Unlocking the symmetric transfer of irrelevant information: gene-environment interplay and enhanced interhemispheric cross-talk.

Hemispheric specialization influences stimulus processing and behavioural control, affecting responses to relevant stimuli. However, most sensory input is irrelevant and must be filtered out to prevent interference with task-relevant behaviour, a process known as habituation. Despite habituation's vital role, little is known about hemispheric specialization for this brain function. We conducted an experiment with domestic chicks, an elite animal model to study lateralization. They were exposed to distracting visual stimuli while feeding when using binocular or monocular vision. Switching the viewing eye after habituation, we examined if habituation was confined to the stimulated hemisphere or shared across hemispheres. We found that both hemispheres learned equally to ignore distracting stimuli. However, embryonic light stimulation, influencing hemispheric specialization, revealed an asymmetry in interhemispheric transfer of the irrelevant information discarded via habituation. Unstimulated chicks exhibited a directional bias, with the right hemisphere failing to transfer distracting stimulus information to the left hemisphere, while transfer from left to right was possible. Nevertheless, embryonic light stimulation counteracted this asymmetry, enhancing communication from the right to the left hemisphere and reducing the pre-existing imbalance. This sharing extends beyond hemisphere-specific functions and encompasses a broader representation of irrelevant events.

Lateralized motor behaviour in the righting responses of the cane toad (Rhinella marina).

This paper reports a series of tests for fore- and hind-limb preferences used by cane toads, Rhinella marina, to assist returning to the righted position after being overturned. We confirm the strong and significant right-handedness reported in this species, which under certain conditions exceeded 90% right-hand preference at the group level. Toads were tested under a variety of conditions including horizontal and inclined surfaces, with and without the opportunity for the forelimbs to grasp a support, in order to assess the effects of different vestibular and proprioceptive input on the strength and direction of fore- and hind-limb preferences. A range of behavioural strategies indicated learning effects; however, the strength or direction of limb preferences did not increase significantly with experience, even in toads retested multiple times. Comparisons with the mammalian condition for limb preferences are discussed with relevance to practice effects and established limb preferences, and to effects associated with arousal or stress. In contrast to the expectation that handedness in toads represents intentional or voluntary preferences, the presence of lateralized central pattern generators in the toads is postulated to explain the different forms of lateralization revealed by our tests.

Asymmetry of brain and behavior in animals: Its development, function, and human relevance.

Since the discovery of brain asymmetry in a wide range of vertebrate species, it has become possible to study development and expression of lateralized behavior accurately in well-controlled experiments. Several species have emerged as useful models for investigating aspects of lateralization. Discussed here are: (1) the influence of exposure to light during embryonic development on lateralization, (2) effects of steroid hormones on lateralization, (3) developmental changes in which hemisphere is controlling behavior, and (4) asymmetry in memory formation and recall. The findings have bearing on understanding the development of hemispheric specialization in humans and are likely to provide insight into dysfunctional behavior associated with weak or absent lateralization and impaired interhemispheric communication (e.g., autism, schizophrenia, and dyslexia). This review features research on chicks, pigeons, and zebrafish, with the addition of some recent evidence of lateralization in bees. Discoveries made using these species have highlighted the interaction between experience, hormones, and genetic factors during development, and have provided some of the first clear evidence of the advantage of having a lateralized brain.

Ontogenetic development of magnetic compass orientation in domestic chickens (Gallus gallus).

Domestic chickens (Gallus gallus) can be trained to search for a social stimulus in a specific magnetic direction, and cryptochrome 1a, found in the retina, has been proposed as a receptor molecule mediating magnetic directions. The present study combines immuno-histochemical and behavioural data to analyse the ontogenetic development of this ability. Newly hatched chicks already have a small amount of cryptochrome 1a in their violet cones; on day 5, the amount of cryptochrome 1a reached the same level as in adult chickens, suggesting that the physical basis for magnetoreception is present. In behavioural tests, however, young chicks 5 to 7 days old failed to show a preference of the training direction; on days 8, 9 and 12, they could be successfully trained to search along a specific magnetic axis. Trained and tested again 1 week later, the chicks that had not shown a directional preference on days 5 to 7 continued to search randomly, while the chicks tested from day 8 onward preferred the correct magnetic axis when tested 1 week later. The observation that the magnetic compass is not functional before day 8 suggests that certain maturation processes in the magnetosensitive system in the brain are not yet complete before that day. The reasons why chicks that have been trained before that day fail to learn the task later remain unclear.

Knowledge of lateralized brain function can contribute to animal welfare.

