Human laterality for manipulation and gestural communication: A study of beach-volleyball players during the Olympic Games.

Comparative studies can help understand better brain functional lateralization for manipulation and language. This study investigated and compared, for the first time, human adults' laterality for manipulation and gestures in a non-experimental social context. We analysed the manual laterality of 48 beach volleyball athletes for four frequently expressed behaviours: a complex throwing action (jump serve) and three gestures (CLAP HAND, PUMP FIST and SLAP HAND-TO-HAND). We evaluated population-level laterality bias for each of the four behaviours separately, compared manual laterality between behaviours and investigated factors influencing gestural laterality. We furthered our between-gestures comparison by taking into account three categories of factors simultaneously: gesture characteristics (sensory modality), interactional context components (positions of interactants and emotional valence), and individual demographic characteristics (age, sex and country). Our study showed that (1) each behaviour considered presented a population-level right-hand bias, (2) differences of laterality between behaviours were probably related to gesture sensory modality and (3) signaller's laterality was modulated differently in relation to positions of interactants, emotional valence, age and sex. Our results support the literature suggesting that left-hemisphere specialization for manipulation and language (speech and gestures) may have evolved from complex manual activities such as throwing and from gestural communication.

Decision-making under risk of gain in young children and mangabey monkeys.

In contrast to human adults, risk proneness in the gain domain is usually observed in both young children and non-human primates. It is currently unclear what mechanism might be underlying such economic preferences. We investigated decision-making under risk of gain in toddlers and monkeys. The choices of 2.5-year-old children and red-capped mangabeys (Cercocebus torquatus torquatus) were examined in a gambling task for food reward in which participants have to choose between two options, a secure option and a risky option. In contrast to monkeys, toddlers showed a strong preference for the risky option over the safe option. In order to test the hypothesis that risky choices in participants reflect inhibitory control difficulties, toddlers and mangabeys were presented in Experiment 2 with a situation analogous to that used in Experiment 1 except for the fact that the opaque cover under which was placed the secure option was replaced by a transparent cover. In this second experiment, toddlers continued to show a preference for the risky option over the safe option. In contrast, mangabeys showed a preference for the safe option over the risky option in Trial 1 but they shifted their economic preferences in Trial 2. We argue that decision-making strategies under risk of gain in both toddlers and mangabeys (a) do not reflect poor behavioral control and (b) are not reducible to perception-action couplings.

A multifactorial investigation of captive gorillas' intraspecific gestural laterality.

Multifactorial investigations of intraspecific laterality of primates' gestural communication aim to shed light on factors that underlie the evolutionary origins of human handedness and language. This study assesses gorillas' intraspecific gestural laterality considering the effect of various factors related to gestural characteristics, interactional context and sociodemographic characteristics of signaller and recipient. Our question was: which factors influence gorillas' gestural laterality? We studied laterality in three captive groups of gorillas (N = 35) focusing on their most frequent gesture types (N = 16). We show that signallers used predominantly their hand ipsilateral to the recipient for tactile and visual gestures, whatever the emotional context, gesture duration, recipient's sex or the kin relationship between both interactants, and whether or not a communication tool was used. Signallers' contralateral hand was not preferentially used in any situation. Signallers' right-hand use was more pronounced in negative contexts, in short gestures, when signallers were females and its use increased with age. Our findings showed that gorillas' gestural laterality could be influenced by different types of social pressures thus supporting the theory of the evolution of laterality at the population level. Our study also evidenced that some particular gesture categories are better markers than others of the left-hemisphere language specialization.

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 Brazza's 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.

Baboons' hand preference resists to spatial factors for a communicative gesture but not for a simple manipulative action.

