Visuo-motor lateralization in Apis mellifera: flight speed differences in foraging choices.

Evidence of lateralization has been provided in Apis mellifera in olfactory learning and social interactions, but not much is known about how it influences visuo-motor tasks. This study investigates visuo-motor biases in free-flying honeybees by analysing left/right choices related to foraging in a Y-maze. Individual bees were trained to associate a visual stimulus (a blue or yellow target) with a reward/punishment: the Blue + group was reinforced for the blue and punished for the yellow, and vice versa for the Yellow + group. In unrewarded tests, we assessed for each bee the directional choice for one of the two identical targets (12 trials with blue targets and 12 with yellow targets) placed in the left and right arms of the maze as well as the flight times to reach the target chosen. The results did not reveal a significant directional preference at the population level, but only at the individual level, with some individuals presenting a strong bias for choosing the right or left stimulus. However, the data revealed an interesting new factor: the influence of both direction and colour on flight times. Overall, bees took less time to choose the stimulus in the left arm. Furthermore, the yellow target, when previously associated with a punishment, was reached on average faster than the punished blue target, with a higher number of no-choices for punished blue targets than for punished yellow targets. This opens new perspectives not only on the study of lateralization in Apis mellifera, but also on the bees' chromatic preferences.

How bumblebees coordinate path integration and body orientation at the start of their first learning flight.

The start of a bumblebee's first learning flight from its nest provides an opportunity to examine the bee's learning behaviour during its initial view of the nest's unfamiliar surroundings. Like many other hymenopterans, bumblebees store views of their nest surroundings while facing their nest. We found that a bumblebee's first fixation of the nest is a coordinated manoeuvre in which the insect faces the nest with its body oriented towards a particular visual feature within its surroundings. This conjunction of nest fixation and body orientation is preceded and reached by means of a translational scan during which the bee flies perpendicularly to its preferred body orientation. The utility of the coordinated manoeuvre is apparent during the bees' first return flight after foraging. Bees then adopt a similar preferred body orientation when close to the nest. How does a bee, unacquainted with its surroundings, know when it is facing its nest? A likely answer is through path integration, which gives bees continuously updated information about the current direction of their nest. Path integration also gives bees the possibility to fixate the nest when their body points in a desired direction. The three components of this coordinated manoeuvre are discussed in relation to current understanding of the central complex in the insect brain, noting that nest fixation is egocentric, whereas the preferred body orientation and flight direction that the bee adopts within the visual surroundings of the nest are geocentric.

Does owner handedness influence paw preference in dogs?

Handedness has proven to be the most effective and least intrusive measure of laterality in many species. Several studies have investigated paw preference in dogs (Canis familiaris) without considering the potential impact that owner's handedness may have on it, despite dogs being a domesticated species. The aim of this study was to investigate whether owner handedness influences paw preference in their dogs. Sixty-two dogs had their paw preference tested using a Paw Task and a Reach Task in their home over 10 days, recorded by their owners. Interestingly, it was found that left-handed owners were more likely to own a dog with a left paw bias, and right-handed owners were more likely to own a dog with a right paw bias. In the Paw Task, the hand presented to a dog did not significantly predict which paw the dog lifted in response. Furthermore, it was found that females displayed a right paw bias at all age groups. However, males had a left paw bias in puppyhood and right paw bias in older age groups. We conclude that owner handedness influences paw preference in dogs, and it should be considered when suitably pairing dogs to potential owners, especially in assistance work.

Testing of behavioural asymmetries as markers for brain lateralization of emotional states in pet dogs: A critical review.

Domestic dogs (Canis familiaris) hold a unique position in human society, particularly in their role as social companions; as such, it is important to understand their emotional lives. There has been growing interest in studying behavioural biases in dogs as indirect markers (reflecting lateralized brain activity) of their emotional states. In this paper, we not only review the previous literature on emotion-related behavioural lateralization in dogs, but also propose and apply the concept of evidential weight to previous research. This allows us to examine different hypotheses about emotion-related brain asymmetries (i.e., Right-Hemisphere-, Valence-, Approach-Withdrawal-Hypothesis) on the basis of a "likelihood-ist" concept of evidence. We argue that previous studies have not been able to discriminate well between competing hypotheses and tended to focus on confirmation bias than critically assess different hypotheses; as such there is a strong case for more systematic investigation to pull these theories apart. We present the areas for future research and explain their importance for understanding the emotional lives of dogs.

Investigating the influence of neuter status on paw preference in dogs and cats.

