Lateralisation of visual function in yellow-eyed mullet (Aldrichetta forsteri) and its role in schooling behaviour

Lateralisation of cognitive function is a common phenomenon found throughout the animal kingdom. In fish, lateralisation is involved in visually mediated behaviours such as schooling, predator avoidance and foraging. This study sought to quantify visual laterality in yellow-eyed mullet (Aldrichetta forsteri), to determine visual asymmetries and the significance of lateralisation, and the factors which influence functional behaviours in schooling fish. Tank-based experiments investigated individual and population level lateralisation, schooling behaviour, and optic lobe asymmetry. Variation in direction and strength of lateralisation in individuals was found in juveniles, but at a population level significant bias was found in adults. Right eye biased fish had a larger right optic lobe than control fish. Strongly lateralised fish showed a tendency to occupy positions of safety within the school more frequently than control fish. In combination with observed differences in schooling behaviour, the possibility of ontogenetic plasticity in behavioural lateralisation and optic lobe morphology is suggested.     

Spatial attention and neglect: parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events.

The syndrome of contralesional neglect reflects a lateralized disruption of spatial attention. In the human, the left hemisphere shifts attention predominantly in the contralateral hemispace and in a contraversive direction whereas the right hemisphere distributes attention more evenly, in both hemispaces and both directions. As a consequence of this asymmetry, severe contralesional neglect occurs almost exclusively after right hemisphere lesions. Patients with left neglect experience a loss of salience in the mental representation and conscious perception of the left side and display a reluctance to direct orientating and exploratory behaviours to the left. Neglect is distributed according to egocentric, allocentric, world-centred, and object-centred frames of reference. Neglected events can continue to exert an implicit influence on behaviour, indicating that the attentional filtering occurs at the level of an internalized representation rather than at the level of peripheral sensory input. The unilateral neglect syndrome is caused by a dysfunction of a large-scale neurocognitive network, the cortical epicentres of which are located in posterior parietal cortex, the frontal eye fields, and the cingulate gyrus. This network coordinates all aspects of spatial attention, regardless of the modality of input or output. It helps to compile a mental representation of extrapersonal events in terms of their motivational salience, and to generate 'kinetic strategies' so that the attentional focus can shift from one target to another.     

Complementary left and right eye use during predator inspection and shoal-mate scrutiny in minnows

Minnows Phoxinus phoxinus did not show any difference in the average distance from a predator associated with the left or right position of a shoal-mate. While inspection behaviour of fish tested with a mirror on their left side was indistinguishable from the behaviour of controls tested without a mirror, inspection behaviour of fish tested with the mirror on their right side appeared to be changed and incoherent in both temporal and spatial parameters. These results suggest that, as in mosquitofish Gambusia holbrooki , the condition with the mirror on the left provided the best arrangement of monocular lateral stimulation in which each stimulus fell into the correct lateral visual field. Minnows showed a significant left eye preference during scrutiny of their mirror image when tested in the absence of any predator and a significant right eye preference while monitoring a live predator in the absence of a social partner.     

Social recognition and approach in the chick: lateralization and effect of visual experience

Chicks, Gallus gallus domesticus, tested monocularly on day 3 after hatching recognize familiar versus unfamiliar conspecifics and choose to approach one or other when they use the left eye, whereas they approach familiar and unfamiliar chicks at random when they use the right eye. In experiment 1 we investigated the effects of light exposure of embryos prior to hatching on this particular form of lateralization. Irrespective of whether they hatched from eggs incubated in the dark or from eggs exposed to light during the final days of incubation, chicks using the left eye had higher choice scores (meaning they chose to approach either a familiar or an unfamiliar chick) than chicks using the right eye or both eyes. Therefore, light experience prior to hatching did not influence the lateralization of individual recognition or choice behaviour, although it did affect latency to move out of, and time spent in, the centre of the runway. Experiment 2 showed that visual/social experience posthatching influences choice behaviour: chicks housed in a group in the light for 12 h on day 1 posthatching made a clear choice between familiar and unfamiliar chicks when tested on day 3, but chicks kept in a group in the dark on day 1 did not make a choice, instead alternating between the two stimuli. In experiment 3 we found that posthatching visual/social experience increased the choice scores of chicks using the right eye and thereby removed any lateralization of choice behaviour. The results suggest that visual experience of a social group is required before chicks using their right eye (and left hemisphere) will pay attention to the cues that distinguish one chick from another. Chicks using their left eye (and right hemisphere) recognize the difference between individuals without requiring visual experience with other chicks. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Light intensity and schooling behaviour in larval gulf menhaden