Olive baboons (Papio anubis) do acquire and use intentional requesting gestures in experimental contexts. Individual's hand preference for these gestures is consistent with that observed for typical communicative gestures, but not for manipulative actions. Here, we examine whether the strength of hand preference may also be a good marker of hemispheric specialization for communicative gestures, hence differing from the strength of hand preference for manipulative actions. We compared the consistency of individuals' hand preference with regard to the variation in space of either (i) a communicative partner or (ii) a food item to grasp using a controlled set-up. We report more consistent hand preference for communicative gestures than for grasping actions. Established hand preference in the midline was stronger for gesturing than for grasping and allowed to predict the consistency of hand preference across positions. We found no significant relation between the direction of hand preference and the task.

Visual laterality in dolphins: importance of the familiarity of stimuli.

BACKGROUND: Many studies of cerebral asymmetries in different species lead, on the one hand, to a better understanding of the functions of each cerebral hemisphere and, on the other hand, to develop an evolutionary history of hemispheric laterality. Our animal model is particularly interesting because of its original evolutionary path, i.e. return to aquatic life after a terrestrial phase. The rare reports concerning visual laterality of marine mammals investigated mainly discrimination processes. As dolphins are migrant species they are confronted to a changing environment. Being able to categorize new versus familiar objects would allow dolphins a rapid adaptation to novel environments. Visual laterality could be a prerequisite to this adaptability. To date, no study, to our knowledge, has analyzed the environmental factors that could influence their visual laterality. RESULTS: We investigated visual laterality expressed spontaneously at the water surface by a group of five common bottlenose dolphins (Tursiops truncatus) in response to various stimuli. The stimuli presented ranged from very familiar objects (known and manipulated previously) to familiar objects (known but never manipulated) to unfamiliar objects (unknown, never seen previously). At the group level, dolphins used their left eye to observe very familiar objects and their right eye to observe unfamiliar objects. However, eyes are used indifferently to observe familiar objects with intermediate valence. CONCLUSION: Our results suggest different visual cerebral processes based either on the global shape of well-known objects or on local details of unknown objects. Moreover, the manipulation of an object appears necessary for these dolphins to construct a global representation of an object enabling its immediate categorization for subsequent use. Our experimental results pointed out some cognitive capacities of dolphins which might be crucial for their wild life given their fission-fusion social system and migratory behaviour.

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.

Age- and sex-specific patterns of vocal behavior in De Brazza's monkeys (Cercopithecus neglectus).

Although vocal production is strongly genetically determined in nonhuman primates, vocal usage is more likely to be influenced by experience. Nonetheless, sex differences in both production and usage can be found in the vocal repertoire of adults, but little attention has been paid to their ontogeny. Here, we provide the first comprehensive analysis of the vocal repertoire of De Brazza's monkeys (Cercopithecus neglectus), with particular attention to age- and sex-specific patterns. This species has special interest because it is the only monogamous species of guenons, but it nevertheless shares the strong sexual morphological and behavioral dimorphism seen in other guenons. A structurally based classification of calls recorded in 23 captive individuals has been cross-validated by an analysis of the associated contexts of emission. We identified sound units that could be uttered alone or concatenated to form 10 call types, including only three types shared by all age-sex-classes. Both age- and sex-discrepancy in terms of phonation could be explained by maturational changes and morphological dimorphism. In general, call production and usage parallel those seen in other guenons, suggesting that phylogeny and sexual dimorphism play important roles in vocal communication in this species. However, the boundary between adult male and female vocal repertoires appeared to be less strict than previously reported, suggesting that both sexes have the capacity to produce calls of the other sex but that social roles may constrain this expression. Similarly, age-specific vocal patterns would reflect respective social roles, and experience to some extent. Finally, calling rates would reflect age-/sex-specific degree of involvement in intragroup social networks. These findings highlight the relative importance of phylogeny, morphology, and social system on the shaping of individual repertoires in nonhuman primates.

Context-Dependent Gestural Laterality: A Multifactorial Analysis in Captive Red-Capped Mangabeys.