The specialized functions of each hemisphere of the vertebrate brain are summarized together with the current evidence of lateralized behavior in farm and companion animals, as shown by the eye or ear used to attend and respond to stimuli. Forelimb preference is another manifestation of hemispheric lateralization, as shown by differences in behavior between left- and right-handed primates, left- and right-pawed dogs and cats, and left- and right-limb-preferring horses. Left-limb preference reflects right hemisphere use and is associated with negative cognitive bias. Positive cognitive bias is associated with right-limb and left-hemisphere preferences. The strength of lateralization is also associated with behavior. Animals with weak lateralization of the brain are unable to attend to more than one task at a time, and they are more easily stressed than animals with strong lateralization. This difference is also found in domesticated species with strong vs. weak limb preferences. Individuals with left-limb or ambilateral preference have a bias to express functions of the right hemisphere, heightened fear and aggression, and greater susceptibility to stress. Recognition of lateralized behavior can lead to improved welfare by detecting those animals most likely to suffer fear and distress and by indicating housing conditions and handling procedures that cause stress.

Unfolding a sequence of sensory influences and interactions in the development of functional brain laterality.

Evidence of sensory experience influencing the development of lateralized brain and behavior is reviewed. The epigenetic role of light exposure during two specific stages of embryonic development of precocial avian species is a particular focus of the research discussed. Two specific periods of light sensitivity (in early versus late incubation), each depending on different subcellular and cellular processes, affect lateralized behavior after hatching. Auditory and olfactory stimulation during embryonic development is also discussed with consideration of interactions with light-generated visual lateralization.

Brain Lateralization and Cognitive Capacity.

One way to increase cognitive capacity is to avoid duplication of functions on the left and right sides of the brain. There is a convincing body of evidence showing that such asymmetry, or lateralization, occurs in a wide range of both vertebrate and invertebrate species. Each hemisphere of the brain can attend to different types of stimuli or to different aspects of the same stimulus and each hemisphere analyses information using different neural processes. A brain can engage in more than one task at the same time, as in monitoring for predators (right hemisphere) while searching for food (left hemisphere). Increased cognitive capacity is achieved if individuals are lateralized in one direction or the other. The advantages and disadvantages of individual lateralization are discussed. This paper argues that directional, or population-level, lateralization, which occurs when most individuals in a species have the same direction of lateralization, provides no additional increase in cognitive capacity compared to individual lateralization although directional lateralization is advantageous in social interactions. Strength of lateralization is considered, including the disadvantage of being very strongly lateralized. The role of brain commissures is also discussed with consideration of cognitive capacity.

A function for the bicameral mind.

Why do the left and right sides of the brain have different functions? Having a lateralized brain, in which each hemisphere processes sensory inputs differently and carries out different functions, is common in vertebrates, and it has now been reported for invertebrates too. Experiments with several animal species have shown that having a lateralized brain can enhance the capacity to perform two tasks at the same time. Thus, the different specializations of the left and right sides of the brain seem to increase brain efficiency. Other advantages may involve control of action that, in Bilateria, may be confounded by separate and independent sensory processing and motor outputs on the left and right sides. Also, the opportunity for increased perceptual training associated with preferential use of only one sensory or motoric organ may result in a time advantage for the dominant side. Although brain efficiency of individuals can be achieved without the need for alignment of lateralization in the population, lateral biases (such as preferences in the use of a laterally-placed eye) usually occur at the population level, with most individuals showing a similar direction of bias. Why is this the case? Not only humans, but also most non-human animals, show a similar pattern of population bias (i.e., directional asymmetry). For instance, in several vertebrate species (from fish to mammals) most individuals react faster when a predator approaches from their left side, although some individuals (a minority usually ranging from 10 to 35%) escape faster from predators arriving from their right side. Invoking individual efficiency (lateralization may increase fitness), evolutionary chance or simply genetic inheritance cannot explain this widespread pattern. Using mathematical theory of games, it has been argued that the population structure of lateralization (with either antisymmetry or directional asymmetry) may result from the type of interactions asymmetric organisms face with each other.

Chicks prefer to peck at insect-like elongated stimuli moving in a direction orthogonal to their longer axis.

Spontaneous preferences towards possible prey have been little investigated using targets in motion. Preferences of domestic chicks (Gallus gallus) to peck at video-images of stimuli representing live insects moving along their longer body axis (i.e. "forwards") or along the shorter body axis (i.e. "sideways") were investigated. Chicks presented with both types of stimulus displayed a significant preference for pecking at stimuli moving sideways. This preference was already present on day 1 post-hatching, and it strengthened on day 6 for those chicks that had experienced pecking at live insects. Head angles used to fixate the stimuli prior to pecking were also analysed and were consistent (i.e. 30 degrees -35 degrees and 60 degrees -65 degrees ) with those reported for fixation of non-edible targets (larger stimuli at a distance). In a first control experiment the same video-presented stimuli were used but the insect's legs were removed to reduce flickering. In a second control experiment, paper-printed images of the whole insect were used. In both cases, the sideways direction of movement was clearly preferred. Overall, our data show that chicks have a spontaneous preference to peck at video-images resembling live insects moving along their shorter body axis. Sideways movement may constitute a crucial signal attracting chicks' attention and enhancing predatory responses possibly because of stronger stimulation of motion detectors.

