Audrey Maille

To Beg, or Not to Beg? That Is the Question: Mangabeys Modify Their Production of Requesting Gestures in Response to Human’s Attentional States

Background Although gestural communication is widespread in primates, few studies focused on the cognitive processes underlying gestures produced by monkeys. Methodology/Principal Findings The present study asked whether red-capped mangabeys (Cercocebus torquatus) trained to produce visually based requesting gestures modify their gestural behavior in response to human’s attentional states. The experimenter held a food item and displayed five different attentional states that differed on the basis of body, head and gaze orientation; mangabeys had to request food by extending an arm toward the food item (begging gesture). Mangabeys were sensitive, at least to some extent, to the human’s attentional state. They reacted to some postural cues of a human recipient: they gestured more and faster when both the body and the head of the experimenter were oriented toward them than when they were oriented away. However, they did not seem to use gaze cues to recognize an attentive human: monkeys begged at similar levels regardless of the experimenter’s eyes state. Conclusions/Significance These results indicate that mangabeys lowered their production of begging gestures when these could not be perceived by the human who had to respond to it. This finding provides important evidence that acquired begging gestures of monkeys might be used intentionally.

Inferences about the location of food in lemurs (Eulemur macaco and Eulemur fulvus): a comparison with apes and monkeys.

The ability of black and brown lemurs (Eulemur macaco and Eulemur fulvus) to make inferences about hidden food was tested using the same paradigm as in Call’s (J Comp Psycol 118:232–241, 2004) cup task experiment. When provided with either visual or auditory information about the content of two boxes (one empty, one baited), lemurs performed better in the auditory condition than in the visual one. When provided with visual or auditory information only about the empty box, one subject out of four was above chance in the auditory condition, implying inferential reasoning. No subject was successful in the visual condition. This study reveals that (1) lemurs are capable of inferential reasoning by exclusion and (2) lemurs make better use of auditory than visual information. The results are compared with the performances recorded in apes and monkeys under the same paradigm.

Which are the features of the TUBE task that make it so efficient in detecting manual asymmetries? An investigation in two Cercopithecine species (Cercopithecus neglectus and Cercocebus torquatus).

In the last decade, the TUBE task has been repeatedly shown to be highly efficient in detecting manual asymmetries that are strong hand preferences reflecting hemispheric specialization, in non human primates. The TUBE task was thus classified as a high-level task, presumably because it involves bimanual coordination. However, this task also requires a precise action made by digit(s), which may also be a crucial feature in eliciting manual asymmetries. In the present study, we compared hand preferences for a new TUBE-unimanual task and the classic TUBE-bimanual task, both performed mostly by using the forefinger, in 12 guenons (De Brazzas monkey: Cercopithecus neglectus) and 18 mangabeys (red-capped mangabey: Cercocebus torquatus). We found a relationship between hand preferences exhibited for the two tasks, suggesting that precise use of the forefinger may induce the activation of a specialized hemisphere in both the TUBE-unimanual and the TUBE-bimanual task. However, we showed that the strength of manual laterality was higher in the TUBE-bimanual task than in the TUBE-unimanual task, indicating that bimanual coordination may enhance the expression of hand preferences. We propose that the TUBE-bimanual task is highly efficient in detecting hemispheric specialization because bimanual role differentiation would make precise digit use highly skillful. Finally, we revealed species differences in hand use, especially in females: the most arboreal species, De Brazzas monkeys, increased left-hand use from the TUBE-unimanual to the TUBE-bimanual task whereas the most terrestrial species, red-capped mangabeys, increased right-hand use.

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.

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.

Manual laterality and strategy use for a coordinated bimanual task requiring precise and power grip in guenons and mangabeys

Bimanual tasks have been repeatedly shown to elicit manual asymmetries supposed to reflect hemispheric specialization. And yet, a coordinated bimanual task, the BOX task, appears to be inefficient in detecting biases of hand preferences. The BOX task involves two sequential actions requiring a precise grip, lift the lid of a box and grasp a small item inside the box (while holding the lid). In the present study, we compared manual laterality exhibited for the classic bimanual BOX task and for a unimanual BOX task in 11 De Brazzas monkeys (Cercopithecus neglectus) and 19 red‐capped mangabeys (Cercocebus torquatus). In addition, we assessed strategy use for solving the bimanual BOX task. We found that left‐hand use for grasping the item was higher in the BOX‐bimanual task than in the BOX‐unimanual task. We propose that this increase in left‐hand use for grasping the item results from both a hemispheric specialization for lifting the lid and an advantage in using a skillful strategy. Indeed, we revealed (1) group‐level right biases for lifting the lid and (2) a complete differentiation between the roles of the two hands in subjects showing a left‐hand preference for grasping the item. Finally, the bimanual BOX task showed age differences in the two species, either in manual laterality for grasping the item or in strategy use. This study provides additional evidence that manual laterality might be sensitive to maturational factors and characteristics of the bimanual tasks such as the order and the features of sequential actions. Am. J. Primatol. 75:1096–1107, 2013.

Does a Nonprimate Mammal, the Northern Tree Shrew (Tupaia belangeri), Exhibit Paw Preference in Two Forms of a Grasping Task?

Tree shrews represent a relevant model to study the evolution of primate manual laterality as they are phylogenetically close to primates, they are able to grasp despite having a nonopposable thumb, and they possess a well-developed visual system. In this study, we examined the paw laterality and grasping success rate of 30 Tupaia belangeri (15 males, 15 females) in 2 forced-food grasping tasks (i.e., in a forced-food grasping experiment, the animal has to use paws instead of mouth for food retrieval). We also attempted to determine whether paw usage would be affected by the availability of visual cues using both a visual task (transparent tube) and a nonvisual task (identical but opaque tube). In both tasks, tree shrews showed paw preferences at an individual but not at a population level. Paw laterality (direction and strength) did not differ between tasks. Moreover, in the specific task that we used, grasping success rate was not affected by an absence of visual cues, indicating that tree shrews did not rely on visual guidance to direct their grasps in this forced-food grasping experiment. Our findings suggest that, in contrast to primates, paw usage in tree shrews may result from a modification of a fixed motor pattern in which the preferred direction may be learned. This basic motor organization might be a first step in the evolution of manual laterality, which eventually became controlled by vision in the primate lineage.