Catarrhine primates gesture preferentially with their right hands, which led to the hypothesis of a gestural origin of human left-hemispheric specialization for language. However, the factors influencing this gestural laterality remain understudied in non-hominoid species, particularly in intraspecific contexts, although it may bring valuable insights into the proximate and ultimate causes of language lateralization. We present here a preliminary investigation of intraspecific gestural laterality in catarrhine monkeys, red-capped mangabeys (Cercocebus torquatus). We described the spontaneous production of brachio-manual intentional gestures in twenty-five captive subjects. Although we did not evidence any significant gestural lateralization neither at the individual- nor population-level, we found that mangabeys preferentially use their right hands to gesture in negative social contexts, such as aggressions, suggesting an effect of emotional lateralization, and that they adapt to the position of their receiver by preferentially using their ipsilateral hand to communicate. These results corroborate previous findings from ape studies. By contrast, factors related to gesture form and socio-demographic characteristics of signaler and receiver did not affect gestural laterality. To understand better the relationships between gestural laterality and brain lateralization from an evolutionary perspective, we suggest that the gestural communication of other monkey species should be examined with a multifactorial approach.

Visual laterality in dolphins when looking at (un)familiar humans.

Understanding the evolution of brain lateralisation including the origin of human visual laterality requires an understanding of brain lateralisation in related animal species. However, little is known about the visual laterality of marine mammals. To help correct this lack, we evaluated the influence of familiarity with a human on the visual response of five captive bottlenose dolphins. Dolphins gazed longer at unfamiliar than at familiar humans, revealing their capacity to discriminate between these two types of stimuli. Pooled data for responses to all test stimuli demonstrated a preferential use of left eye by all our five dolphin subjects. However, familiarity with particular humans did not influence preferential use of a given eye. Finally, we compared our results with those on other vertebrates.

Differential outcomes of unilateral interferences at birth.

Behavioural modifications, including modifications of emotional reactivity, can occur following early experience such as handling (manual rubbing). Here, we investigated the effects of unilateral tactile stimulation at an early stage on emotional reactions later on. We handled newborn foals intensively on one side of their body. This early unilateral tactile experience had medium-term effects: the reactions of foals to a human approach, when they were 10 days old, differed according to the side stimulated at birth. Fewer right-handled foals accepted contact with humans, they delayed first contact longer and they evaded approaching humans sooner than did non-handled and left-handled foals. These results raise questions concerning the organization of neonatal care in animals and humans.

Task complexity, posture, age, sex: which is the main factor influencing manual laterality in captive Cercocebus torquatus torquatus?

Behavioural asymmetries reflect brain asymmetry in nonhuman primates (NHP) as in humans. By investigating manual laterality, researchers can study the evolution of brain hemisphere specialisation. Three dominant theories aim to establish an evolutionary scenario. The most recent theory relates different levels of manual laterality to task complexity. Our investigation aimed to evaluate the importance of two extrinsic factors (posture and the need for manual coordination) and two intrinsic factors (age and sex) on the expression of manual laterality by red-capped mangabeys. We observed 19 captive-born mangabeys, in spontaneous situations and under experimental conditions (seven experimental tasks varying in complexity). No directionality was observed in hand preference at the group level whatever the task. But our data revealed an effect of task complexity: more subjects were lateralised than not lateralised for the bipedal task and for the three most complex tasks. Finally, we evidenced an age and a sex effect. We compare our results with data for several other primate species and discuss them in the light of different manual laterality theories.

Facial displays in red-capped mangabeys (Cercocebus torquatus): Repertoire, social context, and potential intentionality.

