Unconstrained 3D-kinematics of prehension in five primates: Lemur,capuchin, gorilla,chimpanzee, human

Primates are known for their use of the hand in many activities including food grasping. Yet, most studies concentrate on the type of grip used. Moreover, kinematic studies remain limited to a few investigations of the distal elements in constrained conditions in humans and macaques. In order to improve our understanding of the prehension movement in primates, we analyse here the behavioural strategies (e.g., types of grip, body postures) as well as the 3D kinematics of the whole forelimb and the trunk during the prehension of small static food items in five primate species in unconstrained conditions. All species preferred the quadrupedal posture except lemurs, which used a typical crouched posture. Grasp type differed among species, with smaller animals (capuchins and lemurs) using a whole-hand grip and larger animals (humans, gorillas, chimpanzees) using predominantly a precision grip. Larger animals had lower relative wrist velocities and spent a larger proportion of the movement decelerating. Humans grasped food items with planar motions involving small joint rotations, more similar to the smaller animals than to gorillas and chimpanzees, which used greater rotations of both the shoulder and forearm. In conclusion, the features characterising human food prehension are present in other primates, yet differences exist in joint motions. These results provide a good basis to suggest hypotheses concerning the factors involved in driving the evolution of grasping abilities in primates.     

How Aging Affects Grasping Behavior and Pull Strength in Captive Gray Mouse Lemurs (<Emphasis Type="Italic">Microcebus murinus</Emphasis>)

Prehension is essential for animal survival and fitness. It is involved in locomotion and feeding behavior and subject to physical and physiological constraints. Studies of prehension in primates have explored the importance of food properties and of the environment, but aging has rarely been studied although prehensile capacity may deteriorate with age in humans. To test the hypothesis that aging affects grasping abilities and to reveal possible behavioral adaptations to this, we quantified behavioral grasping strategies and pull strength in 10 young adult (2–3 yr old) and 10 aged (7–8 yr old) gray mouse lemurs (Microcebus murinus). We assessed grasping strategies in an experimental cage by quantifying grip types used to grasp static and mobile foods. We measured strength using a Kistler triaxial force platform. Our results show that 1) mobile and static foods affected individuals of different ages in similar ways; 2) older individuals used more mouth grasps than young ones; 3) aged individuals made twice as many attempts as young ones when grasping mobile food items but this difference was not significant; and 4) there were no differences in hand grip strength between age classes but young individuals showed a higher foot pull strength compared to old ones. These data suggest that the observed differences in behavior may be due to a decrease in foot grip strength, which in turn influences stability on narrow branches, forcing animals to use their hands to maintain stability and preventing them from using their hands for food-related tasks.     

Grasping behavior in tufted capuchin monkeys (Cebus apella): grip types and manual laterality for picking up a small food item

This study investigates prehension in 20 tufted capuchins (Cebus apella) in a reaching task requiring individuals to grasp a small food item fixed to a tray. The aim was twofold: 1) to describe capuchins' grasping techniques in detail, focusing on digit movements and on different areas of contact between the grasping fingers; and 2) to assess the relationship between grip types and manual laterality in this species. Capuchins picked up small food items using a wide variety of grips. In particular, 16 precision grip variants and 4 power grip variants were identified. The most frequently used precision grip involved the distal lateral areas of the thumb and the index finger, while the most preferred kind of power grip involved the thumb and the palm, with the thumb being enclosed by the other fingers. Immature capuchins picked up small food items using power grips more often than precision grips, while adult individuals exhibited no significant preference for either grip type. The analysis performed on the time capuchins took to grasp the food and withdraw it from the tray hole revealed that 1) precision grips were as efficient as power grips; 2) for precision grips, the left hand was faster than the right hand; and 3) for power grips, both hands were equally quick. Hand preference analysis, based on the frequency for the use of either hand for grasping actions, revealed no significant hand bias at group level. Likewise, there was no significant relationship between grip type and hand preference.     

