Lateralization in feeding is food type specific and impacts feeding success in wild birds

Current research suggests that hemispheric lateralization has significant fitness consequences. Foraging, as a basic survival function, is a perfect research model to test the fitness impact of lateralization. However, our understanding of lateralized feeding behavior is based predominantly on laboratory studies, while the evidence from wild animals in natural settings is limited. Here we studied visual lateralization in yellow‐footed green pigeons (Treron phoenicoptera) feeding in the wild. We aimed to test whether different types of food objects requiring different searching strategies elicit different eye/hemisphere biases. When feeding on relatively large, uniformly colored food objects (mahua flowers) which can be present or absent in the viewed patch, the majority of pigeons relied mostly on the left eye–right hemisphere. In contrast, when feeding on smaller and more abundant food objects, with color cues signaling its ripeness (sacred figs), right‐eye (left‐hemisphere) preference prevailed. Our results demonstrate that oppositely directed visual biases previously found in different experimental tasks occur in natural feeding situations in the form of lateralized viewing strategies specific for different types of food. The results suggest that pigeons rely on the hemisphere providing more advantages for the consumption of the particular type of food objects, implying the relevance of brain lateralization as a plastic adaptation to ecological demands. We assessed the success of food discrimination and consumption to examine the link between lateralization and cognitive performance. The use of the preferred eye resulted in better discrimination of food items. Discrimination accuracy and feeding efficiency were significantly higher in lateralized individuals. The results showed that visual lateralization impacted pigeons’ feeding success, implicating important fitness benefits associated with lateralization.     

Enhanced schooling performance in lateralized fishes

The occurrence of functional left-right cerebral asymmetries has been documented in a wide range of animals, suggesting that the lateralization of cognitive functions enjoys some kind of selective advantage over the bilateral control of the same functions. Here, we compared schooling performance of fishes with high or low degree of lateralization, which were obtained through selective breeding. Schools of lateralized fishes moving in a novel environment showed significantly more cohesion and coordination than schools of non-lateralized (NL) fishes. Pairs of fishes lateralized in opposite directions were as efficient as pairs of same laterality, suggesting that the performance of lateralized fishes derives from a computational advantage rather than being the consequence of a behavioural similarity among schoolmates. In schools composed of both lateralized and NL fishes, the latter were more often at the periphery of the school while lateralized fishes occupied the core, a position normally safer and energetically less expensive.     

Lateralization When Monitoring Predators in the Wild: A Left Eye Control in the Common Wall Lizard (Podarcis muralis)

Lateralization is the function specialization between left and right brain hemispheres. It is now ascertained in ectotherms too, where bias in eye use for different tasks, i.e., visual lateralization, is widespread. The lateral eye position on the head of ectotherm animals, in fact, allows them to observe left/right stimuli independently and allows lateralized individuals to carry out left and right perceived tasks at the same time. A recent study conducted on common wall lizards, Podarcis muralis, showed that lizards predominantly monitor a predator with the left eye while escaping. However, this work was conducted in a controlled laboratory setting owing to the difficulty of carrying out lateralization experiments under natural conditions. Nevertheless, field studies could provide important information to support what was previously found in the laboratory and demonstrate that these traits occur in nature. In this study, we conducted a field study on the antipredatory behavior of P. muralis lizards. We simulated predatory attacks on lizards in their natural environment. We found no lateralization in the measure of eye used by the lizard to monitor the predator before escaping from it, but the eye used was probably determined by the relative position of the lizard and the predator just before the attack. This first eye used did not affect escape decisions; lizards chose to escape toward the nearest refuge irrespective of whether it was located to the lizard’s left or right side. However, once they had escaped to a refuge, lizards had a left eye–mediated bias to monitor the predator when first emerging from the refuge, and this bias was likely independent of other environmental variables. Hence, these field findings support a left eye–mediated observation of the predator in P. muralis lizards, which confirms previous findings in this and other species.     

