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).     

Relationship between paw preference strength and noise phobia in Canis familiaris

The authors investigated the relationship between degree of lateralization and noise phobia in 48 domestic dogs (Canis familiaris) by scoring paw preference to hold a food object and relating it to reactivity to the sounds of thunderstorms and fireworks, measured by playback and a questionnaire. The dogs without a significant paw preference were significantly more reactive to the sounds than the dogs with either a left-paw or right-paw preference. Intense reactivity, therefore, is associated with a weaker strength of cerebral lateralization. The authors note the similarity between their finding and the weaker hand preferences shown in humans suffering extreme levels of anxiety and suggest neural mechanisms that may be involved.     

Posturally related variations in the hand preferences of the ruffed lemur (Varecia variegata variegata)

The hand preferences of 5 semi-free-ranging black-and-white ruffed lemurs were assessed by using three distinct testing procedures. Testing conditions varied in the extent to which they required animals to make a whole body postural adjustment prior to making a reach. Minimal bodily adjustment was necessary for free foraging, whereas discrete food presentations on land (DFP-land) and in a moat (DFP-moat) promoted a gross reorientation of the animal's entire body. In the DFP-moat condition 4 animals exhibited exclusive use of the left hand, and only 1 of 515 reaches was made with the right hand. Similarly, all 5 animals showed a pronounced left hand preference in the DFP-land condition. The free-foraging condition revealed a hand preference for only 1 of the 5 subjects, and that preference was weak in comparison with those measured in the other two test conditions. These findings indicate that whole body postural adjustments critically influenced the expression of hand preference and should be taken into consideration in future studies of primate hand preferences.     

Development of hand preferences in marmosets (Callithrix jacchus) and effects of aging

The authors investigated the development of unimanual hand use and hand preferences during feeding in 15 marmosets (Callithrix jacchus), ages birth to 51-70 months. Bimanual hand use was common at 1-2 months, but by 5-8 months unimanual holding had developed and so had significant hand preferences. Half of the marmosets preferred to pick up and take food to the mouth with the left hand, and half preferred the right hand. Individuals maintained the same hand preference at all ages examined. Significant relationships were also found between the postures adopted during feeding and the direction of hand preferences displayed by juvenile marmosets. There was a positive correlation between increased suspension and increased left-hand preference, and a negative correlation between increased feeding in a tripedal posture and increased left-hand preference. These results are discussed in terms of motor development and hemispheric specialization.     

Adapting chronometric tests for field studies of cognitive ability

This study was designed to examine the relationship of hand preference to performance on a thumb-positioning task. Two hypotheses were proposed on the basis of hemispheric lateralization. The first stated that all subjects would perform the task more accurately using the left thumb, regardless of hand preference. The second hypothesis tested was that left-handed subjects would perform more accurately than right-handed subjects. Each of 20 neurologically intact adults grouped by hand preference reproduced a criterion thumb position with both thumbs simultaneously. Absolute error, recorded for each movement and analyzed by mixed analysis of variance, did support the first hypothesis. However, the left-handed group did not perform statistically differently from right-handed subjects. Factors influencing the data are discussed and recommendations for further studies are made.     

Hand preferences in unimanual and bimanual feeding by wild vervet monkeys (Cercopithecus aethiops)

Lateral preference was examined in spontaneous feeding actions in 2 troops of wild vervet monkeys (Cercopithecus aethiops). Processing of 4 foods (termites, leaf shoots, sugarcane, and fruit) was studied. Actions included unimanual reaching to moving objects, operating from an unstable posture, and coordinated bimanual processing. Between 19 and 31 subjects were available, according to the task. In 2 tasks, laterality of 2 independent stages was measured separately, giving 6 measures in all. On 4 of these measures, most monkeys were ambipreferent, and only a few showed significant hand preferences. Only for termite feeding and detaching material from fruits did the majority show significant lateralization; no tasks elicited exclusive use of 1 hand. Preference appeared labile, because in 2 tasks, population trends reversed with increasing age. No population trends to left or right were found; instead, these monkeys showed ambilaterality, with lateralization associated with task complexity.     