Intrinsic hand proportions of euarchontans and other mammals: implications for the locomotor behavior of plesiadapiforms

Arboreal primates have distinctive intrinsic hand proportions compared with many other mammals. Within Euarchonta, platyrrhines and strepsirrhines have longer manual proximal phalanges relative to metacarpal length than colugos and terrestrial tree shrews. This trait is part of a complex of features allowing primates to grasp small-diameter arboreal substrates. In addition to many living and Eocene primates, relative elongation of proximal manual phalanges is also present in most plesiadapiforms. In order to evaluate the functional and evolutionary implications of manual similarities between crown primates and plesiadapiforms, we measured the lengths of the metacarpal, proximal phalanx, and intermediate phalanx of manual ray III for 132 extant mammal species (n=702 individuals). These data were compared with measurements of hands in six plesiadapiform species using ternary diagrams and phalangeal indices. Our analyses reveal that many arboreal mammals (including some tree shrews, rodents, marsupials, and carnivorans) have manual ray III proportions similar to those of various arboreal primates. By contrast, terrestrial tree shrews have hand proportions most similar to those of other terrestrial mammals, and colugos are highly derived in having relatively long intermediate phalanges. Phalangeal indices of arboreal species are significantly greater than those of the terrestrial species in our sample, reflecting the utility of having relatively long digits in an arboreal context. Although mammals known to be capable of prehensile grips demonstrate long digits relative to palm length, this feature is not uniquely associated with manual prehension and should be interpreted with caution in fossil taxa. Among plesiadapiforms, Carpolestes, Nannodectes, Ignacius, and Dryomomys have manual ray III proportions that are unlike those of most terrestrial species and most similar to those of various arboreal species of primates, tree shrews, and rodents. Within Euarchonta, Ignacius and Carpolestes have intrinsic hand proportions most comparable to those of living arboreal primates, while Nannodectes is very similar to the arboreal tree shrew Tupaia minor. These results provide additional evidence that plesiadapiforms were arboreal and support the hypothesis that Euarchonta originated in an arboreal milieu.     

On the Evolution of Handedness: Evidence for Feeding Biases

Many theories have been put forward to explain the origins of right-handedness in humans. Here we present evidence that this preference may stem in part from a right hand advantage in grasping for feeding. Thirteen participants were asked to reach-to-grasp food items of 3 different sizes: SMALL (Cheerios®), MEDIUM (Froot Loops®), and LARGE (Oatmeal Squares®). Participants used both their right- and left-hands in separate blocks (50 trials each, starting order counterbalanced) to grasp the items. After each grasp, participants either a) ate the food item, or b) placed it inside a bib worn beneath his/her chin (25 trials each, blocked design, counterbalanced). The conditions were designed such that the outward and inward movement trajectories were similar, differing only in the final step of placing it in the mouth or bib. Participants wore Plato liquid crystal goggles that blocked vision between trials. All trials were conducted in closed-loop with 5000 ms of vision. Hand kinematics were recorded by an Optotrak Certus, which tracked the position of three infrared diodes attached separately to the index finger, thumb, and wrist. We found a task (EAT/PLACE) by hand (LEFT/RIGHT) interaction on maximum grip aperture (MGA; the maximum distance between the index finger and thumb achieved during grasp pre-shaping). MGAs were smaller during right-handed movements, but only when grasping with intent to eat. Follow-up tests show that the RIGHT-HAND/EAT MGA was significantly smaller than all other hand/task conditions. Because smaller grip apertures are typically associated with greater precision, our results demonstrate a right-hand advantage for the grasp-to-eat movement. From an evolutionary perspective, early humans may have preferred the hand that could grasp food with more precision, thereby maximizing the likelihood of retrieval, consumption, and consequently, survival.     

