in a teleost fish

Escape performance is fundamental for survival in fish and most other animals. While previous work has shown that both intrinsic (e.g. size, shape) and extrinsic (e.g. temperature, hypoxia) factors can affect escape performance, the possibility that behavioural asymmetry may affect timing and locomotor performance in startled fish is largely unexplored. Numerous studies have found a relationship between brain lateralization and performance in several cognitive tasks. Here, we tested the hypothesis that behavioural lateralization may affect escape performance in a teleost, the shiner perch Cymatogaster aggregata. Escape responses were elicited by mechanical stimulation and recorded using high-speed video (250 Hz). A number of performance variables were analysed, including directionality, escape latency, turning rate and distance travelled within a fixed time. A lateralization index was obtained by testing the turning preference of each subject in a detour test. While lateralization had no effect on escape directionality, strongly lateralized fish showed higher escape reactivity, i.e. shorter latencies, which were associated with higher turning rates and longer distances travelled. Therefore, lateralization is likely to result in superior ability to escape from predator attacks, since previous work has shown that escape timing, turning rate and distance travelled are among the main determinants of escape success.     

Lateralization in Escape Behaviour at Different Hierarchical Levels in a Gecko: Tarentola angustimentalis from Eastern Canary Islands

At the individual level, to be behaviourally lateralized avoids costly duplication of neural circuitry and decreases possible contradictory order from the two brain hemispheres. However, being prey behaviour lateralized at higher hierarchical levels could generate different negative implications, especially if predators are able to make predictions after multiple encounters. These conflicting pressures, namely between the advantages for individuals and the disadvantages for populations could be concealed if higher-level lateralization would arise from the combination of lateralized behaviours of individuals which are mutually dependent. Here, we investigated the lateralization patterns in the escape behaviour of the gecko Tarentola angustimentalis undergoing a predatory attack simulation in a “T” maze experiment. Results showed that gecko populations displayed different degrees of lateralization, with an overall dominance of right-biased individuals. This trend is similar to that observed in the Podarcis wall lizards, which share predators with Tarentola. In addition, different morphological parameters plausible to affect refuge selection were explored in order to link directional asymmetries at morphological level with lateralization during refuge selection.     

Lateralization in the invertebrate brain: left-right asymmetry of olfaction in bumble bee, Bombus terrestris

Brain and behavioural lateralization at the population level has been recently hypothesized to have evolved under social selective pressures as a strategy to optimize coordination among asymmetrical individuals. Evidence for this hypothesis have been collected in Hymenoptera: eusocial honey bees showed olfactory lateralization at the population level, whereas solitary mason bees only showed individual-level olfactory lateralization. Here we investigated lateralization of odour detection and learning in the bumble bee, Bombus terrestris L., an annual eusocial species of Hymenoptera. By training bumble bees on the proboscis extension reflex paradigm with only one antenna in use, we provided the very first evidence of asymmetrical performance favouring the right antenna in responding to learned odours in this species. Electroantennographic responses did not reveal significant antennal asymmetries in odour detection, whereas morphological counting of olfactory sensilla showed a predominance in the number of olfactory sensilla trichodea type A in the right antenna. The occurrence of a population level asymmetry in olfactory learning of bumble bee provides new information on the relationship between social behaviour and the evolution of population-level asymmetries in animals.     

Glycosyltransferases in Different Brain Regions During Chick Embryo Development

Glycosphingolipids, in particular gangliosides, play a crucial role in neuronal development and are known to change dramatically in total content and distribution in different brain areas during embryogenesis. In the present work we analyzed the activity of enzymes involved in the metabolism of gangliosides, at different periods of functional maturation in different regions of chick embryo brain. Our data demonstrate differences in the enzymatic activities in the examined areas; these differences might be correlated with the functional lateralization occurring in the brain during development. Significative differences were found in glycosphingolipid composition between controlateral cerebral hemispheres and optic lobes; these results together with previous data we found, contribute to reinforce our hypothesis on the occurrence of biochemical lateralization during early brain development.     

Sex differences in the cerebral lateralization of a cichlid fish when detouring to view emotionally conditioned stimuli

The lateralization of emotion has been described in a variety of animals. The right hemisphere has been implicated in the processing of negative emotions while positive emotions are processed in the left. Most animal studies of this phenomenon to date have used intrinsically emotionally arousing stimuli and there are few examples of lateralized responses to learned emotional triggers. It is known that males and females may demonstrate different patterns of lateralization, and that these sex differences may interact with other variables. We investigated the lateralized response of male and female convict cichlids to emotionally conditioned stimuli. One stimulus was given an appetitive (positive emotional valence) association by pairing with food. The other stimulus was given an aversive (negative emotional valence) association by pairing with a chemical alarm signal. We found that males tend to be more strongly lateralized to aversive stimuli while females are more strongly lateralized when responding to appetitive stimuli.     

Lateralization of Aggression during Reproduction in Male Siamese Fighting Fish

A preference for the left‐eye use during aggressive interactions has been widely reported in the literature, even though in some cases the direction of lateralization varies among individuals within populations. Laterality of aggression in male Siamese fighting fish has been described in a number of studies, yet very little is known about lateralization of aggression during reproduction and/or parental care in fish. Here, we aimed to investigate the relationship between the different reproductive phases and lateralization in eye use during aggressive interactions in males of Siamese fighting fish. Lateralization in eye use is influenced during the early reproductive state, before and after the bubble nest construction stages. We found that nest‐holding males preferentially used the right eye before and after bubble nest construction independent of the sex of the intruder. During the later reproductive phases, aggressiveness increased whereby the direction of lateralization rather than the degree was influenced supporting the hypothesis that reproductive state influences behavioral consistency in Siamese fighting fish.