Motor lateralization is commonly observed through preferential paw use in dogs and cats. Previous studies have uncovered sex-related differences in paw preference, hypothesizing that these differences may be related to sex hormones. The current study aimed to compare neutered and entire individuals to further investigate whether paw preference is influenced by sex hormones. Dog and cat owners were required to fill in a questionnaire with demographic information such as sex and neuter status of their pets. They then carried out two simple paw preference tasks within their homes: a "reaching for food" task and a "reaching for a toy" task. This study revealed an overall preference among the 272 dogs and 137 cats tested to use their right paw in both tasks. In cats, the degree of paw preference (i.e., regardless of the direction) was significantly influenced by an interaction between neuter status and life stage. Also in dogs, both life stage and an interaction between neuter status and life stage tended to influence the degree of paw preference. Post-hoc power analysis revealed a lack of statistical power, suggesting that future studies using a larger sample size are needed to further investigate potential effects of neuter status on paw preference.

Is There an Association between Paw Preference and Emotionality in Pet Dogs?

Research with humans and other animals has suggested that preferential limb use is linked to emotionality. A better understanding of this still under-explored area has the potential to establish limb preference as a marker of emotional vulnerability and risk for affective disorders. This study explored the potential relationship between paw preference and emotionality in pet dogs. We examined which paw the dogs preferentially used to hold a Kong™ and to perform two different locomotion tests. Dogs' emotionality was assessed using a validated psychometric test (the Positive and Negative Activation Scale-PANAS). Significant positive correlations were found for dogs' paw use between the different locomotion tasks, suggesting that dogs may show a more general paw preference that is stable across different types of locomotion. In comparison, the correlations between the Kong™ Test and locomotion tests were only partially significant, likely due to potential limitations of the Kong™ Test and/or test-specific biomechanical requirements. No significant correlations were identified between paw preference tests and PANAS scores. These results are in contrast to previous reports of an association between dog paw preference and emotionality; animal limb preference might be task-specific and have variable task-consistency, which raises methodological questions about the use of paw preference as a marker for emotional functioning.

Abnormal visual attention to simple social stimuli in 4-month-old infants at high risk for Autism.

Despite an increasing interest in detecting early signs of Autism Spectrum Disorders (ASD), the pathogenesis of the social impairments characterizing ASD is still largely unknown. Atypical visual attention to social stimuli is a potential early marker of the social and communicative deficits of ASD. Some authors hypothesized that such impairments are present from birth, leading to a decline in the subsequent typical functioning of the learning-mechanisms. Others suggested that these early deficits emerge during the transition from subcortically to cortically mediated mechanisms, happening around 2-3 months of age. The present study aimed to provide additional evidence on the origin of the early visual attention disturbance that seems to characterize infants at high risk (HR) for ASD. Four visual preference tasks were used to investigate social attention in 4-month-old HR, compared to low-risk (LR) infants of the same age. Visual attention differences between HR and LR infants emerged only for stimuli depicting a direct eye-gaze, compared to an adverted eye-gaze. Specifically, HR infants showed a significant visual preference for the direct eye-gaze stimulus compared to LR infants, which may indicate a delayed development of the visual preferences normally observed at birth in typically developing infants. No other differences were found between groups. Results are discussed in the light of the hypotheses on the origins of early social visual attention impairments in infants at risk for ASD.

Looking at lateralization as a dynamic and plastic feature of nervous systems.

In the last few decades, research on lateralization has expanded our knowledge about the manifestation, development, and mechanisms of this fascinating feature of nervous systems. This has been possible not only thanks to human studies, but to the use of animal models and the introduction of ground-breaking techniques within this research field. However, recent studies have also demonstrated how complex this phenomenon is and highlighted that we still lack a complete understanding of brain and behavioural asymmetries. Here, I comment on two of the challenges presented by Ocklenburg and colleagues that research on lateralization has to face in the next future. I argue that, in order to improve our understanding of lateralization, we have to consider it as a dynamic and plastic characteristic, which is strongly influenced by both internal factors, such as an animal's motivation and emotional states, and external factors, including the physical environment and the social context.

Small and Large Bumblebees Invest Differently when Learning about Flowers.

Honeybees1 and bumblebees2 perform learning flights when leaving a newly discovered flower. During these flights, bees spend a portion of the time turning back to face the flower when they can memorize views of the flower and its surroundings. In honeybees, learning flights become longer when the reward offered by a flower is increased.3 We show here that bumblebees behave in a similar way, and we add that bumblebees face an artificial flower more when the concentration of the sucrose solution that the flower provides is higher. The surprising finding is that a bee's size determines what a bumblebee regards as a "low" or "high" concentration and so affects its learning behavior. The larger bees in a sample of foragers only enhance their flower facing when the sucrose concentration is in the upper range of the flowers that are naturally available to bees.4 In contrast, smaller bees invest the same effort in facing flowers whether the concentration is high or low, but their effort is less than that of larger bees. The way in which different-sized bees distribute their effort when learning about flowers parallels the foraging behavior of a colony. Large bumblebees5,6 are able to carry larger loads and explore further from the nest than smaller ones.7 Small ones with a smaller flight range and carrying capacity cannot afford to be as selective and so accept a wider range of flowers. VIDEO ABSTRACT.