Patterns of hand and mouth lateral biases in bamboo leaf shoot feeding and simple food reaching in the gentle lemur (Hapalemur griseus)

Lateralized feeding behaviors of 7 wild-born and 6 captive-born Hapalemur griseus sp. were evaluated in two conditions, simple food reaching and species-typical bamboo foraging. Gentle lemurs were found to have the strongest lateral hand preference in simple food reaching of any prosimian species yet studied. However in this small sample, population-level lateralization was not found: 5 preferred the right hand and 8 the left. The movement pattern used by hapalemurs when feeding on bamboo leaf shoots was categorized into four components: PULL IN, COUNTERFORCE, TURN, and FEED IN. Lateral hand bias was scored for all four components and lateral mouth preference was scored for the two components that involved the mouth (COUNTERFORCE and FEED IN). Strong positive correlations were found between hand preference in the most lateralized components of shoot eating (TURN and FEED IN) and simple food reaching. This suggests that the gentle lemurs' species-typical bamboo feeding behavior may contribute to the exceptionally strong hand preference for simple food reaching seen in this species. There were negative correlations between the component measure of shoot feeding that required strength (COUNTERFORCE) and the components that required manipulation (TURN and FEED IN). Within the COUNTERFORCE and FEED IN components, mouth preference and hand preference were positively associated in a manner that suggested one side of the mouth was preferred for removing the shoot and the other side for mastication. Asymmetrical dental wear may provide a means of dating behavioral lateralization in ancestral species. © 1993 Wiley-Liss, Inc.     

Handedness and Grooming in Pan troglodytes: Comparative Analysis Between Findings in Captive and Wild Individuals

Grooming is a complex set of motor actions, common in highly social primates. We tested for asymmetries in hand use during unimanual and bimanual allogrooming in 215 captive chimpanzees. In addition to hand use, we coded in the ethogram whether the manual grooming action co-occurred with the use of the mouth. Overall, grooming did not elicit strong handedness at the individual level, but there is a small yet significant population-level right-hand bias for bimanual grooming. Mouth use during grooming had no influence on hand use. A comparison of the findings with previously published data on handedness for grooming in wild chimpanzees suggests that wild apes are more right-handed than captive individuals are for allogrooming. Collectively, the results suggest that role differentiation of the hands is an important factor in the assessment of handedness for grooming, and perhaps additional manual actions of chimpanzees and other primates.     

Primate origins: evolutionary change in digital ray patterning and segmentation

This study presents evidence that the first primates share with extant lemurs, tarsiers, and anthropoids hand proportions unlike those of their close relatives, the tree shrews (Scandentia), colugos (Dermoptera), and plesiadapiforms. Specifically, early primates as well as modern strepsirhines and haplorhines have relatively short metacarpals and long proximal phalanges giving them a grasping, prehensile hand. Limb development was studied in the primate Microcebus murinus and a comparative sample of rodents, artiodactyls, and marsupials to investigate the role of embryonic patterning in the morphogenesis and evolution of primate hand proportions. Comparative analysis shows that the derived finger proportions of primates are generated during the early phases of digital ray patterning and segmentation, when the interzone cells marking the presumptive metacarpo- and interphalangeal joints first appear. Interspecific variation in relative digit and metapodial proportions therefore has high developmental penetrance; that is, adult differences are observed at early ontogenetic stages. The paleontological, comparative, and developmental data are therefore consistent with the hypothesis that the early Cenozoic origin of primates involved an evolutionary change in digital ray pattern formation ultimately yielding a grasping, prehensile hand.     

Behavioral and functional strategies during tool use tasks in bonobos

Different primate species have developed extensive capacities for grasping and manipulating objects. However, the manual abilities of primates remain poorly known from a dynamic point of view. The aim of the present study was to quantify the functional and behavioral strategies used by captive bonobos (Pan paniscus) during tool use tasks. The study was conducted on eight captive bonobos which we observed during two tool use tasks: food extraction from a large piece of wood and food recovery from a maze. We focused on grasping postures, in‐hand movements, the sequences of grasp postures used that have not been studied in bonobos, and the kind of tools selected. Bonobos used a great variety of grasping postures during both tool use tasks. They were capable of in‐hand movement, demonstrated complex sequences of contacts, and showed more dynamic manipulation during the maze task than during the extraction task. They arrived on the location of the task with the tool already modified and used different kinds of tools according to the task. We also observed individual manual strategies. Bonobos were thus able to develop in‐hand movements similar to humans and chimpanzees, demonstrated dynamic manipulation, and they responded to task constraints by selecting and modifying tools appropriately, usually before they started the tasks. These results show the necessity to quantify object manipulation in different species to better understand their real manual specificities, which is essential to reconstruct the evolution of primate manual abilities.     

