Laterality enhances cognition in Australian parrots

Cerebral lateralization refers to the division of information processing in either hemisphere of the brain and is a ubiquitous trait among vertebrates and invertebrates. Given its widespread occurrence, it is likely that cerebral lateralization confers a fitness advantage. It has been hypothesized that this advantage takes the form of enhanced cognitive function, potentially via a dual processing mechanism whereby each hemisphere can be used to process specific types of information without contralateral interference. Here, we examined the influence of lateralization on problem solving by Australian parrots. The first task, a pebble-seed discrimination test, was designed for small parrot species that feed predominately on small seeds, which do not require any significant manipulation with the foot prior to ingestion. The second task, a string-pull problem, was designed for larger bodied species that regularly use their feet to manipulate food objects. In both cases, strongly lateralized individuals (those showing significant foot and eye biases) outperformed less strongly lateralized individuals, and this relationship was substantially stronger in the more demanding task. These results suggest that cerebral lateralization is a ubiquitous trait among Australian parrots and conveys a significant foraging advantage. Our results provide strong support for the enhanced cognitive function hypothesis.     

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.     

Lateralization in the predatory behaviour of the common wall lizard (Podarcis muralis)

Ectotherms have been shown being lateralized as well as mammals and birds. This is particularly evident in visual lateralization, i.e. the different use of the eyes, leading to use a specific eye to observe specific kind of stimuli and to process them with the correspondent contralateral hemisphere. Several lower vertebrates are facilitated in this from the lateral position of the eyes, enabling them to carry out more tasks simultaneously, controlled by different eyes and relative hemispheres. Predatory responses seem usually mediated by the right eye/left hemisphere in fishes, amphibians and some sauropsids, but there are no strong evidences of this in lizards. Eighteen wild males of the Common wall lizard Podarcis muralis were tested individually in captivity to ascertain whether they are lateralized to look at prey with a specific eye. The lizards were gently induced entering a 30-cm long central arm of a T-maze which led to a 44.5-cm long arm cross-arm at whose extremities there were two identical prey, Tenebrio molitor larvae, familiar to the lizards. We recorded what direction the lizards chose to reach the prey and the frequency and duration of head turning, indicative of looking either prey with the left or the right eye. We found that individuals show being lateralized at individual level. The preferred direction taken to reach the prey is the right for the majority of those (4 of 5) showing an evident preference, indicating also a possible form of laterality at population level. In addition, lizards maintained the same head side of the direction taken turned for more time towards the prey than the opposite head side, revealing an eye preference for observing this kind of cue. Our study demonstrates how males of Podarcis muralis have a visual lateralization to capture prey. Furthermore, it is another support to the hypothesis of vertebrate lateralization derivation from a common ancestor.     

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.     

Reverse lateralization of visual discriminative abilities in the European starling

Previous experiments on visual feature discrimination abilities have consistently shown a right-eye system lateralization in pigeons, Columba livia, and young domestic chickens, Gallus gallus domesticus, both nonpasserine species. Recently, however, it has been shown that photoreceptor distribution in the left and right retinas are asymmetrical in the European starling, Sturnus vulgaris, a passerine species. Single cone receptors are significantly more abundant in the left retina, which suggests that starlings should perform visual discrimination tasks more proficiently with the left eye, in contrast to previous findings with nonpasserines. We tested this hypothesis using the technique of monocular occlusion. In the first experiment, starlings were tested on a simultaneous visual discrimination task in three conditions: binocular (both eyes), left monocular (left eye only) and right monocular (right eye only). Subjects in the binocular and left-monocular conditions achieved significantly higher performance scores on the discrimination task than birds in the right-monocular condition. A second experiment found similar results, with birds in the left-monocular condition learning the discrimination task more than twice as quickly as those in the right-monocular condition. Subsequent tests with the alternative eye for both groups indicated no interocular transfer. These findings suggest that visual discriminative abilities in starlings are asymmetrical, and that they are lateralized in the opposite eye system than has been reported for all other species tested to date.     