Visuo-motor biases in buff-tailed bumblebees (Bombus terrestris).

Bees provide a good model to investigate the evolution of lateralization. So far, most studies focused on olfactory learning and memories in tethered bees. This study investigated possible behavioural biases in free-flying buff-tailed bumblebees (Bombus terrestris) by analysing their turning decisions in a T-maze. Bees of various size were trained to associate a syrup reward with a blue target placed at the centre of the T-maze. The bees were then tested over 16 trials by presenting them with blue targets at the end of the maze's arms. The maze was rotated 180° after the first 8 trials to control for environmental factors. The number of turnings to the left and right arms were analysed. The bees sampled exhibited a population-level rightward turning bias. As bumblebees vary significantly in size with large bees being better learners than smaller ones, we measured the thorax width to identify a possible relationship between size and bias. No significant correlation was identified. This study shows that bees present lateralization in a visuo-motor task that mimics their foraging behaviour, indicating a possible specialization of the right side of the nervous system in routine tasks.

No evidence that footedness in pheasants influences cognitive performance in tasks assessing colour discrimination and spatial ability.

The differential specialization of each side of the brain facilitates the parallel processing of information and has been documented in a wide range of animals. Animals that are more lateralized as indicated by consistent preferential limb use are commonly reported to exhibit superior cognitive ability as well as other behavioural advantages. We assayed the lateralization of 135 young pheasants (Phasianus colchicus), indicated by their footedness in a spontaneous stepping task, and related this measure to individual performance in either 3 assays of visual or spatial learning and memory. We found no evidence that pronounced footedness enhances cognitive ability in any of the tasks. We also found no evidence that an intermediate footedness relates to better cognitive performance. This lack of relationship is surprising because previous work revealed that pheasants have a slight population bias towards right footedness, and when released into the wild, individuals with higher degrees of footedness were more likely to die. One explanation for why extreme lateralization is constrained was that it led to poorer cognitive performance, or that optimal cognitive performance was associated with some intermediate level of lateralization. This stabilizing selection could explain the pattern of moderate lateralization that is seen in most non-human species that have been studied. However, we found no evidence in this study to support this explanation.

Low survival of strongly footed pheasants may explain constraints on lateralization.

Brain lateralization is considered adaptive because it leads to behavioral biases and specializations that bring fitness benefits. Across species, strongly lateralized individuals perform better in specific behaviors likely to improve survival. What constrains continued exaggerated lateralization? We measured survival of pheasants, finding that individuals with stronger bias in their footedness had shorter life expectancies compared to individuals with weak biases. Consequently, weak, or no footedness provided the highest fitness benefits. If, as suggested, footedness is indicative of more general brain lateralization, this could explain why continued brain lateralization is constrained even though it may improve performance in specific behaviors.

The Dominant Role of Visual Motion Cues in Bumblebee Flight Control Revealed Through Virtual Reality.

Flying bees make extensive use of optic flow: the apparent motion in the visual scene generated by their own movement. Much of what is known about bees' visually-guided flight comes from experiments employing real physical objects, which constrains the types of cues that can be presented. Here we implement a virtual reality system allowing us to create the visual illusion of objects in 3D space. We trained bumblebees, Bombus ignitus, to feed from a static target displayed on the floor of a flight arena, and then observed their responses to various interposing virtual objects. When a virtual floor was presented above the physical floor, bees were reluctant to descend through it, indicating that they perceived the virtual floor as a real surface. To reach a target at ground level, they flew through a hole in a virtual surface above the ground, and around an elevated virtual platform, despite receiving no reward for avoiding the virtual obstacles. These behaviors persisted even when the target was made (unrealistically) visible through the obstructing object. Finally, we challenged the bees with physically impossible ambiguous stimuli, which give conflicting motion and occlusion cues. In such cases, they behaved in accordance with the motion information, seemingly ignoring occlusion.

Insights into the evolution of lateralization from the insects.

