Hand Preference In Nonhuman Primates Research Articles

Development of Hand and Paw Preferences and Their Association with Other Patterns of Behaviour and Cognition

Hand preference in non-human primates has been studied extensively with the aim of understanding the evolution of hemispheric asymmetry and hand preferences in humans. However, the focus has been on hand preferences expressed in adulthood, with a surprising lack of studies on hand preferences in infants and changes that occur during the development of other, potentially associated, asymmetries in the brain and behaviour. This paper reports on the development of hand preference for grasping food and taking it to the mouth in common marmosets. It considers the development of other types of behaviour, such as head cocking and anogenital licking, that parallel and might influence the development of hand preferences during the first months of life. It then discusses behavioural differences between left- and right-handed adult marmosets, including response to novel stimuli, social behaviour and cognitive bias. The need to study the development of hand preferences together with the development of these other expressions of cognitive function is highlighted. The question to be addressed by empirical studies is whether hand preference is a downstream manifestation of the development of hemispheric differences in sensory processing and cognition, or whether it is instrumental in the development of functional differences between the hemispheres. Comparison is made to paw preference and associated behaviour in non-primate species.

Lion-tailed macaques show a stable direction and reinforcement of hand preference in simple reaching tasks over several years

Research on hand preference in non-human primates provides information about the evolutionary origin of population-level bias of human handedness. Human hand preference has been shown to remain stable throughout an individual's lifespan. However, the stability of hand preference and its change with age in non-human primates remains questionable. We recorded hand use in lion-tailed macaques (Macaca silenus) during simple reaching tasks in three time periods over six years. We tested the effect of age and body posture on the direction and strength of hand preference in 23 observed individuals. In a subsample of 13 individuals followed for two or three subsequent time periods, we assessed the stability of hand preference across study periods. The direction of hand preference was highly stable; we detected no individuals changing from a left- to right-, or right- to left- preference and repeated quantitative measures of hand preference were correlated among subsequent study periods. Hand preference was, however, reinforced in older individuals and an individual's hand preference was stronger in postures with both hands free for foraging. Stable hand preference at an individual level, and its reinforcement over an individual's lifetime, is emerging as a robust finding across the primate order.

Hand preference in unimanual and bimanual coordinated tasks in wild western lowland gorillas (Gorilla gorilla gorilla) feeding on African ginger (Zingiberaceae).

Bimanual coordinated behaviors are critical for detecting robust individual hand preference in nonhuman primates but are particularly challenging to observe in the wild. This study focuses on spontaneous feeding behavior on African ginger (Aframomum sp. and Renealmia sp.), which involves a unimanual task (reaching and pulling out a ginger stem) and a bimanual coordinated task (extracting pith from a ginger stem) by wild western lowland gorillas. Study subjects were 21 gorillas in the Moukalaba-Doudou National Park, Gabon. We examined whether they exhibit significant hand preference at the individual and group levels for both tasks. Sixteen gorillas showed significant hand preference in the unimanual task, whereas all 21 individuals showed significant hand preference in the bimanual coordinated task. Hand preference was significantly stronger in the bimanual coordinated task than in the unimanual task. It is noteworthy that gorillas showed a significant right-hand preference at the group level for the bimanual task (roughly 70% of the subjects). This study confirmed that bimanual coordinated tasks are more sensitive in detecting hand preferences in nonhuman primates. In addition to the bimanual nature of the task, the precision grip for processing and the importance of African ginger as a food resource might influence the expression of hand preference. Evidence of a group-level right-hand preference may support the "postural origins theory." Because all wild African great apes feed on the pith of African ginger, comparing this task and its hand preferences can contribute toward a better understanding of the evolution of handedness in Hominidae.

Handedness in monkeys reflects hemispheric specialization within the central sulcus. An in vivo MRI study in right- and left-handed olive baboons

Handedness, one of the most prominent expressions of laterality, has been historically considered unique to human. This noteworthy feature relates to contralateral inter-hemispheric asymmetries in the motor hand area following the mid-portion of the central sulcus. However, within an evolutionary approach, it remains debatable whether hand preferences in nonhuman primates are associated with similar patterns of hemispheric specialization. In the present study conducted in Old world monkeys, we investigate anatomical asymmetries of the central sulcus in a sample of 86 olive baboons (Papio anubis) from in vivo T1 anatomical magnetic resonance images (MRI). Out of this sample, 35 individuals were classified as right-handed and 28 as left-handed according to their hand use responses elicited by a bimanual coordinated tube task. Here we report that the direction and degree of hand preference (left or right), as measured by this manual task, relates to and correlates with contralateral hemispheric sulcus depth asymmetry, within a mid-portion of the central sulcus. This neuroanatomical manifestation of handedness in baboons located in a region, which may correspond to the motor hand area, questions the phylogenetic origins of human handedness that may date back to their common ancestor, 25–40 millions years ago.