Australian lungfish (Neoceratodus forsteri): a missing link in the evolution of complementary side biases for predator avoidance and prey capture.

Side biases in behavior, reflecting lateral specializations of the brain, are widespread amongst vertebrates. We studied laterality in the Australian lungfish (Neoceratodus forsteri) to gain insight into the evolution of the complementary specializations of predator avoidance (right hemisphere) and foraging behavior (left hemisphere). Because N. forsteri is the closest extant ancestor of the first land-dwelling vertebrates, knowledge of laterality in this species should provide a missing link in the transition from fish to tetrapods. Predator escape responses were elicited by generating pressure waves and a significant bias for C-start responses to the left side was found. This bias was unaffected by activity levels that change according to a diurnal cycle: activity is higher in the dark phase than the light phase. A complementary bias to turn to the right side was found during feeding behavior. This pattern of opposite-side specializations matches that known for fish, anurans, reptiles, birds and, as some evidence indicates, also mammals. Hence, we conclude that it is a homologous pattern of lateralization that evolved in early aquatic vertebrates and was retained as they made the transition to land-dwelling tetrapods.

Light exposure during incubation and social and vigilance behaviour of domestic chicks.

Light exposure of chick eggs during a sensitive period at the end of the incubation period leads to the development of lateralised visual behaviour, and here we show that social behaviour is also influenced by this exposure. Groups of eight chicks of three types-(1) all incubated in the dark (Da), (2) all exposed to light (Li), (3) half Da and half Li (Mixed)-were tested on a range of tasks involving social competition and vigilance for a simulated predator. We confirmed a previous finding that lowest-ranking chicks in Li groups gained less access to a food bowl when they had to compete with group members than did the lowest-ranking chicks in the Da groups, and we extended this result to show that the Mixed groups performed like the Li groups. We also showed that before presentation of a novel stimulus resembling a predator, fewer of the chicks in the Da groups than in the Li and Mixed groups looked up, but during presentation of the predator more Da than Li chicks looked up. Hence, light exposure before hatching affects post-hatching social and vigilance behaviour.

Complementary Specializations of the Left and Right Sides of the Honeybee Brain.

Honeybees show lateral asymmetry in both learning about odors associated with reward and recalling memory of these associations. We have extended this research to show that bees exhibit lateral biases in their initial response to odors: viz., turning toward the source of an odor presented on their right side and turning away from it when presented on their left side. The odors we presented were the main component of the alarm pheromone, isoamyl acetate (IAA), and four floral scents. The significant bias to turn toward IAA odor on the right and away from it on the left is, we argue, a lateralization of the fight-flight response elicited by this pheromone. It contrasts to an absence of any asymmetry in the turning response to an odor of the flowers on which the bees had been feeding prior to testing: to this odor they turned toward when it was presented on either the left or right side. Lemon and orange odors were responded to differently on the left and right sides (toward on the right, away on the left), but no asymmetry was found in responses to rose odor. Our results show that side biases are present even in the initial, orienting response of bees to certain odors.

Correlations between hand preference and cortical thickness in the secondary somatosensory (SII) cortex of the common marmoset, Callithrix jacchus.

Cortical asymmetries are well established in humans for language and motor regions and correlate with handedness. Here the authors investigate structural differences in the hemispheres of left- and right-handed common marmosets using surface photography and histology. The hand preferences of 11 marmosets were assessed over their adult life span using a simple reaching task. A significant correlation was found between the length of the right lateral sulcus/brain weight and the % right-hand preference (r = .86, p = .001). Cortical thickness on the superior bank of the right lateral sulcus posteriorly was also positively correlated with % right-hand preference (r = .69, p = .025). Comparison of this site with previously published functional maps of the marmoset cortex show this area corresponds to SII, a region involved in tactile processing and somatosensory discriminations. It is suggested that the correlation between SII thickness and right-hand preference would be consistent with the fact that right-handed marmosets are more proactive than left-handers in exploring novel objects by touch. Enlargement of a cortical area involved tactile discriminations could be a precursor to the evolution of right-handedness as a population bias.

Lateralized response of chicks to magnetic cues.