Note on hand use in the manipulation of joysticks by rhesus monkeys (Macaca mulatta) and chimpanzees (Pan troglodytes)

In a recent article MacNeilage, Studdert-Kennedy, and Lindblom (1987) proposed that nonhuman primate handedness may be contingent on the specific task requirements with visual-spatial tasks yielding left-hand preferences and fine motor tasks producing right-hand preferences. This study reports hand preferences in the manipulation of joysticks by 2 rhesus monkeys (Macaca mulatta) and 3 chimpanzees (Pan troglodytes). Reach data were also collected on these same subjects and served as a basis for comparison with preference data for manipulation of the joystick. The data indicated that all 5 subjects demonstrated significant right-hand preferences in manipulating the joystick. In contrast, no significant hand preferences were found for the reach data. Reaction time data also indicated that the right hand could perform a perceptual-motor task better than the left hand in all 5 subjects. Overall, the data indicate that reach tasks may not be sensitive enough measures to produce reliable hand preferences, whereas tasks that assess fine motor control produce significant hand preferences.     

Parallel working memory for spatial location and food-related object cues in foraging pigeons: binocular and lateralized monocular performance

During foraging, animals can increase their success by both remembering feeding sites and remembering food-related object cues. Because earlier studies have tested either the site or object memory in isolation, the aim of the present study was to evaluate how efficiently birds can utilize both memories simultaneously. Furthermore, the idea was tested that lateralization might be the principle of brain organization that allows for efficient parallel processing. Pigeons learned to search for food in a complex maze with 16 baited sites. To obtain the maximum reward they had to perform two tasks in parallel, a spatial working memory task and an object-specific working memory task. Birds performed well on this dual task but, compared with spatial working memory alone, they were impaired during the first choices of a trial (Experiment 1). When the left and the right brain hemispheres were tested separately by means of monocular occlusion (Experiment 2), object discrimination was better when birds used their right eye/left hemisphere. This was most pronounced during the first choices of a trial. On the spatial component of the task, performance on binocular trials was better than on monocular trials, but monocularly both hemispheres performed at the same level. Results show that on this dual task, discrimination of food-related object cues predominantly involved the left brain hemisphere whereas both hemispheres contributed equally to spatial performance.     

Eye preferences in captive chimpanzees

Over the last century, the issue of brain lateralization in primates has been extensively investigated and debated, yet no previous study has reported eye preference in great apes. This study examined eye preference in 45 captive chimpanzees (Pan troglodytes) in response to various stimuli. Eye preference was assessed when animals looked through a hole that only accommodated one eye at an empty box, a mirror, a picture of a dog, a rubber snake, food biscuits, bananas, a rubber duck, and a video camera. Main effects of stimulus type were found for direction of eye preference, number of looks, and looking duration, but not for strength of eye preference. A left-eye bias was found for viewing the rubber snake and a right-eye bias was found for viewing the bananas, supporting theories that emotional valence may affect lateralized behaviors. In addition, a significant shift in eye preference took place from the initial look to subsequent looks when viewing the snake. These results are not consistent with previous reports of human eye preference and may reflect lateralization differences for emotional processing. No relationship between eye preference and previously recorded hand preference was found.     

Intermanual differences on neuropsychological motor tasks in a Japanese university student sample

We explored the intermanual difference scores of 128 Japanese university students for five typical neuropsychological motor tasks (grip strength, finger tapping, two versions of the grooved pegboard, and the dot‐filling test) and examined the relation between hand preference and intermanual difference in motor proficiency. Using the Edinburgh Handedness Inventory, 18 and 110 participants were identified as left‐ and right‐handed, respectively. Although the right hand performed better than the left for right‐handed participants, and vice versa, in all five tasks, the degree of intermanual difference varied between tasks. A discriminant function analysis using the laterality quotients of the five motor tasks as independent variables indicated that hand preference was predictable from the task performances with an accuracy of 90% or more. The dot‐filling test and finger tapping had stronger canonical loadings than the other tasks.     

Evolution of hemispheric specialization: advantages and disadvantages

Lateralization of the brain appeared early in evolution and many of its features appear to have been retained, possibly even in humans. We now have a considerable amount of information on the different forms of lateralization in a number of species, and the commonalities of these are discussed, but there has been relatively little investigation of the advantages of being lateralized. This article reports new findings on the differences between lateralized and nonlateralized chicks. The lateralized chicks were exposed to light for 24 h on day 19 of incubation, a treatment known to lead to lateralization of a number of visually guided responses, and the nonlateralized chicks were incubated in the dark. When they were feeding, the lateralized chicks were found to detect a stimulus resembling a raptor with shorter latency than nonlateralized chicks. This difference was not a nonspecific effect caused by the light-exposed chicks being more distressed by the stimulus. Instead, it appears to be a genuine advantage conferred by having a lateralized brain. It is suggested that having a lateralized brain allows dual attention to the tasks of feeding (right eye and left hemisphere) and vigilance for predators (left eye and right hemisphere). Nonlateralized chicks appear to perform these dual tasks less efficiently than lateralized ones. Reference is made to other species in discussing these results.     