Visual laterality of calf-mother interactions in wild whales

Background

Behavioral laterality is known for a variety of vertebrate and invertebrate animals. Laterality in social interactions has been described for a wide range of species including humans. Although evidence and theoretical predictions indicate that in social species the degree of population level laterality is greater than in solitary ones, the origin of these unilateral biases is not fully understood. It is especially poorly studied in the wild animals. Little is known about the role, which laterality in social interactions plays in natural populations. A number of brain characteristics make cetaceans most suitable for investigation of lateralization in social contacts.

Methodology/Principal Findings

Observations were made on wild beluga whales (Delphinapterus leucas) in the greatest breeding aggregation in the White Sea. Here we show that young calves (in 29 individually identified and in over a hundred of individually not recognized mother-calf pairs) swim and rest significantly longer on a mother''s right side. Further observations along with the data from other cetaceans indicate that found laterality is a result of the calves'' preference to observe their mothers with the left eye, i.e., to analyze the information on a socially significant object in the right brain hemisphere.

Conclusions/Significance

Data from our and previous work on cetacean laterality suggest that basic brain lateralizations are expressed in the same way in cetaceans and other vertebrates. While the information on social partners and novel objects is analyzed in the right brain hemisphere, the control of feeding behavior is performed by the left brain hemisphere. Continuous unilateral visual contacts of calves to mothers with the left eye may influence social development of the young by activation of the contralateral (right) brain hemisphere, indicating a possible mechanism on how behavioral lateralization may influence species life and welfare. This hypothesis is supported by evidence from other vertebrates.     

The effects of adaptation to urea on feeding rates and growth in Drosophila larvae

A collection of forty populations were used to study the phenotypic adaptation of Drosophila melanogaster larvae to urea‐laced food. A long‐term goal of this research is to map genes responsible for these phenotypes. This mapping requires large numbers of populations. Thus, we studied fifteen populations subjected to direct selection for urea tolerance and five controls. In addition, we studied another twenty populations which had not been exposed to urea but were subjected to stress or demographic selection. In this study, we describe the differentiation in these population for six phenotypes: (1) larval feeding rates, (2) larval viability in urea‐laced food, (3) larval development time in urea‐laced food, (4) adult starvation times, (5) adult desiccation times, and (6) larval growth rates. No significant differences were observed for desiccation resistance. The demographically/stress‐selected populations had longer times to starvation than urea‐selected populations. The urea‐adapted populations showed elevated survival and reduced development time in urea‐laced food relative to the control and nonadapted populations. The urea‐adapted populations also showed reduced larval feeding rates relative to controls. We show that there is a strong linear relationship between feeding rates and growth rates at the same larval ages feeding rates were measured. This suggests that feeding rates are correlated with food intake and growth. This relationship between larval feeding rates, food consumption, and efficiency has been postulated to involve important trade‐offs that govern larval evolution in stressful environments. Our results support the idea that energy allocation is a central organizing theme in adaptive evolution.     

Limb use and preferences in wild orang-utans during feeding and locomotor behavior

Limited data are available on hemispheric lateralization in wild orang-utans. There has been only one previous investigation of limb preferences in wild orang-utans [Yeager, 1991]. We examined the lateralization of limb use in wild Bornean orang-utans (Pongo pygmaeus pygmaeus) with the aim of providing more insight into possible hemispheric specialization in wild nonhuman primates. Here, we report in detail on limb use and preference during arboreal locomotion between trees (N=6) and on feeding involving one limb (N=8) and two limbs (N=6). We distinguished between locomotion between overlapping trees (Type I) and locomotion involving gap crossing (Types II and III). For locomotion Type I, the six orang-utans showed no leading hand preference, however for locomotion Types II and III, all six showed significant right-hand preferences. All eight orang-utans showed individual hand preferences for reaching for food, but no significant group bias was found. Limb preferences for feeding involving two limbs (hand-hand or hand-foot) differed between juveniles (right hand-right foot), adult females (left hand-right hand) and adult males (right hand-left hand). Although not present for all tasks, the results indicate that orang-utans do show evidence of hemispheric specialization, but the use of the hands is not under a strong lateralized hemispheric control and is adaptable.     