Effects of age, sex and manual task on hand preference in wild Rhinopithecus roxellana.

Golden snub-nosed monkeys (Rhinopithecus roxellana), as typical arboreal group-living Old World monkeys, provide an appropriate animal model to research manual laterality and explore the factors affecting hand preference in non-human primates (NHP). This study investigated hand preference based on 63 subjects and four spontaneous manual tasks (including unimanual and bimanual feeding and grooming), and assessed the effects of age, gender and type of task on handedness in R. roxellana. A population-level left-handedness was found not only in the bimanual coordinated tasks (bimanual feeding and grooming), but also in one unimanual reaching task (unimanual feeding). There were no significant differences between the sexes in either direction or strength of hand preference among any task. However, a significant difference between adults and juveniles was found in the unimanual feeding task. This is the first report on handedness in unimanual and bimanual feeding tasks that require bipedal posture in wild R. roxellana. Furthermore, this study demonstrated spontaneous feeding tasks reported previously only in the quadrupedal posture in this species, supporting the importance of factors such as posture and task complexity in the evolution of primate manual lateralization.

Preliminary study on hand preference in captive northern white-cheeked gibbons (Nomascus leucogenys).

The postural origin hypothesis and the task complexity hypothesis propose that hand preference in non-human primates evolved in association with body posture and task complexity, respectively. The results of previous studies testing these two hypotheses, however, vary greatly with the different primate species and methods used. To investigate the effect of body posture and task complexity on hand preference, we recorded bouts of hand usage in nine captive northern white-cheeked gibbons (Nomascus leucogenys) housed at Beijing Zoo as they reached for food items in a ground-reaching task, a box task, and a tube task. The results showed that four to seven of the nine gibbons displayed a hand preference at the individual level in different tasks, and that hand preference in individuals was task-specific; there was no group-level hand preference in any task. The box task seemed to elicit a greater strength of hand preference than the ground-reaching task at the individual level. Although the small sample size rules out drawing any strong conclusions concerning hand preference at the group level, our results suggest that the suspensory reaching posture might increase the expression of hand preference at the individual level. This study provides preliminary information on hand preference in captive northern white-cheeked gibbons, and will be helpful for future studies addressing the origin and evolution of hand preference in small apes.

A comparative assessment of hand preference in captive red howler monkeys, Alouatta seniculus and yellow-breasted capuchin monkeys, Sapajus xanthosternos.

There are two major theories that attempt to explain hand preference in non-human primates–the ‘task complexity’ theory and the ‘postural origins’ theory. In the present study, we proposed a third hypothesis to explain the evolutionary origin of hand preference in non-human primates, stating that it could have evolved owing to structural and functional adaptations to feeding, which we refer to as the ‘niche structure’ hypothesis. We attempted to explore this hypothesis by comparing hand preference across species that differ in the feeding ecology and niche structure: red howler monkeys, Alouatta seniculus and yellow-breasted capuchin monkeys, Sapajus xanthosternos. The red howler monkeys used the mouth to obtain food more frequently than the yellow-breasted capuchin monkeys. The red howler monkeys almost never reached for food presented on the opposite side of a wire mesh or inside a portable container, whereas the yellow-breasted capuchin monkeys reached for food presented in all four spatial arrangements (scattered, on the opposite side of a wire mesh, inside a suspended container, and inside a portable container). In contrast to the red howler monkeys that almost never acquired bipedal and clinging posture, the yellow-breasted capuchin monkeys acquired all five body postures (sitting, bipedal, tripedal, clinging, and hanging). Although there was no difference between the proportion of the red howler monkeys and the yellow-breasted capuchin monkeys that preferentially used one hand, the yellow-breasted capuchin monkeys exhibited an overall weaker hand preference than the red howler monkeys. Differences in hand preference diminished with the increasing complexity of the reaching-for-food tasks, i.e., the relatively more complex tasks were perceived as equally complex by both the red howler monkeys and the yellow-breasted capuchin monkeys. These findings suggest that species-specific differences in feeding ecology and niche structure can influence the perception of the complexity of the task and, consequently, hand preference.

Do right-handed monkeys use the right cheek pouch before the left?