Prenatal light exposure affects development of behavioural lateralization in a livebearing fish

The existence of individual differences in handedness and other lateralized functions is an unresolved problem. Genetic factors account for only a small proportion of the variance but the contribution of environmental influences is still largely unexplored. In chicks and zebrafish the amount of environmental light reaching embryos during development greatly influences the lateralization of adults. To investigate whether a similar effect is present in livebearers, we measured behavioural lateralization in ten-day-old goldbelly topminnows born from females that have been maintained at high or low light intensities during pregnancy. Fish from high-light treatment were significantly lateralized in both visual and motor tests while fish exposed to low light intensities were not. As observed in chicks and zebrafish, the main consequence of light exposure was the alignment of the laterality of different individuals in the same direction. Lateralization is known to affect a number of fitness-related traits in topminnow and we suggest that light influence may be part of an adaptive mechanism allowing to adjust the developmental trajectories of offspring to the prevailing environmental conditions.     

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.     

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.     

Hemispheric Asymmetry in the Auditory Facilitation Effect in Dual-Stream Rapid Serial Visual Presentation Tasks

Even though auditory stimuli do not directly convey information related to visual stimuli, they often improve visual detection and identification performance. Auditory stimuli often alter visual perception depending on the reliability of the sensory input, with visual and auditory information reciprocally compensating for ambiguity in the other sensory domain. Perceptual processing is characterized by hemispheric asymmetry. While the left hemisphere is more involved in linguistic processing, the right hemisphere dominates spatial processing. In this context, we hypothesized that an auditory facilitation effect in the right visual field for the target identification task, and a similar effect would be observed in the left visual field for the target localization task. In the present study, we conducted target identification and localization tasks using a dual-stream rapid serial visual presentation. When two targets are embedded in a rapid serial visual presentation stream, the target detection or discrimination performance for the second target is generally lower than for the first target; this deficit is well known as attentional blink. Our results indicate that auditory stimuli improved target identification performance for the second target within the stream when visual stimuli were presented in the right, but not the left visual field. In contrast, auditory stimuli improved second target localization performance when visual stimuli were presented in the left visual field. An auditory facilitation effect was observed in perceptual processing, depending on the hemispheric specialization. Our results demonstrate a dissociation between the lateral visual hemifield in which a stimulus is projected and the kind of visual judgment that may benefit from the presentation of an auditory cue.     

Lateralized female topminnows can forage and attend to a harassing male simultaneously

Animals engaged in a complex task are often unable to allocateenough attention to a second concurrent task. We tested thehypothesis that cerebral lateralization is advantageous becauseit enables separate and parallel information processing andallows for a more efficient performance of concurrent cognitivetasks. Lateralized and nonlateralized (NL) female Girardinusfalcatus, obtained through a selective breeding experiment,were compared in a situation requiring sharing attention betweentwo simultaneous tasks, retrieving food items scattered on thesurface, and avoiding unsolicited male mating attempts. In thepresence of a sexually harassing male, lateralized females weresignificantly more efficient than NL females in retrieving food,while no difference between these groups was found in controlexperiments in which the male was absent and subjects were notrequired to share attention between foraging and vigilance.Lateralized females showed a negligible decrease in foragingrate while attending the additional task, suggesting that theymay be able to partition the two processes in different partsof the brain.     

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.     

Hemispheric Specialization Varies with EEG Brain Resting States and Phase of Menstrual Cycle

A growing body of behavioral studies has demonstrated that women’s hemispheric specialization varies as a function of their menstrual cycle, with hemispheric specialization enhanced during their menstruation period. Our recent high-density electroencephalogram (EEG) study with lateralized emotional versus neutral words extended these behavioral results by showing that hemispheric specialization in men, but not in women under birth-control, depends upon specific EEG resting brain states at stimulus arrival, suggesting that hemispheric specialization may be pre-determined at the moment of the stimulus onset. To investigate whether EEG brain resting state for hemispheric specialization could vary as a function of the menstrual phase, we tested 12 right-handed healthy women over different phases of their menstrual cycle combining high-density EEG recordings and the same lateralized lexical decision paradigm with emotional versus neutral words. Results showed the presence of specific EEG resting brain states, associated with hemispheric specialization for emotional words, at the moment of the stimulus onset during the menstruation period only. These results suggest that the pre-stimulus EEG pattern influencing hemispheric specialization is modulated by the hormonal state.     