Visual lateralization in wild striped dolphins (Stenella coeruleoalba) in response to stimuli with different degrees of familiarity

Background

Apart from findings on both functional and motor asymmetries in captive aquatic mammals, only few studies have focused on lateralized behaviour of these species in the wild.

Methodology/Principal Findings

In this study we focused on lateralized visual behaviour by presenting wild striped dolphins with objects of different degrees of familiarity (fish, ball, toy). Surveys were conducted in the Gulf of Taranto, the northern Ionian Sea portion delimited by the Italian regions of Calabria, Basilicata and Apulia. After sighting striped dolphins from a research vessel, different stimuli were presented in a random order by a telescopic bar connected to the prow of the boat. The preferential use of the right/left monocular viewing during inspection of the stimuli was analysed.

Conclusion

Results clearly showed a monocular viewing preference with respect to the type of the stimulus employed. Due to the complete decussation of the optical nerves in dolphin brain our results reflected a different specialization of brain hemispheres for visual scanning processes confirming that in this species different stimuli evoked different patterns of eye use. A preferential use of the right eye (left hemisphere) during visual inspection of unfamiliar targets was observed supporting the hypothesis that, in dolphins, the organization of the functional neural structures which reflected cerebral asymmetries for visual object recognition could have been subjected to a deviation from the evolutionary line of most terrestrial vertebrates.     

Individual variation in feeding morphology,not diet,can facilitate the success of generalist species in urban ecosystems

Generalist species dominate urban ecosystems. The success of urban generalists is often related to a plastic diet and feeding traits that allow them to take advantage of a variety of food resources provided by humans in cities. The classification of a species as a generalist is commonly based on mean estimates of diet‐ and feeding‐related traits. However, there is increasing evidence that a generalist population can consist of individual specialists. In such cases, estimates based on mean can hide important individual variation that can explain trophic ecology and the success of urban dwellers. Here, we focus on guppies, Poecilia reticulata, a widespread alien fish species which has invaded both urban and non‐urban systems, to explore the effect of urbanization on individual diet and feeding morphology (cranium shape). Our results show that guppies in urban and non‐urban populations are not individual specialists, having a similar generalist diet despite the high population density. However, there is important individual variation in cranium shape which allow urban guppies to feed more efficiently on highly nutritious food. Our data suggest that individual variation in feeding efficiency can be a critical overlooked trait that facilitates the success of urban generalists.     

In the eye of the beholder: visual mate choice lateralization in a polymorphic songbird

Birds choose mates on the basis of colour, song and body size, but little is known about the mechanisms underlying these mating decisions. Reports that zebra finches prefer to view mates with the right eye during courtship, and that immediate early gene expression associated with courtship behaviour is lateralized in their left hemisphere suggest that visual mate choice itself may be lateralized. To test this hypothesis, we used the Gouldian finch, a polymorphic species in which individuals exhibit strong, adaptive visual preferences for mates of their own head colour. Black males were tested in a mate-choice apparatus under three eye conditions: left-monocular, right-monocular and binocular. We found that black male preference for black females is so strongly lateralized in the right-eye/left-hemisphere system that if the right eye is unavailable, males are unable to respond preferentially, not only to males and females of the same morph, but also to the strikingly dissimilar female morphs. Courtship singing is consistent with these lateralized mate preferences; more black males sing to black females when using their right eye than when using their left. Beauty, therefore, is in the right eye of the beholder for these songbirds, providing, to our knowledge, the first demonstration of visual mate choice lateralization.     

