Amandine Chapelain

Manual laterality in Campbell's Monkeys (Cercopithecus c. campbelli) in spontaneous and experimental actions

Behavioural asymmetries, once thought to be exclusively human, appear to be widespread in vertebrates. A population-level bias should stem from natural selection and reflect a cerebral dominance, while individual preferences might be linked to individual characteristics. Manual laterality has been extensively investigated in non-human primates. However, despite a strong data base, no general patterns have emerged, resulting in a few explanatory theories and little consensus. This study was interested in manual laterality in 12 Campbells monkeys (Cercopithecus c. campbelli). Several theories were examined, using both direct behavioural observations during feeding behaviour and six controlled experimental conditions, in which we varied task demands to investigate the effect of two factors. We systematically varied the individual posture (sat, tripedal, bipedal, clung) and the complexity of the task (box with or without a lid to open). Concerning the direction of preference, we found individual and action-specific preferences for experimental actions, which match previous reports. No population bias emerged and each subject appeared to react differently to the factors, hereby contradicting the theories. However, concerning the strength of preference, all individuals tended to be affected in similar ways. Spontaneous actions were less lateralized than experimental ones, and the simplest task and spontaneous category tended to show the weakest laterality. The relative complexity and novelty of these actions may account for these results.

Hand Preferences for Bimanual Coordination in 77 Bonobos (Pan paniscus): Replication and Extension

The literature on manual laterality in nonhuman primates provides inconsistent and inconclusive findings and is plagued by methodological issues (e.g., small samples, inconsistency in methods, inappropriate measures) and gaps. Few data are available on bonobos and these are only from small samples and for relatively simple tasks. We examined laterality in a large sample of bonobos for a complex task. We tested 48 bonobos from Lola Ya Bonobo sanctuary (DR Congo) in an extension of our previous study of 29 bonobos from 3 European zoos. We assessed hand preferences using the tube task, which involves bimanual coordination: one hand extracts food from a tube that is held by the other hand. This task is a good measure of laterality and it has been used in other studies. We recorded events (frequency) and independent bouts of food extraction. We found significant manual laterality, which was not influenced by the settings or rearing history. We observed little effect of sex and found an influence of age, with greater right hand use in adults. The laterality was marked, with strong preferences and most individuals being lateralized (when analyzing frequency). We found individual preferences, with no group-level bias, even when we combined the data from the sanctuary and the zoos to enlarge the sample to 77. These first data, for a complex task and based on a large sample, are consistent with previous findings in bonobos and in other nonhuman primate species for a variety of tasks. They suggest that, despite particular features in terms of proximity to humans, language and bipedalism, bonobos do not display a laterality that is more marked or more similar to human handedness compared to that of other nonhuman primate species.

Lateralization for visual processes: eye preference in Campbell’s monkeys (Cercopithecus c. campbelli)

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.

How should “ambidexterity” be estimated?

Weak and absent hand preferences have often been associated with developmental disorders or with cognitive functioning in the typical population. The results of different studies in this area, however, are not always coherent. One likely reason for discrepancies in findings is the diversity of cut-offs used to define ambidexterity and mixed right- and mixed left-handedness. Establishing and applying a common criterion would constitute an important step on the way to producing systematically comparable results. We thus decided to try to identify criteria for classifying individuals ambidextrous, mixed right- or left-handed or strong right- or left-handed. For that purpose, we first administered a handedness questionnaire to 716 individuals and performed multiple correspondence analyses to define handedness groups. Twenty-four participants were categorized as ambidextrous (3.3%), as opposed to mixed (29.2%) and strong (56%) right-handers, and to mixed (9.1%) and strong (2.4%) left-handers. We then compared this categorization with laterality index (LI)-based categories using different cut-offs and found that it was most correlated with LI cut-offs at −90, −30, +30 and +90, successively delimiting strong left-handedness, mixed left-handedness, ambidexterity (−30 to +30), mixed right-handedness and strong right-handedness. The characteristics of ambidextrous and lateralized individuals are also compared.