There can be several factors that are likely to have played a role in the evolution of hand preference in humans and non-human primates, which the existing theories do not consider. There exists a possibility that hand preference in non-human primates evolved from the pre-existing lateralities in more elementary brain functions and behavior, or alternatively, the two coevolved. A basic example can be a hand-mouth command system that could have evolved in the context of ingestion. In the present study, we examined the relationship between lateralities in prehension and mastication processes, that is, hand and cheek pouch usage, in free-ranging bonnet macaques, Macaca radiata. The macaques preferentially used one hand–the ‘preferred’ hand, to pick up the bananas lying on the ground. Lateralities in hand and cheek pouch usage (for both filling and emptying) were positively related with each other, that is, the macaques used the cheek pouch corresponding to the preferred hand predominantly and before the other. Moreover, when the macaques used the non-preferred hand to pick up the bananas, the frequency of contralateral cheek pouch usage was higher than the frequency of ipsilateral cheek pouch usage, that is, the combined structure of hand, mouth, and food did not influence the relationship between laterality in hand usage and laterality in cheek pouch usage. These findings demonstrate laterality in a relatively more involuntary function than those explored previously in any non-human primate species (e.g., facial expressions and manual gestures).

Foot use and hand preference during feeding in captive black‐and‐white snub‐nosed monkeys (Rhinopithecus bieti)

Postural origin theory predicts that body postures are related to hand preference in nonhuman primates due to hemispheric specialization. Foot preference, especially in manipulating objects, is also a good predictor of hemispheric specialization in humans. We studied limb (hand and foot) preferences in 11 captive adult black-and-white snub-nosed monkeys (Rhinopithecus bieti) to see how limb preference is influenced by postures and foot manipulation. Hand preference was significantly different for this group between quadrupedal standing and clinging postures, and sitting and clinging postures, but not between bipedal standing and clinging postures. Individuals were significantly more likely to use the right hand in the clinging posture than in quadrupedal standing or sitting postures. In the sitting posture, individuals maintained their respective hand preference even when the food was on the other side of the body. There was a gender difference in the sitting posture, where females preferred their right hand but males preferred their left. Individuals who did not routinely use their feet to manipulate objects, compared to those who did, shifted to greater right hand use from the clinging posture to the bipedal posture. One male individual and his offspring were more likely to use their feet to manipulate objects than the rest of the monkeys. In the present study, we reveal the first evidence of a postural effect on hand preference in R. bieti as well as a foot preference in this species. Our results mostly agree with the postural origin theory and hemispheric specialization.

Hand preference by black-and-white snub-nosed monkeys (Rhinopithecus bieti) in captivity: Influence of tasks and sexes

Task complexity (Fagot & Vauclair 1991), bimanual complementary role differentiation (Uomini 2009), and the obligate use of a particular hemisphere (Rogers, 2009) have been proposed to explain why hand preferences in non-human primates are often influenced by tasks. We examined how tasks (reaching, carrying, extractive foraging, and object manipulation) and gender influenced hand preference in 11 adult black-and-white snub-nosed monkeys (Rhinopithecus bieti) out of a total of 13 known adult captive individuals of this species. A logistic regression was used to analyse 2556 bouts of binary left- vs right- hand use data. The explanatory variables are tasks, gender, and the interaction of tasks and gender. Hand preference is influenced by the task, in that subjects used the right hand significantly more often for extractive foraging and object manipulation than for reaching and carrying. We also found a significant interaction of sex and task: males used the left hand significantly more often than females for reaching and carrying, respectively, but not for extractive foraging or object manipulation. This is the first study on hand preference in R. bieti. As predicted, the hand preference in R. bieti is not a fixed property of the species or sexes but depends on the task.

Influence of the Task on Hand Preference: Individual Differences among Gorillas (Gorilla gorilla gorilla)

The degree of task complexity and bimanual complementarity have been proposed as factors affecting lateralization strength in humans. However, a large number of studies have demonstrated group-level lateral hand bias for different manual activities in numerous non-human primate species. However, no study has tested the effects that a variety of tasks may have in inducing differences in hand preference. Here, we aim to test if 3 adult gorillas exhibited a greater hand preference bias performing 4 tasks of varying complexity: grasping small versus large foods, proto-tool use task and tool use task involving greater visuospatial requirements. We found that (1) the complexity of the task does not necessarily induce a right-handed bias and (2) a subject can be right-handed for a complex task and left-handed for another one. These results, complemented by many publications on hand preference in non-human primates, reveal a great variability in hand preference, which makes it very difficult to deduce any details of hominin handedness with artefacts.