Schooling behaviour was examined in larval gulf menhaden Brevoortia patronus under decreasing and increasing light intensities and related to movements of retinal photoreceptors and pigment. Nearest neighbour angles and nearest neighbour distances between fish were inversely related to light intensity and were independent of the direction of intensity change. Swimming speeds of individual fish were directly related to light intensity when intensity was decreased but did not increase when intensity was raised. The changes in nearest neighbour angles and distances more closely paralleled movements of retinal pigment cells than cone cell migration, suggesting that rod photoreceptors play a greater role than cones in determining the threshold light intensity for schooling. A general model is developed relating the threshold light intensity for schooling to eye diameter for a number of different species and the implications of this relationship are discussed.     

Social cohesion in groups of sheep: Effect of activity level, sex composition and group size

We investigated the effects of activity, group size and sex composition on the cohesion of merino sheep (Ovis aries) groups. Mixed-sex (50% of each sex) and single-sex groups of 2, 4, 6 and 8 sheep were placed within 491-m² arenas located in natural pastures and were video recorded during 6 daily hours. The behaviour, orientation and location of each sheep were then extracted from the films at 1-s intervals. We analysed the polarisation of individual orientations, mean inter-individual and nearest neighbours’ distances, as well as the frequency of pairs of nearest neighbours according to their sex within mixed-sex groups. Sheep were more aggregated than predicted under the null hypothesis of random spatial distribution for all group compositions and sizes. Sheep were more spread out and less aligned in half-active than in all-active groups, showing that social cohesion was reduced by a lack of activity synchronisation. The highest proximity between individuals was found in resting groups, yet alignment was low. The polarisation peaked in all-active groups. Mean inter-individual distance did not vary and the nearest neighbour distance decreased as group size increased. When sheep were all-active or all-resting, mixed-sex groups were more spread out than single-sex ones, with a greater distance between opposite than between same-sex individuals. Nearest neighbours of the same sex were also more frequent than random. Our results show that social cohesion can be modulated by activity synchrony but also by social affinity.     

Reading faces: differential lateral gaze bias in processing canine and human facial expressions in dogs and 4-year-old children

Sensitivity to the emotions of others provides clear biological advantages. However, in the case of heterospecific relationships, such as that existing between dogs and humans, there are additional challenges since some elements of the expression of emotions are species-specific. Given that faces provide important visual cues for communicating emotional state in both humans and dogs, and that processing of emotions is subject to brain lateralisation, we investigated lateral gaze bias in adult dogs when presented with pictures of expressive human and dog faces. Our analysis revealed clear differences in laterality of eye movements in dogs towards conspecific faces according to the emotional valence of the expressions. Differences were also found towards human faces, but to a lesser extent. For comparative purpose, a similar experiment was also run with 4-year-old children and it was observed that they showed differential processing of facial expressions compared to dogs, suggesting a species-dependent engagement of the right or left hemisphere in processing emotions.     

A Bayesian network approach incorporating imputation of missing data enables exploratory analysis of complex causal biological relationships

Bayesian networks can be used to identify possible causal relationships between variables based on their conditional dependencies and independencies, which can be particularly useful in complex biological scenarios with many measured variables. Here we propose two improvements to an existing method for Bayesian network analysis, designed to increase the power to detect potential causal relationships between variables (including potentially a mixture of both discrete and continuous variables). Our first improvement relates to the treatment of missing data. When there is missing data, the standard approach is to remove every individual with any missing data before performing analysis. This can be wasteful and undesirable when there are many individuals with missing data, perhaps with only one or a few variables missing. This motivates the use of imputation. We present a new imputation method that uses a version of nearest neighbour imputation, whereby missing data from one individual is replaced with data from another individual, their nearest neighbour. For each individual with missing data, the subsets of variables to be used to select the nearest neighbour are chosen by sampling without replacement the complete data and estimating a best fit Bayesian network. We show that this approach leads to marked improvements in the recall and precision of directed edges in the final network identified, and we illustrate the approach through application to data from a recent study investigating the causal relationship between methylation and gene expression in early inflammatory arthritis patients. We also describe a second improvement in the form of a pseudo-Bayesian approach for upweighting certain network edges, which can be useful when there is prior evidence concerning their directions.     