Can Population-Level Laterality Stem from Social Pressures? Evidence from Cheek Kissing in Humans

Despite extensive research, the origins and functions of behavioural laterality remain largely unclear. One of the most striking unresolved issues is the fact that laterality generally occurs at the population-level. Why would the majority of the individuals of a population exhibit the same laterality, while individual-level laterality would yet provide the advantages in terms of improving behavioural efficiency? Are social pressures the key factor? Can social pressures induce alignment of laterality between the individuals of a population? Can the effect of social pressures overpass the effect of other possible determining factors (e.g. genes)? We tested this important new hypothesis in humans, for the first time. We asked whether population-level laterality could stem from social pressures. Namely, we assessed social pressures on laterality in an interactive social behaviour: kissing on the cheek as a greeting. We performed observations in 10 cities of France. The observations took place in spots where people of the city meet and greet each other. We showed that: a) there is a population-level laterality for cheek kissing, with the majority of individuals being aligned in each city, and b) there is a variation between populations, with a laterality that depends on the city. These results were confirmed by our complementary data from questionnaires and internet surveys. These findings show that social pressures are involved in determining laterality. They demonstrate that population-level laterality can stem from social pressures.

Hand preference and its flexibility according to the position of the object: a study in cercopithecines examining spontaneous behaviour and an experimental task (the Bishop QHP task)

The extant literature on manual laterality in non-human primates is inconclusive, plagued by inconsistent or contradictory findings and by disturbing methodological issues (e.g. uncontrolled influential factors, comparability issues). The present study examined hand preference and its flexibility in 15 red-capped mangabeys (C. t. torquatus) and 13 Campbell’s monkeys (C. c. campbelli), two species that differ in their degree of arboreality. We investigated the influence of the spatial position of the object on hand preference for reaching. We considered spontaneous behaviour (reaching for food during daily feeding) and an experimental task: the QHP task. The QHP is a task that is used in humans. This is a simple reaching task that involves high spatial constraints on hand use. In our study, the subject had to reach for items that were placed on a semi-circle in front of it on five positions, including in the centre position, in the ipsilateral space and in the contralateral space. We assessed hand preference for reaching in front (baseline condition), and we examined how this preference changed when reaching in lateral positions. For reaching in front, about half of the subjects were lateralized and no group-level bias occurred, for both spontaneous and experimental conditions. When considering reaching in the lateral positions, we observed that the position of the object influenced hand use: individuals used the hand that was closest to the object. The results are discussed in relation to previous findings in humans and in non-human primates and regarding theories on handedness and flexibility of hand preference.

Handedness for Unimanual Grasping in 564 Great Apes: The Effect on Grip Morphology and a Comparison with Hand Use for a Bimanual Coordinated Task

A number of factors have been proposed to influence within and between species variation in handedness in non-human primates. In the initial study, we assessed the influence of grip morphology on hand use for simple reaching in a sample of 564 great apes including 49 orangutans Pongo pygmaeus, 66 gorillas Gorilla gorilla, 354 chimpanzees Pan troglodytes and 95 bonobos Pan paniscus. Overall, we found a significant right hand bias for reaching. We also found a significant effect of the grip morphology of hand use. Grasping with the thumb and index finger was more prevalent in the right compared to left hand in all four species. There was no significant sex effect on the patterns of handedness. In a subsample of apes, we also compared consistency in hand use for simple reaching with previously published data on a task that measures handedness for bimanual actions. We found that the ratio of subjects with consistent right compared to left hand use was more prevalent in bonobos, chimpanzees and gorillas but not orangutans. However, for all species, the proportion of subjects with inconsistent hand preferences between the tasks was relatively high suggesting some measures may be more sensitive in assessing handedness than others.

Manual laterality for pointing gestures compared to grasping actions in guenons and mangabeys

In both humans and apes, the production of communicative gestures appears to be controlled by cerebral structures in the left hemisphere that would be distinct from those involved in noncommunicative actions. Whether communicative gestures also rely on specific lateralized systems in monkeys remains unclear. We assessed manual laterality for requesting gestures, i.e. pointing, and for grasping actions in two species of Old World monkeys, Campbells monkeys, Cercopithecus campbelli, and red-capped mangabeys, Cercocebus torquatus, using the Bishop QHP task. The food items were placed at five positions in front of the monkeys and they were located at out-of-reach, far or close distance from the monkeys, to induce pointing gestures and grasping actions requiring full or low arm extensions, respectively. The mangabeys that exhibited the greatest skills for pointing referentially were more right-handed for pointing gestures than for grasping actions. We propose that in Old World monkeys, as in humans and apes, the production of intentional and referential gestures may rely on the activation of specific regions of the left hemisphere specialized in the processing of communicative signals. Subjects from both species preferred to use the hand that was closest to the item for grasping actions requiring low arm extension whereas they used the contralateral hand for grasping actions requiring full arm extension and pointing gestures. These results are discussed in relation to hypotheses on postural control and arboreality.

Correction: Can Population-Level Laterality Stem from Social Pressures? Evidence from Cheek Kissing in Humans

[This corrects the article DOI: 10.1371/journal.pone.0124477.].