Handedness in nature: first evidence on manual laterality on bimanual coordinated tube task in wild primates

Handedness is a defining feature of human manual skill and understanding the origin of manual specialization remains a central topic of inquiry in anthropology and other sciences. In this study, we examined hand preference in a sample of wild primates on a task that requires bimanual coordinated actions (tube task) that has been widely used in captive primates. The Sichuan snub-nosed monkey (Rhinopithecus roxellana) is an arboreal Old World monkey species that is endemic to China, and 24 adult individuals from the Qinling Mountains of China were included for the analysis of hand preference in the tube task. All subjects showed strong individual hand preferences and significant group-level left-handedness was found. There were no significant differences between males and females for either direction or strength of hand preference. Strength of hand preferences of adults was significantly greater than juveniles. Use of the index finger to extract the food was the dominant extractive-act. Our findings represent the first evidence of population-level left-handedness in wild Old World monkeys and broaden our knowledge on evaluating primate hand preference via experimental manipulation in natural conditions.     

Cortical control of grasp in non-human primates

The skilled use of the hand for grasping and manipulation of objects is a fundamental feature of the primate motor system. Grasping movements involve transforming the visual information about an object into a motor command appropriate for the coordinated activation of hand and finger muscles. The cerebral cortex and its descending projections to the spinal cord are known to play a crucial role for the control of grasp. Recent studies in non-human primates have provided some striking new insights into the respective contribution of the parietal and frontal motor cortical areas to the control of grasp. Also, new approaches allowed investigating the coupling of grasp-related activity in different cortical areas for the control of the descending motor command.     

Patterns of lateralized hand use in an arboreal primate, Simias concolor

Studies of hand use in nonhuman primates suggest that several species exhibit hand preferences for a variety of tasks. The majority of studies, however, focus on the lateralized hand use of captive nonhuman primate populations. Although captive settings offer a more controlled environment for assessing hand preferences, studies of wild populations provide important insights into how handedness is affected by natural environmental conditions and thus potential insights into the evolution of handedness. To investigate handedness in a population of wild nonhuman primates, we studied patterns of lateralized hand use during feeding in four simakobu monkeys (Simias concolor), an arboreal species inhabiting the Mentawai Islands, Indonesia. Our data show that individual variation in hand preferences for feeding existed among our study animals. In addition, each simakobu expressed a significant hand preference for supporting itself on a branch during feeding, an uncoordinated bimanual task. This bias was most prevalent when the branch used for support was a main branch rather than a terminal branch. When both hands were employed in a coordinated bimanual feeding activity (bimanual manipulation), only two subjects showed a significant bias for feeding. Our data suggest that these individuals are more likely to express significant hand preferences when feeding from stable, rather than precarious, positions within the canopy.     

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).     

Hand preference and tool use in wild chimpanzees

The hand preference of chimpanzees in their natural habitat was studied at Bossou, Republic of Guinea, West Africa. The quantitative difference in left/right hand use was small in food picking and carrying. In contrast, the chimpanzees employed either the right or left hand in nutcracking behavior using a pair of stones. All adults and many adolescents and juveniles utilized one hand exclusively for holding a hammer stone. Left hand preference was more prevalent among adults. However, when adolescents and juveniles were included, there was no significant bias in the ratio of left/right handers. Nut-cracking behavior requires long-term learning of the fine manipulation of stones and nuts by both hands. Each hand has a separate role, and the hands work together in nut cracking. The differential and complementary use of both hands may be a prime factor promoting exclusive hand preference in chimpanzees comparable to that of humans.     