Dynamic spatial coding within the dorsal frontoparietal network during a visual search task

To what extent are the left and right visual hemifields spatially coded in the dorsal frontoparietal attention network? In many experiments with neglect patients, the left hemisphere shows a contralateral hemifield preference, whereas the right hemisphere represents both hemifields. This pattern of spatial coding is often used to explain the right-hemispheric dominance of lesions causing hemispatial neglect. However, pathophysiological mechanisms of hemispatial neglect are controversial because recent experiments on healthy subjects produced conflicting results regarding the spatial coding of visual hemifields. We used an fMRI paradigm that allowed us to distinguish two attentional subprocesses during a visual search task. Either within the left or right hemifield subjects first attended to stationary locations (spatial orienting) and then shifted their attentional focus to search for a target line. Dynamic changes in spatial coding of the left and right hemifields were observed within subregions of the dorsal front-parietal network: During stationary spatial orienting, we found the well-known spatial pattern described above, with a bilateral hemifield representation in the right hemisphere and a contralateral preference in the left hemisphere. However, during search, the right hemisphere had a contralateral preference and the left hemisphere equally represented both hemifields. This finding leads to novel perspectives regarding models of visuospatial attention and hemispatial neglect.     

Functional asymmetry of the neocortex electrical activity during food conditioning in dogs

Four dogs were trained to perform a conditioned alimentary response to a sound stimulus. The EEG was recorded from six pairs of chronically implanted neocortical electrodes. The EEG spectra and coherence functions between the neighboring derivations of each of the hemispheres were analyzed in the theta, alpha, beta 1 and beta 2 frequency ranges. At the first stages of conditioning, the percent of cases increased when the highest mean values of EEG frequency were localized in the left hemisphere. Later on the percent of cases, when the mean coherence values in the left hemisphere were higher than in the right hemisphere, also increased. At the stage of conditioned response stabilization, this asymmetry either disappeared or the right hemisphere became more active than the left one. The spatial localization of the maximal values of the EEG frequency was different for different frequency ranges. The highest values in the beta 1 range were more frequently registered in the posterior cortical regions and in the beta 2 range they were revealed, predominantly, in the anterior areas. The maximal values of coherence dominated in the anterior regions and their spatial distribution was similar for different frequencies. Thus, the initial stages of conditioning are accompanied by activation of the left hemisphere.     

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.     

Why do birds sleep with one eye open? Light exposure of the chick embryo as a determinant of monocular sleep.

Together with some aquatic mammals, birds exhibit a unique behavioral and electrophysiological state called "unihemispheric sleep," in which one cerebral hemisphere is awake and the other is sleeping. Slow-wave sleep in one hemisphere is associated with closure of the contralateral eye, while the eye contralateral to the awake hemisphere is open; closure of both eyes, in contrast, is associated with bihemispheric slow-wave sleep or with REM sleep. During the last few days of incubation, the chick's embryo is turned in the egg so that it occludes its left eye, whereas light entering through the shell can stimulate the right eye. Here we show that in the first two days after hatching, chicks coming from eggs incubated in the light prevalently slept with their right eye open, whereas those coming from eggs incubated in the dark prevalently slept with their left eye open. Thus, asymmetric light stimulation in the embryo can modulate the left-right direction of eye opening during post-hatching monocular sleep.     

The effects of simulated microgravity on characteristics of slow presaccadic potentials