Relating Lateralization of Eye Use to Body Motion in the Avoidance Behavior of the Chameleon (Chamaeleo chameleon)

Lateralization is mostly analyzed for single traits, but seldom for two or more traits while performing a given task (e.g. object manipulation). We examined lateralization in eye use and in body motion that co-occur during avoidance behaviour of the common chameleon, Chamaeleo chameleon. A chameleon facing a moving threat smoothly repositions its body on the side of its perch distal to the threat, to minimize its visual exposure. We previously demonstrated that during the response (i) eye use and body motion were, each, lateralized at the tested group level (N = 26), (ii) in body motion, we observed two similar-sized sub-groups, one exhibiting a greater reduction in body exposure to threat approaching from the left and one – to threat approaching from the right (left- and right-biased subgroups), (iii) the left-biased sub-group exhibited weak lateralization of body exposure under binocular threat viewing and none under monocular viewing while the right-biased sub-group exhibited strong lateralization under both monocular and binocular threat viewing. In avoidance, how is eye use related to body motion at the entire group and at the sub-group levels? We demonstrate that (i) in the left-biased sub-group, eye use is not lateralized, (ii) in the right-biased sub-group, eye use is lateralized under binocular, but not monocular viewing of the threat, (iii) the dominance of the right-biased sub-group determines the lateralization of the entire group tested. We conclude that in chameleons, patterns of lateralization of visual function and body motion are inter-related at a subtle level. Presently, the patterns cannot be compared with humans'' or related to the unique visual system of chameleons, with highly independent eye movements, complete optic nerve decussation and relatively few inter-hemispheric commissures. We present a model to explain the possible inter-hemispheric differences in dominance in chameleons'' visual control of body motion during avoidance.     

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.     

Asymmetry pays: visual lateralization improves discrimination success in pigeons

Functional cerebral asymmetries, once thought to be exclusively human, are now accepted to be a widespread principle of brain organization in vertebrates [1]. The prevalence of lateralization makes it likely that it has some major advantage. Until now, however, conclusive evidence has been lacking. To analyze the relation between the extent of cerebral asymmetry and the degree of performance in visual foraging, we studied grain-grit discrimination success in pigeons, a species with a left hemisphere dominance for visual object processing [2,3]. The birds performed the task under left-eye, right-eye or binocular seeing conditions. In most animals, right-eye seeing was superior to left-eye seeing performance, and binocular performance was higher than each monocular level. The absolute difference between left- and right-eye levels was defined as a measure for the degree of visual asymmetry. Animals with higher asymmetries were more successful in discriminating grain from grit under binocular conditions. This shows that an increase in visual asymmetry enhances success in visually guided foraging. Possibly, asymmetries of the pigeon's visual system increase the computational speed of object recognition processes by concentrating them into one hemisphere while preventing the other side of the brain from initiating conflicting search sequences of its own.     

Breaking the balance: ocular BDNF-injections induce visual asymmetry in pigeons

In pigeons, asymmetric photic stimulation around hatch induces functional visual asymmetries that are accompanied by left-right differences in tectal cell sizes. Different aspects of light-dependent neuronal differentiation are known to be mediated by the brain-derived neurotrophic factor (BDNF). Therefore, we investigated by means of single or triple BDNF- or saline-injections into the right eye of dark-incubated pigeon hatchlings if ocular BDNF enrichment mimics the effects of biased visual input. As adults, the birds were tested in a grit-grain discrimination task to estimate the degree and direction of visual lateralization followed by a morphometric analysis of retinal and tectal cells. The grit-grain discrimination task demonstrated that triple BDNF-injections enhanced visuoperceptual and visuomotor functioning of the left eye system. Morphometric analysis showed bilateral cell-type dependent effects within the optic tectum. While single-BDNF injections increased cell body sizes of calbindin-positive efferent neurons, triple-injections decreased cell sizes of parvalbumin-positive cells. Moreover, single BDNF-injections increased retinal cell sizes within the contralateral eye. Analysis of BDNF-induced intracellular signaling demonstrated enhanced downstream Ras activation for at least 24 h within both tectal halves whereas activity changes within the contralateral retina could not be detected. This points to primarily tectal effects of ocular BDNF. In sum, exogenous BDNF modulates the differentiation of retinotectal circuitries and dose-dependently shifts lateralized visuomotor processing towards the noninjected side. Since these effects are opposite to embryonic light stimulation, it is unlikely that the impact of light onto asymmetry formation is mediated by retinal BDNF.     