Rats’ learning of a new motor skill: Insight into the evolution of motor sequence learning

Recent behavioral and neural evidence has suggested that ethologically relevant sub-movements (movement primitives) are used by primates for more complex motor skill learning. These primitives include extending the hand, grasping an object, and holding food while moving it toward the mouth. In prior experiments with rats performing a reach-to-grasp-food task, we observed that especially during early task learning, rats appeared to have movement primitives similar to those seen in primates. Unlike primates, however, during task learning the rats performed these sub-movements in a disordered manner not seen in humans or macaques, e.g. with the rat chewing before placing the food pellet in its mouth. Here, in two experiments, we tested the hypothesis that for rats, learning this ecologically relevant skill involved learning to concatenate the sub-movements in the correct order. The results confirmed our initial observations, and suggested that several aspects of forepaw/hand use, taken for granted in primate studies, must be learned by rats to perform a logically connected and seemingly ecologically important series of sub-movements. We discuss our results from a comparative and evolutionary perspective.     

Learned Manipulation at Unconstrained Contacts Does Not Transfer across Hands

Recent studies about sensorimotor control of the human hand have focused on how dexterous manipulation is learned and generalized. Here we address this question by testing the extent to which learned manipulation can be transferred when the contralateral hand is used and/or object orientation is reversed. We asked subjects to use a precision grip to lift a grip device with an asymmetrical mass distribution while minimizing object roll during lifting by generating a compensatory torque. Subjects were allowed to grasp anywhere on the object’s vertical surfaces, and were therefore able to modulate both digit positions and forces. After every block of eight trials performed in one manipulation context (i.e., using the right hand and at a given object orientation), subjects had to lift the same object in the second context for one trial (transfer trial). Context changes were made by asking subjects to switch the hand used to lift the object and/or rotate the object 180° about a vertical axis. Therefore, three transfer conditions, hand switch (HS), object rotation (OR), and both hand switch and object rotation (HS+OR), were tested and compared with hand matched control groups who did not experience context changes. We found that subjects in all transfer conditions adapted digit positions across multiple transfer trials similar to the learning of control groups, regardless of different changes of contexts. Moreover, subjects in both HS and HS+OR group also adapted digit forces similar to the control group, suggesting independent learning of the left hand. In contrast, the OR group showed significant negative transfer of the compensatory torque due to an inability to adapt digit forces. Our results indicate that internal representations of dexterous manipulation tasks may be primarily built through the hand used for learning and cannot be transferred across hands.     

Behavioral Assessment of Manual Dexterity in Non-Human Primates

The corticospinal (CS) tract is the anatomical support of the exquisite motor ability to skillfully manipulate small objects, a prerogative mainly of primates¹. In case of lesion affecting the CS projection system at its origin (lesion of motor cortical areas) or along its trajectory (cervical cord lesion), there is a dramatic loss of manual dexterity (hand paralysis), as seen in some tetraplegic or hemiplegic patients. Although there is some spontaneous functional recovery after such lesion, it remains very limited in the adult. Various therapeutic strategies are presently proposed (e.g. cell therapy, neutralization of inhibitory axonal growth molecules, application of growth factors, etc), which are mostly developed in rodents. However, before clinical application, it is often recommended to test the feasibility, efficacy, and security of the treatment in non-human primates. This is especially true when the goal is to restore manual dexterity after a lesion of the central nervous system, as the organization of the motor system of rodents is different from that of primates^1,2. Macaque monkeys are illustrated here as a suitable behavioral model to quantify manual dexterity in primates, to reflect the deficits resulting from lesion of the motor cortex or cervical cord for instance, measure the extent of spontaneous functional recovery and, when a treatment is applied, evaluate how much it can enhance the functional recovery.The behavioral assessment of manual dexterity is based on four distinct, complementary, reach and grasp manual tasks (use of precision grip to grasp pellets), requiring an initial training of adult macaque monkeys. The preparation of the animals is demonstrated, as well as the positioning with respect to the behavioral set-up. The performance of a typical monkey is illustrated for each task. The collection and analysis of relevant parameters reflecting precise hand manipulation, as well as the control of force, are explained and demonstrated with representative results. These data are placed then in a broader context, showing how the behavioral data can be exploited to investigate the impact of a spinal cord lesion or of a lesion of the motor cortex and to what extent a treatment may enhance the spontaneous functional recovery, by comparing different groups of monkeys (treated versus sham treated for instance). Advantages and limitations of the behavioral tests are discussed. The present behavioral approach is in line with previous reports emphasizing the pertinence of the non-human primate model in the context of nervous system diseases^2,3.     