The parameters of saccades and presaccadic slow potentials were studied in seven right-handed male volunteers with a dominant right eye before and after exposure to 6-day dry immersion. Visual stimuli were presented using three light diodes, which were located in the center of the visual field (the central fixation stimulus) and 10° to the right and left of it (peripheral stimuli (PSs)). The subjects performed a test with simple saccades to a PS and a test with antisaccades to the point located symmetrically in the opposite visual field. The EEG (19 monopolar leads) and electrooculogram were recorded. To isolate slow potentials, backward EEG averaging was performed, with the moment of switching on the PS serving as a trigger for the averaging. It was found that the characteristics of saccadic eye movements did not substantially change after exposure to immersion. However, both tests revealed a change in topography and a decrease in the amplitude of presaccadic slow negative potentials (PSNPs) during immersion. Characteristically, the focus of presaccadic negativity shifted to the right hemisphere so that the PSNP amplitude sharply decreased in the left and increased in the right hemisphere. A significant decrease in the PSNP amplitude on day 6 of immersion was found in the midline and left-hemispheric frontal and parietal leads. It may be suggested that, because of support unloading and a decrease in proprioceptive input, exposure to microgravity causes a decrease in the activity of the left hemisphere and prefrontal and parietal cortices, initially involved in preparation and realization of motor responses. The activation of the right hemisphere could be of compensatory character.     

Neighbourhood analysis as an indicator of spatial requirements of broiler chickens

The appropriate stocking density for broiler chickens is a much discussed topic in animal welfare. To determine at which stocking density the level of crowding becomes aversive to 4–6-week-old broiler chickens, spatial distribution and behaviour of groups stocked at 8, 19, 29, 40, 45, 51, 61 or 72 birds per 3.3 m² were analysed. Spatial distribution was evaluated using three different indices: inter-individual distances, nearest neighbour distances and Dirichlet polygon areas. The assumption was that broilers would increase the distance to their pen mates if high densities (i.e., close proximity to pen mates) were experienced as aversive, whereas they would decrease this distance if close proximity was experienced positively. Increased distances to pen mates would lead to increased nearest neighbour distances and a more homogeneous distribution (i.e., lower variation of inter-individual distances and of Dirichlet-polygon size) than expected by chance. The distribution expected by chance was determined from both a random distribution and a ‘resource-corrected’ random distribution (which incorporated environmental influences on spatial distribution but excluded social ones).Behavioural observations showed that at higher stocking densities more sitting bouts (P = 0.003) and adjustments of the sitting and lying posture (P < 0.001) occurred. It was also found that nearest neighbour distance varied according to behaviour (P = 0.001). Birds that were eating/drinking were further apart from their nearest neighbour than birds that were foraging, preening, adjusting their sitting or lying posture or showing “other” behaviour.The results from all three methods of spatial analysis suggested that broilers in groups ≥19 birds per 3.3 m² (ultimately equivalent to 15 kg/m²) started to experience the proximity of conspecifics as aversive at some point during the last 3 weeks of rearing. However, nearest neighbour distance analysis showed evidence of aversiveness earlier in life than the other methods of analyzing spatial distribution (variation in inter-individual distance and polygon size), suggesting that nearest neighbour distance is the more sensitive indicator of space requirements.When uneven use of the different areas within the pen was reflected in the expected distribution (i.e., for comparisons to the resource-corrected random distribution) different results were obtained than when such measures were omitted (i.e., for comparisons to the random distribution). As such, this study emphasises the importance of accounting for environmental influences on distribution within a pen.     

It's in the eye of the beholder: visual lateralisation in response to the social environment in poeciliids

The social environment offers fish complex information about the quality, performance, personality and other cues of potential mates and competitors simultaneously. It is likely, therefore, that the environmental information regarding the context of mate choice is perceived and processed differently in species and sexes in respect to lateralisation. The present study comparatively assessed visual lateralisation behaviour in response to different social or sexual stimuli in three closely related poeciliid species (P. latipinna, P. mexicana, P. formosa) in comparison to a more distantly related species (P. reticulata). Individuals were presented with four different social or sexual stimuli that were tested against a control stimulus; (a) a conspecific male, (b) a conspecific female, (c) a heterosexual conspecific pair, (d) three conspecific females (shoal). In order to approach a target stimulus, focal fish had to perform detours to the right or left of a vertically straight-shaped barrier. The three closely related poeciliid species, P. latipinna, P. mexicana, P. formosa, appeared to have a general tendency to turn right (i.e., left-eye preference), whereas the more distantly related P. reticulata males and females showed an overall bias to the left (i.e., right-eye preference) in response to various social–sexual incitements. Moreover, body size seemed to significantly influence especially the males’ detour behaviour, with smaller males acting in opposition to their larger conspecifics in response to certain social stimuli. In this case, smaller and larger Poecilia spp. males responded in the same way as smaller and larger males of the other three poeciliid species. Therefore, results possibly point to differences in the degree of general social behaviour between closely and more distantly related species and mating motivation amongst larger and smaller individuals when placed in a novel social environment. Hence, present results possibly suggest a sex-specific functional lateralisation for the analysis of visual information and seem to support the closer ancestral relationships between the Poecilia spp. tested in this study and the more distantly related guppies in terms of their left–right lateralisation. Generally, present results suggest that functional asymmetries in behaviour could be widespread among vertebrates, thus supporting the hypothesis of an early evolution of lateralisation in brain and behaviour.     