Behavioral lateralization is widespread across the animals, being found in numerous vertebrate species as well as in species from across many invertebrate phyla. Numerous recent studies have focused on lateralization in the insects, exploring the behaviors themselves as well as their neural basis and the possible selective pressures that led to their evolution. Lateralization in the insects can occur in any sensory modality and may be generated by peripheral or central neural asymmetries. The lateralization of particular insect behaviors can show either population-level or individual-level lateralization but which of these types of lateralization is present is strongly influenced by their social environment. Different behaviors from the same species show population-level or individual-level lateralization depending on whether these behaviors are used in social interactions or not. This has broad implications for our understanding of how lateralization and handedness evolves not just in insects but also in vertebrates.

Variations on a theme: bumblebee learning flights from the nest and from flowers.

On leaving a significant place to which they will return, bees and wasps perform learning flights to acquire visual information to guide them back. The flights are set in different contexts, such as from their nest or a flower, which are functionally and visually different. The permanent and inconspicuous nest hole of a bumblebee worker is locatable primarily through nearby visual features, whereas a more transient flower advertises itself by its colour and shape. We compared the learning flights of bumblebees leaving their nest or a flower in an experimental situation in which the nest hole, flower and their surroundings were visually similar. Consequently, differences in learning flights could be attributed to the bee's internal state when leaving the nest or flower rather than to the visual scene. Flights at the flower were a quarter as long as those at the nest and more focused on the flower than its surroundings. Flights at the nest covered a larger area with the bees surveying a wider range of directions. For the initial third of the learning flight, bees kept within about 5 cm of the flower and nest hole, and tended to face and fixate the nest, flower and nearby visual features. The pattern of these fixations varied between nest and flower, and these differences were reflected in the bees' return flights to the nest and flower. Together, these findings suggest that learning flights are tuned to the bees' inherent expectations of the visual and functional properties of nests and flowers.

Male bumblebees perform learning flights on leaving a flower but not when leaving their nest.

Female bees and wasps demonstrate, through their performance of elaborate learning flights, when and where they memorise features of a significant site. An important feature of these flights is that the insects look back to fixate the site that they are leaving. Females, which forage for nectar and pollen and return with it to the nest, execute learning flights on their initial departure from both their nest and newly discovered flowers. To our knowledge, these flights have so far only been studied in females. Here, we describe and analyse putative learning flights observed in male bumblebees Bombus terrestris L. Once male bumblebees are mature, they leave their nest for good and fend for themselves. We show that, unlike female foragers, males always fly directly away from their nest, without looking back, in keeping with their indifference to their natal nest. In contrast, after males have drunk from artificial flowers, their flights on first leaving the flowers resemble the learning flights of females, particularly in their fixation of the flowers. These differences in the occurrence of female and male learning flights seem to match the diverse needs of the two sexes to learn about disparate, ecologically relevant places in their surroundings.

Difference in Visual Social Predispositions Between Newborns at Low- and High-risk for Autism.

Some key behavioural traits of Autism Spectrum Disorders (ASD) have been hypothesized to be due to impairments in the early activation of subcortical orienting mechanisms, which in typical development bias newborns to orient to relevant social visual stimuli. A challenge to testing this hypothesis is that autism is usually not diagnosed until a child is at least 3 years old. Here, we circumvented this difficulty by studying for the very first time, the predispositions to pay attention to social stimuli in newborns with a high familial risk of autism. Results showed that visual preferences to social stimuli strikingly differed between high-risk and low-risk newborns. Significant predictors for high-risk newborns were obtained and an accurate biomarker was identified. The results revealed early behavioural characteristics of newborns with familial risk for ASD, allowing for a prospective approach to the emergence of autism in early infancy.

The Bee as a Model to Investigate Brain and Behavioural Asymmetries.

The honeybee Apis mellifera, with a brain of only 960,000 neurons and the ability to perform sophisticated cognitive tasks, has become an excellent model in life sciences and in particular in cognitive neurosciences. It has been used in our laboratories to investigate brain and behavioural asymmetries, i.e., the different functional specializations of the right and the left sides of the brain. It is well known that bees can learn to associate an odour stimulus with a sugar reward, as demonstrated by extension of the proboscis when presented with the trained odour in the so-called Proboscis Extension Reflex (PER) paradigm. Bees recall this association better when trained using their right antenna than they do when using their left antenna. They also retrieve short-term memory of this task better when using the right antenna. On the other hand, when tested for long-term memory recall, bees respond better when using their left antenna. Here we review a series of behavioural studies investigating bees' lateralization, integrated with electrophysiological measurements to study asymmetries of olfactory sensitivity, and discuss the possible evolutionary origins of these asymmetries. We also present morphological data obtained by scanning electron microscopy and two-photon microscopy. Finally, a behavioural study conducted in a social context is summarised, showing that honeybees control context-appropriate social interactions using their right antenna, rather than the left, thus suggesting that lateral biases in behaviour might be associated with requirements of social life.