Feeding Responses of Hatchery-Reared Gilthead Sea Bream (Sparus aurata L.) to a Commercial Diet and Natural Prey Items

Many fish species have evolved feeding mechanisms and behaviours enabling them to feed on specific prey. However, such mechanisms may not be optimal for feeding on commercial-pelleted diets in aquaculture. Gilthead sea bream chew and occasionally eject pellets or parts of pellets from the mouth when feeding on commercial diets. This may result in an increase in nutritional waste from the intensive culture of this species. In this study we examined the prevalence of this food processing behaviour in two sizes of sea bream, feeding on three types of natural prey items in comparison to a commercial pellet, to give an insight into the circumstances in which excess chewing and ejection of food items from the mouth occurred. These included two hard-textured food items (commercial pellet and hard-shelled prey) and two soft-textured food items (larvae and small crustacean). Both sizes of sea bream frequently consumed the soft-textured food types, however large sea bream also frequently consumed hard-textured pellets. Hard-textured food required longer handling times and elicited more chewing and the ejection of food items from the mouth. These results suggest that future investigations on the food processing behaviour and consequent waste when fed commercial diets differing in texture could give an insight into improving diets and feeding efficiency for intensively cultivated gilthead sea bream.     

Feeding Responses of Hatchery-Reared Gilthead Sea Bream (Sparus aurata L.) to a Commercial Diet and Natural Prey Items

Many fish species have evolved feeding mechanisms and behaviours enabling them to feed on specific prey. However, such mechanisms may not be optimal for feeding on commercial-pelleted diets in aquaculture. Gilthead sea bream chew and occasionally eject pellets or parts of pellets from the mouth when feeding on commercial diets. This may result in an increase in nutritional waste from the intensive culture of this species. In this study we examined the prevalence of this food processing behaviour in two sizes of sea bream, feeding on three types of natural prey items in comparison to a commercial pellet, to give an insight into the circumstances in which excess chewing and ejection of food items from the mouth occurred. These included two hard-textured food items (commercial pellet and hard-shelled prey) and two soft-textured food items (larvae and small crustacean). Both sizes of sea bream frequently consumed the soft-textured food types, however large sea bream also frequently consumed hard-textured pellets. Hard-textured food required longer handling times and elicited more chewing and the ejection of food items from the mouth. These results suggest that future investigations on the food processing behaviour and consequent waste when fed commercial diets differing in texture could give an insight into improving diets and feeding efficiency for intensively cultivated gilthead sea bream.     

Effect of Removal from the Family Group on Feeding Behavior by Captive Callithrix jacchus

Common marmosets are omnivorous primates with a highly diversified diet. There is no study describing if and how the diet is learned. Infants get their first bits of solid food from other monkeys in the group, which suggests that they may need an introduction to food items by older individuals before including them in their diet. We assessed the acceptance of novel and familiar food items by common marmosets, both isolated and in their family groups. We tested adult, subadults and juveniles from 5 captive families while isolated and in their family groups. The test consisted of presenting for 10 min novel and familiar food items to isolated individuals or to the whole family. We recorded the latency to start eating and the number of food items ingested. When isolated, adults ate more novel and familiar food items than juveniles did. They also started eating sooner than juveniles did. When tested alone, all juveniles, except one, never tasted novel food, and juveniles ingested fewer familiar food items than adults did. When tested in their family groups, juveniles ingested more familiar and novel food than when they were isolated. Our results suggest that: 1. juvenile common marmosets show more food neophobia than adults do, especially when alone; 2. the family group may facilitate the acceptance of novel food items by juveniles; 3. the family group, besides promoting the acceptance of novel food, may also increase its ingestion; and 4. dietary acquisition in Callithrix jacchus involves social facilitation.