A new tool for measuring hand preference in non-human primates: Adaptation of Bishop's Quantifying Hand Preference task for Olive baboons

As non-human primates are phylogenetically close to humans, they are ideal models to investigate the precursors of human brain hemispheric specialisation. However, in spite of hundreds of reports investigating hand preference, empirically based theories generating valuable predictions are still lacking, mainly because of a disappointing deficiency in comparability between studies and even more so between species. Therefore, we propose here to adapt, for the first time, the Quantifying Hand Preference (QHP) task, devised for humans, to non-human primates. This test could be a very useful standard measure of hand preference for simple reaching in non-human primates because of its simplicity to set up and of the parameters (e.g., subject's posture; position of the item) it can control. Our test subjects were 42 baboons of various ages and both sexes. Our results highlight the crucial influence of item position on hand preference for simple reaching, even when the item is positioned close to the subjects’ body midline. Both sex and age influence baboons’ handedness index but this effect varies according to the position of the item to be grasped. We discuss our results within the theoretical framework concerning hemispheric specialisation for object manipulation and with the perspective of replicating this experiment with other non-human primate species and genera.

Laterality in Maternal Cradling and Infant Positional Biases: Implications for the Development and Evolution of Hand Preferences in Nonhuman Primates.

Left-sided maternal cradling has been widely reported in human populations. In this paper, I review the evidence of laterality in maternal cradling and infant positional biases in non-human primates. The review revealed some evidence of population-left sided cradling in great apes but little consistency in bias was found among Old and New World monkeys. Very little data have been reported in prosimians. I further describe how asymmetries in either maternal cradling or infant positional biases may explain individual and species differences in hand preference.

Handedness in Chimpanzees (Pan troglodytes) Is Associated With Asymmetries of the Primary Motor Cortex but Not With Homologous Language Areas.

The neurobiology of hand preferences in nonhuman primates is poorly understood. In this study, the authors report the first evidence of an association between hand preference and precentral gyrus-morphology in chimpanzees (Pan troglodytes). Hand preferences did not significantly correlate with other asymmetric brain regions associated with language functions in humans including the planum temporale and frontal operculum. The overall results suggest that homologous regions of the motor cortex control hand preferences in humans and apes and that these functions evolved independently of left-hemisphere specialization for language and speech.

Effect of practice on hand preference on a color visual discrimination task by capuchin monkeys (Cebus apella).

Effects of practice on hand preference in nonhuman primates have indicated an initial right-hemispheric advantage in new tasks that can be reversed or disappear after a long period of training. The aim of this study was to examine the effects of 6-mo. practice on hand preference in capuchin monkeys (Cebus apella) performing a color visual discrimination task which requires attention and learning or memory processes. For this purpose, an early period of practice (first 200 trials) was compared with a late period of practice (the last 200 trials after 6 mo. practice). No population-level biases were observed between the use of hands either early in training or after 6 mo. of practice. Individual analysis indicated that two of the five subjects tested strengthened their initial hand preference but three subjects changed their preference with the practice. No correlation was observed between hand use and performance. These results suggest that hand preference in capuchin monkeys can be influenced by practice and is not only a direct function of hemispheric specialization.

EFFECT OF PRACTICE ON HAND PREFERENCE ON A COLOR VISUAL DISCRIMINATION TASK BY CAPUCHIN MONKEYS (CEBUS APELLA)

Effects of practice on hand preference in nonhuman primates have indicated an initial right-hemispheric advantage in new tasks that can be reversed or disappear after a long period of training. The aim of this study was to examine the effects of 6-mo. practice on hand preference in capuchin monkeys (Cebus apella) performing a color visual discrimination task which requires attention and learning or memory processes. For this purpose, an early period of practice (first 200 trials) was compared with a late period of practice (the last 200 trials after 6 mo. practice). No population-level biases were observed between the use of hands either early in training or after 6 mo. of practice. Individual analysis indicated that two of the five subjects tested strengthened their initial hand preference but three subjects changed their preference with the practice. No correlation was observed between hand use and performance. These results suggest that hand preference in capuchin monkeys can be influenced by practice and is not only a direct function of hemispheric specialization.

On the other hand : Statistical issues in the assessment and interpretation of hand preference data in nonhuman primates

I describe methodological and statistical issues in the assessment of hand preference in nonhuman primates and discuss them in the context of a recent paper by McGrew and Marchant (1997) in which they conclude that there is no convincing evidence of population-level hand preferences in nonhuman primates. The criteria used by them to evaluate individual and population-level hand preferences are flawed, which results in an oversimplification of findings in nonhuman primates. I further argue that the classification schema used by McGrew and Marchant (1997) to compare hand preference distributions between species is theoretically weak and does not offer a meaningful way to compare human and nonhuman primate handedness.

Handedness in great apes: A review of findings

We present data on hand preference in great apes and discuss them in the context of theoretical models of hand preference in nonhuman primates presented by MacNeilageet al. (1987) and by Fagot and Vauclair (1991). We also discuss several methodological and statistical issues as they pertain to the assessment of hand preference in great apes and other primate species. Finally, we present a comparative framework for the study of hand preference, emphasizing the importance of studies with great apes in developing evolutionary models of hemispheric specialization.