Human gestures trigger different attentional shifts in chimpanzees (Pan troglodytes) and humans (Homo sapiens)

Brain lateralization has been the matter of extensive research over the last centuries, but it remains an unsolved issue. While hand preferences have been extensively studied, very few studies have investigated laterality of eye use in non-human primates. We examined eye preference in 14 Campbell’s monkeys (Cercopithecus c. campbelli). We assessed eye preference to look at a seed placed inside a tube using monocular vision. Eye use was recorded for 100 independent and non-rewarded trials per individual. All of the 14 monkeys showed very strong preferences in the choice of the eye used to look inside the tube (mean preference: 97.6%). Eight subjects preferred the right eye and six subjects preferred the left eye. The results are discussed in light of previous data on eye preference in primates, and compared to data on hand preference from these subjects. Our findings would support the hypothesis for an early emergence of lateralization for perceptual processes compared to manual motor functions.     

Damage-induced alarm cues influence lateralized behaviour but not the relationship between behavioural and habenular asymmetry in convict cichlids (<Emphasis Type="Italic">Amatitlania nigrofasciata</Emphasis>)

Cerebral lateralization, the partitioning of functions into a certain hemisphere of the brain, is ubiquitous among vertebrates. Evidence suggests that the cognitive processing of a stimulus is performed with a specific hemisphere depending in part upon the emotional valence of the stimulus (i.e. whether it is appetitive or aversive). Recent work has implicated a predominance of right-hemisphere processing for aversive stimuli. In fish with laterally placed eyes, the preference to view an object with a specific eye has been used as a proxy for assessing cerebral lateralization. The habenula, one of the most well-known examples of an asymmetrical neural structure, has been linked to behavioural asymmetry in some fish species. Here, we exposed convict cichlid fish (Amatitlania nigrofasciata) to both a social and non-social lateralization task and assessed behavioural lateralization in either the presence or absence of an aversive stimulus, damage-induced alarm cues. We also assessed whether behavioural asymmetry in these tests was related to asymmetry of the habenular nuclei. We found that when alarm cues were present, fish showed increased left-eye (and by proxy, right hemisphere) preference for stimulus viewing. In addition, females, but not males, showed stronger eye preferences when alarm cues were present. We did not find a relationship between behavioural lateralization and habenular lateralization. Our results conflict with previous reports of concordance between behavioural and habenular lateralization in this fish species. However, our results do provide support for the hypothesis of increased right-hemisphere use when an organism is exposed to aversive stimuli.     

The development of hand preference in children: The effect of task demands and links with manual dexterity

Lateralisation of hand preference and manual dexterity are known to develop over childhood, while in adulthood strength of hand preference has been shown to interact with extrinsic task demands. Some evidence exists to suggest that strength of hand preference and motor skill may be related. In the current study a handedness inventory, midline crossing (QHP) and peg-moving tasks were used to investigate: (1) the development of hand preference between 4 and 11 years; (2) whether extrinsic task demands affect strength of hand preference, and (3) whether strength of hand preference was associated with manual dexterity. Younger children (4–5 years) showed weak hand preference in comparison to older children (8–11 years), and extrinsic task demands influenced willingness to cross the body’s midline with the preferred hand. Age and peg-moving speed were associated with midline crossing in certain task conditions. Overall, results suggest a coupling between manual dexterity and brain maturation in typical development.     

Manual laterality in nonhuman primates: a distinction between handedness and manual specialization

This article examines individual and group manual lateralization in nonhuman primates as a function of task's demands. It is suggested to distinguish low- from high-level manual activities with respect to the novelty variable and to the spatiotemporal scale of the movements. This review shows that low-level tasks lead to (a) symmetrical distributions of hand biases for the group and (b) manual preferences that are not indicative of the specialization of the contralateral hemisphere. In contrast, behaviors expressed in high-level tasks (a) show asymmetrical distribution of hand biases for the group and (b) seem to be related to a specialization of the contralateral hemisphere. Two types of lateralization, handedness and manual specialization, correspond to the 2 levels of tasks that are distinguished.     

Behavioral asymmetries of psychomotor performance in rhesus monkeys (Macaca mulatta): a dissociation between hand preference and skill.

Hand preferences were recorded for 35 rhesus monkeys (Macaca mulatta) as they manipulated a joystick in response to 2 computerized tasks. These preferences were then used to contrast 8 left- and 10 right-handed subjects on performance measures of hand skill. Individual hand preferences were found, but no significant population asymmetry was observed across the sample. However, the performance data reveal substantial benefits of right-handedness for joystick manipulation, as this group of monkeys mastered the 2 psychomotor tasks significantly faster than did their left-handed counterparts. The data support earlier reports of a right-hand advantage for joystick manipulation and also support the importance of distinguishing between hand preference and manual performance in research on functional asymmetries.     