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.     

Lateralized visual behavior in bottlenose dolphins (Tursiops truncatus) performing audio-visual tasks: the right visual field advantage

Analyzing cerebral asymmetries in various species helps in understanding brain organization. The left and right sides of the brain (lateralization) are involved in different cognitive and sensory functions. This study focuses on dolphin visual lateralization as expressed by spontaneous eye preference when performing a complex cognitive task; we examine lateralization when processing different visual stimuli displayed on an underwater touch-screen (two-dimensional figures, three-dimensional figures and dolphin/human video sequences). Three female bottlenose dolphins (Tursiops truncatus) were submitted to a 2-, 3- or 4-, choice visual/auditory discrimination problem, without any food reward: the subjects had to correctly match visual and acoustic stimuli together. In order to visualize and to touch the underwater target, the dolphins had to come close to the touch-screen and to position themselves using monocular vision (left or right eye) and/or binocular naso-ventral vision. The results showed an ability to associate simple visual forms and auditory information using an underwater touch-screen. Moreover, the subjects showed a spontaneous tendency to use monocular vision. Contrary to previous findings, our results did not clearly demonstrate right eye preference in spontaneous choice. However, the individuals' scores of correct answers were correlated with right eye vision, demonstrating the advantage of this visual field in visual information processing and suggesting a left hemispheric dominance. We also demonstrated that the nature of the presented visual stimulus does not seem to have any influence on the animals' monocular vision choice.     

Rethinking Motor Lateralization: Specialized but Complementary Mechanisms for Motor Control of Each Arm

Motor lateralization in humans has primarily been characterized as “handedness”, resulting in the view that one arm-hemisphere system is specialized for all aspects of movement while the other is simply a weaker analogue. We have proposed an alternative view that motor lateralization reflects proficiency of each arm for complementary functions that arises from a specialization of each hemisphere for distinct movement control mechanisms. However, before this idea of hemispheric specialization can be accepted, it is necessary to precisely identify these distinct, lateralized mechanisms. Here we show in right-handers that dominant arm movements rely on predictive mechanisms that anticipate and account for the dynamic properties of the arm, while the non-dominant arm optimizes positional stability by specifying impedance around equilibrium positions. In a targeted-reaching paradigm, we covertly and occasionally shifted the hand starting location either orthogonal to or collinear with a particular direction of movement. On trials on which the start positions were shifted orthogonally, we did not notice any strong interlimb differences. However, on trials on which start positions were shifted orthogonally, the dominant arm largely maintained the direction and straightness of its trajectory, while the non-dominant arm deviated towards the previously learned goal position, consistent with the hypothesized control specialization of each arm-hemisphere system. These results bring together two competing theories about mechanisms of movement control, and suggest that they coexist in the brain in different hemispheres. These findings also question the traditional view of handedness, because specialized mechanisms for each arm-hemisphere system were identified within a group of right-handers. It is likely that such hemispheric specialization emerged to accommodate increasing motor complexity during evolution.     

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.     

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.     

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.     

Hemispheric specialization for global and local processing: the effect of stimulus category.

Neuropsychological evidence indicates that the global aspect of complex visual scenes is preferentially processed by the right hemisphere, and local aspects are preferentially processed by the left hemisphere. Using letter-based hierarchical stimuli (Navon figures), we recently demonstrated, in a directed-attention task, lateralized neural activity (assessed by positron emission tomography) in the left prestriate cortex during local processing, and in the right prestriate cortex during global processing. Furthermore, temporal-parietal cortex was critically activated bilaterally in a divided-attention task that involved varying the number of target switches between local and global levels of letter-based hierarchical stimuli. Little is known about whether such stimulus categories influence such hemispheric lateralization. We now present data on brain activity, derived from positron emission tomography, in normal subjects scanned during either local or global processing of object-based hierarchical stimuli. We again observe attentional modulation of neural activity in prestriate cortex. There is now greater right-sided activation for local processing and greater left-sided activation for global processing, which is the opposite of that seen with letter-based stimuli. The results suggest that the relative differential hemispheric activations in the prestriate areas during global and local processing are modified by stimulus category.     

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.     

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.     

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.