The costs of hemispheric specialization in a fish

Laboratory and field studies have documented better cognitive performance associated with marked hemispheric specialization in organisms as diverse as chimpanzees, domestic chicks and topminnows. While providing an evolutionary explanation for the emergence of cerebral lateralization, this evidence represents a paradox because a large proportion of non-lateralized (NL) individuals is commonly observed in animal populations. Hemispheric specialization often determines large left–right differences in perceiving and responding to stimuli. Using topminnows selected for a high or low degree of lateralization, we tested the hypothesis that individuals with greater functional asymmetry pay a higher performance cost in situations requiring matching information from the two eyes. When trained to use the middle door in a row of a nine, NL fish correctly chose the central door in most cases, while lateralized fish showed systematic leftward or rightward biases. When choosing between two shoals, each seen with a different eye, NL fish chose the high-quality shoal significantly more often than the lateralized fish, whose performance was affected by eye preference for analysing social stimuli. These findings suggest the existence of a trade-off between computational advantages of hemispheric specialization and the ecological cost of making suboptimal decisions whenever relevant information is located on both sides of the body.     

Development of lateralization of the magnetic compass in a migratory bird

The magnetic compass of a migratory bird, the European robin (Erithacus rubecula), was shown to be lateralized in favour of the right eye/left brain hemisphere. However, this seems to be a property of the avian magnetic compass that is not present from the beginning, but develops only as the birds grow older. During first migration in autumn, juvenile robins can orient by their magnetic compass with their right as well as with their left eye. In the following spring, however, the magnetic compass is already lateralized, but this lateralization is still flexible: it could be removed by covering the right eye for 6 h. During the following autumn migration, the lateralization becomes more strongly fixed, with a 6 h occlusion of the right eye no longer having an effect. This change from a bilateral to a lateralized magnetic compass appears to be a maturation process, the first such case known so far in birds. Because both eyes mediate identical information about the geomagnetic field, brain asymmetry for the magnetic compass could increase efficiency by setting the other hemisphere free for other processes.     

Individual variation in winter supplementary food consumption and its consequences for reproduction in wild birds

The provision of wild birds with supplementary food has increased substantially over recent decades. While it is assumed that provisioning birds is beneficial, supplementary feeding can have detrimental ‘carry‐over’ effects on reproductive traits. Due to difficulties in monitoring individual feeding behaviour, assessing how individuals within a population vary in their exploitation of supplementary food resources has been limited. Quantifying individual consumption of supplementary food is necessary to understand the operation of carry‐over effects at the individual level. We used Radio Frequency Identification (RFID) technology and automated feeders to estimate individual consumption of supplementary winter food in a large wild population of great tits Parus major and blue tits Cyanistes caeruleus. Using these data, we identified demographic factors that explained individual variation in levels of supplementary food consumption. We also tested for carry‐over effects of supplementary food consumption on recruitment, reproductive success and a measure of survival. Individual variation in consumption of supplementary food was explained by differences between species, ages, sexes and years. Individuals were consistent across time in their usage of supplementary resources. We found no strong evidence that the extent of supplementary food consumption directly influenced subsequent fitness parameters. Such effects may instead result from supplementary food influencing population demographics by enhancing the survival and subsequent breeding of less competitive individuals, which reduce average breeding parameters and increase density‐dependent competition. Carry‐over effects of supplementary feeding are not universal and may depend upon the temporal availability of the food provided. Our study demonstrates how RFID systems can be used to examine individual‐level behaviour with minimal effects on fitness.     

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.