Performance on the Hamilton search task,and the influence of lateralization,in captive orange-winged Amazon parrots (Amazona amazonica)

Psittacines are generally considered to possess cognitive abilities comparable to those of primates. Most psittacine research has evaluated performance on standardized complex cognition tasks, but studies of basic cognitive processes are limited. We tested orange-winged Amazon parrots (Amazona amazonica) on a spatial foraging assessment, the Hamilton search task. This task is a standardized test used in human and non-human primate studies. It has multiple phases, which require trial and error learning, learning set breaking, and spatial memory. We investigated search strategies used to complete the task, cognitive flexibility, and long-term memory for the task. We also assessed the effects of individual strength of motor lateralization (foot preference) and sex on task performance. Almost all (92 %) of the parrots acquired the task. All had significant foot preferences, with 69 % preferring their left foot, and showed side preferences contralateral to their preferred limb during location selection. The parrots were able to alter their search strategies when reward contingencies changed, demonstrating cognitive flexibility. They were also able to remember the task over a 6-month period. Lateralization had a significant influence on learning set acquisition but no effect on cognitive flexibility. There were no sex differences. To our knowledge, this is the first cognitive study using this particular species and one of the few studies of cognitive abilities in any Neotropical parrot species.     

Does Octopus vulgaris have preferred arms?

Previous behavioral studies in Octopus vulgaris revealed lateralization of eye use. In this study, the authors expanded the scope to investigate arm preferences. The octopus's generalist hunting lifestyle and the structure of their arms suggest that these animals have no need to designate specific arms for specific tasks. However, octopuses also show behaviors, like exploration, in which only single or small groups of arms are involved. Here the authors show that octopuses had a strong preference for anterior arm use to reach for and explore objects, which points toward a task division between anterior and posterior arms. Four out of 8 subjects also showed a lateral bias. In addition, octopuses had a preference for a specific arm to reach into a T maze to retrieve a food reward. These findings give evidence for limb-specialization in an animal whose 8 arms were believed to be equipotential.     

Can wild common marmosets (Callithrix jacchus) solve the parallel strings task?

Patterned string tasks are a test of perceptual capacity and the understanding of means-end connections. Primates can solve complex forms of this task in laboratories. However, this may not indicate the level of such cognition that is commonly employed in the wild, where decision-making time is often short and distractions such as predator avoidance and competition between conspecifics are often prevalent. The current study tests whether wild common marmosets (Callithrix jacchus) can successfully complete the simplest form of the patterned string task, parallel strings, while in their natural environment. Although 12 out of 13 marmosets could successfully complete the task, in previous laboratory-based studies on primates, the errors at this task by all primate species tested were consistently lower than in the present study. This is probably explained by the added difficulties imposed by the natural setting of the task in the present study, exemplified by a significant increase in observed vigilance behaviour by subject animals prior to attempts at the task that were unsuccessful. The undertaking of such tasks by common marmosets in situ probably provides a more reasonable representation of the levels of cognitive capacity expressed by this species in the wild than do laboratory-based studies of the task.     

Eye as a key element of conspecific image eliciting lateralized response in fish

Visual lateralization in different aspects of social behaviour has been found for numerous species of vertebrates ranging from fish to mammals. For inspection of a shoal mate, many fishes show a left eye–right hemisphere preference. Here, we tested the hypothesis that in fish, there is a key cue in the conspecific appearance, which elicits lateralized response to the whole image of the conspecific. In a series of eight experiments, we explored eye preferences in cryptic-coloured Amur sleeper, Perccottus glenii, fry. Fish displayed left-eye preferences at the population level for inspection of a group of conspecifics, their own mirror image, and a motionless flat model of a conspecific. In contrast, no population bias was found for scrutinizing an empty environment or a moving cylinder. When fry were showed a model of a conspecific in a lateral view with the eye displaced from the head to the tail, they again showed a significant preference for left-eye use. On the other hand, ‘eyeless’ conspecific model elicited no lateralized viewing in fry. Finally, the left-eye preference was revealed for scrutiny of the image of a conspecific eye alone. We argue that in Amur sleeper fry, eye is the element of the conspecific image, which can serve as a ‘key’ for the initiation of lateralized social response. This key element may serve as a trigger for the rapid recognition of conspecifics in the left eye–right hemisphere system. Possible causes and advantages of lateralized perception of social stimuli and their key elements are discussed in the context of current theories of brain lateralization.