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.     

Ecological and Social Determinants of Group Cohesiveness and Within‐Group Spatial Position in Wild Assamese Macaques

Individual spatial positioning plays an important role in mediating the costs and benefits of group living and, as such, shapes different aspects of animal social systems including group structure and cohesiveness. Here, we aim to quantify variation in individual spacing behaviour and its correlates in a group of wild Assamese macaques (Macaca assamensis) in north‐eastern Thailand, which experiences both predation pressure and within‐group feeding competition. Data on individual spatial positions were collected during group scans using GPS devices and results suggest that both group cohesiveness and individual spatial positions within a group can be adjusted to mediate the costs and benefits of group living. Individuals had greater nearest neighbour distances and lower numbers of close neighbours when the group was feeding, compared to when the main group activity was resting/social or moving. This is likely due to the high costs of proximity associated with feeding competition. Immature individuals and females with young infants which are more vulnerable to predation were located closer to the centre of the group than both adult males and females without infants. This indicates the importance of predation risk in driving individual spatial position. Among adults, higher ranking individuals occupied more central positions within the group while lower ranking individuals were more peripheral. It appears that low ranking individuals trade reduced feeding interference and improved feeding success for increased predation risk. This could help explain why females in the study population do not display a rank related skew in energy intake.     

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.     

Hemispheric specialization in dogs for processing different acoustic stimuli

Considerable experimental evidence shows that functional cerebral asymmetries are widespread in animals. Activity of the right cerebral hemisphere has been associated with responses to novel stimuli and the expression of intense emotions, such as aggression, escape behaviour and fear. The left hemisphere uses learned patterns and responds to familiar stimuli. Although such lateralization has been studied mainly for visual responses, there is evidence in primates that auditory perception is lateralized and that vocal communication depends on differential processing by the hemispheres. The aim of the present work was to investigate whether dogs use different hemispheres to process different acoustic stimuli by presenting them with playbacks of a thunderstorm and their species-typical vocalizations. The results revealed that dogs usually process their species-typical vocalizations using the left hemisphere and the thunderstorm sounds using the right hemisphere. Nevertheless, conspecific vocalizations are not always processed by the left hemisphere, since the right hemisphere is used for processing vocalizations when they elicit intense emotion, including fear. These findings suggest that the specialisation of the left hemisphere for intraspecific communication is more ancient that previously thought, and so is specialisation of the right hemisphere for intense emotions.     

Spatial pattern,regeneration and growth rates of Brachystegia spiciformis and Julbernardia globiflora

Past work on tree-to-tree interactions in semi-arid savannas, through the use of nearest neighbour analysis, has shown both a regular dispersion pattern and a positive correlation between the size of a tree and the distance to its nearest neighbour. From these results, the importance of competition has been inferred. In the present study, tree-to-tree interactions in a mesic savanna woodland at Marondera, Zimbabwe, dominated by relatively small-sized individuals of Brachystegia spiciformis and Julbernardia globiflora, were examined. Results show that the regular dispersion pattern is uncommon; that there are few significant positive correlations between size of individual and distance to nearest neighbour; and that growth rate is not consistently correlated with size and distance of nearest neighbour. Results of a study of regeneration relative to canopy cover suggest a possible mechanism for these findings: unlike semi-arid savannas, young plants often grow in under-canopy environments so that early spacing of young trees does not occur. Significant positive correlations between the size of a tree and the distance to its nearest neighbour were found in a stand of larger, presumably older, trees, suggesting that such a relationship only develops in mesic miombo woodland through a thinning process as the trees mature. Familial clumping, which is common in the study area, may mask spatial patterns.Abbreviations RBAI Relative basal area increment