Previous research has shown that the ability to orient with the use of directional cues from the geomagnetic field is lateralized in three avian species: orientation is possible when the birds are restricted to use of their right eye, but not when they have to use their left eye. This has been interpreted as possible lateralization of the perception mechanisms for magnetic cues in favour of the right eye. Recent discovery of magnetic compass orientation in domestic chicks, a species in which lateralization has been well studied, has made available a model system in which to explore these lateralized processes more fully. Hence we tested chicks monocularly in the same test conditions as used previously to demonstrate the chick's use of a magnetic compass. In a magnetic field with North shifted by 90 degrees , chicks using their right eye oriented according to magnetic cues, whereas chicks using the left eye did not, but continued to prefer the original direction. Analysis of the times taken to respond indicated longer latencies in the chicks using their left eye, suggesting a possible conflict between cues. The different behaviour of the chicks using their left eye might not be a matter of a right eye-left hemisphere specialization for detecting magnetic directions, but of hemispheric specialization for attending to specific types of cues.

Visuospatial reaching preferences of common marmosets (Callithrix jacchus): an assessment of individual biases across a variety of tasks.

Using multiple measures of hand preference, the authors investigated lateralization at an individual level in 21 common marmosets. Despite showing group biases for sensory and communication functions, these same marmosets did not show a group bias in direction of lateralized hand use. Hand preferences were recorded on four novel reaching tasks requiring different levels of visual guidance and postural control. As found for simple food holding (with the same subjects), they displayed strong individual hand preferences but no group bias indicative of handedness. The strength of hand preference was influenced by task demands: stronger preferences were expressed when subjects adopted a suspended posture, and when "successful" versus "unsuccessful" foraging strategies were compared. Comparisons between visuospatial reaching and simple food holding preferences also revealed that half of the subjects displayed a division of function between the hands/hemispheres; subjects displayed opposing preferences in simple and visuospatial reaching, which would be beneficial for the performance of coordinated bimanual tasks. Given the apparent absence of a selective advantage for handedness, the authors suggest that hand preferences may reflect hemispheric dominance of other cognitive domains (i.e., temperament).

Howard I. Kushner's On the Other Hand: Left Hand, Right Brain, Mental Disorder, and History.

After a distinguished career as a professor at Emory University and San Diego State University, this left-handed author-whose mother was also a southpaw-examines left-handedness in the context of studies that have contested the classifications and meanings of disability, forcing researchers to re-examine their assumptions and attitudes about disability while challenging public policies aimed at them.

Manual bias, behavior, and cognition in common marmosets and other primates.

This chapter examines the importance of studying hand preference together with different expressions of behavior. Cognitive differences between left- and right-handed primates are discussed. As shown in several species of primate, eye preference, but not hand preference, is biased at the level of the population and reflects hemispheric asymmetry of processing. Hand preference, determined from simple grasping of pieces of food and taking them to the mouth, is consistent for individuals but it is not population biased. It is a measure of an individual's preference to use a particular hemisphere, and hence which cognitive processes are characteristic of the individual. Compared to left-handed subjects, right-handed subjects are more active in exploring novel objects, show more social facilitation of behavior, have a positive cognitive bias, and express lower levels of fear and stress responses. In marmosets, learning of food searching tasks is not associated with hand preference. Strength of hand preference, rather than its direction, is linked to the ability to perform two tasks at once, viz., detection of a predator while searching for food. Marmosets with strong hand preferences are able to perform these two tasks at once but those with weak or no hand preference are unable to do so.

Food Calls in Common Marmosets, Callithrix jacchus, and Evidence That One Is Functionally Referential.

We studied three calls of common marmosets, Callithrix jacchus, elicited in the context of food. Call A, but not B or C, had been described previously as a food call. We presented insects (live mealworms or crickets) and fruit (banana or blueberries) and used playbacks of calls. We found that Call C was produced only in response to seeing insects, and not fruit; it consistently signaled the availability of insects (includes mealworms), and more so when this food could be seen but not consumed. Playback of Call C caused the marmosets to stop feeding on a less preferred food (banana) and, instead, go to inspect a location where mealworms had been found previously, providing evidence that it has referential meaning. No such immediate response was elicited on hearing Call A or background noise. Call A differed from C in that it was produced more frequently when the marmosets were consuming the food than when they could only see it, and call A showed no specificity between insects and fruit. Call B was emitted less frequently than the A or C calls and, by the marmosets that were tested alone, most often to crickets. An audience effect occurred, in that all three calls were emitted more often when the marmosets were tested alone than when in pairs. Recognition of the functional significance of marmoset calls can lead to improved husbandry of marmosets in captivity.