Primate communication relies strongly on the visual modality, notably through the production of a wide range of expressive facial signals. We investigated here the facial display repertoire of a relatively little-studied cercopithecid species, red-capped mangabeys (Cercocebus torquatus), and questioned whether their facial displays were dependent on social contexts and accompanied by indices of intentionality. Although the dual intentional and emotional use of apes' facial expressions has recently been suggested, the question of whether monkeys produce facial expressions intentionally to communicate remains open. We described 6 facial displays produced by captive red-capped mangabeys in social contexts. They are based on movements of the mouth, eyebrows, and ears, possibly graded in intensity and produced independently or in combination. We showed that most of the facial displays were produced preferentially in specific social contexts and that repertoires varied with subjects' characteristics, highlighting the communicative function of these displays. Moreover, behavioral markers of intentionality commonly used in gestural studies were found to accompany the production of some of the facial signals observed. Particularly, playful "open mouth" appeared strongly associated with intentionality indices, as previously noticed in ape species. All other facial displays, except yawns, did not exhibit all defined intentional indices but were, at least, directed toward a recipient. Interestingly, yawns presented different variants of intensity associated presumably with different social functions. Altogether, these results emphasize the communicative function of red-capped mangabeys' facial displays and provide a basis for further research on their intentional communication. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Sex differences in the vocal repertoire of adult red-capped mangabeys (Cercocebus torquatus): A multi-level acoustic analysis.

Sex differences in the vocal behavior of nonhuman primates can take various forms: sex-specific call types, differential production of shared call types, or sex discrepancy in phonation. Also, a growing literature is evidencing that systematically analyzing the vocal repertoires of primates at the call level might lead to underestimating their communicative abilities. Here, we present an extensive multi-level analysis of the still unknown vocal repertoire of adult red-capped mangabeys (Cercocebus torquatus), with a special emphasis on sex differences. We collected recordings from seven adult males and seven adult females housed in captivity. We present a structurally-based classification of mangabey calls that we cross-validated by an analysis of the associated contexts of emission. We found 12 sound units (including six sex-specific) that were concatenated to form eight call types (including four sex-specific), which were produced either singularly or in sequences composed of one ("repetition") or several ("combination") call types. We extracted organizational principles that ruled call composition and calling patterns. This revealed a high degree of potentially meaningful variability in terms of semantics and syntax. Male-female discrepancy in terms of phonation could be related to morphological dimorphism and would enable listeners to behave appropriately according to the sex of the caller. Sex differences in repertoire size, structural gradation, and call usage could reflect specificities of male-female social roles. We discuss the pertinence of these sex differences according to social system and habitat quality.

The origins of gestures and language: history, current advances and proposed theories.

Investigating in depth the mechanisms underlying human and non-human primate intentional communication systems (involving gestures, vocalisations, facial expressions and eye behaviours) can shed light on the evolutionary roots of language. Reports on non-human primates, particularly great apes, suggest that gestural communication would have been a crucial prerequisite for the emergence of language, mainly based on the evidence of large communication repertoires and their associated multifaceted nature of intentionality that are key properties of language. Such research fuels important debates on the origins of gestures and language. We review here three non-mutually exclusive processes that can explain mainly great apes' gestural acquisition and development: phylogenetic ritualisation, ontogenetic ritualisation, and learning via social negotiation. We hypothesise the following scenario for the evolutionary origins of gestures: gestures would have appeared gradually through evolution via signal ritualisation following the principle of derived activities, with the key involvement of emotional expression and processing. The increasing level of complexity of socioecological lifestyles and associated daily manipulative activities might then have enabled the acquisition and development of different interactional strategies throughout the life cycle. Many studies support a multimodal origin of language. However, we stress that the origins of language are not only multimodal, but more broadly multicausal. We propose a multicausal theory of language origins which better explains current findings. It postulates that primates' communicative signalling is a complex trait continually shaped by a cost-benefit trade-off of signal production and processing of interactants in relation to four closely interlinked categories of evolutionary and life cycle factors: species, individual and context-related characteristics as well as behaviour and its characteristics. We conclude by suggesting directions for future research to improve our understanding of the evolutionary roots of gestures and language.

Red-capped mangabeys (Cercocebus torquatus) adapt their interspecific gestural communication to the recipient's behaviour.

Sensitivity to recipient's attention and responsiveness are critical markers of intentional communication. Although previous research showed that ape gestures can be intentional, few studies have yet addressed this question concerning monkeys. Here, we characterise the effect of a recipient's presence, attentional state and responsiveness on the interspecific gestural communication of captive red-capped mangabeys (Cercocebus torquatus). Previous reports showed that they produced learnt begging gestures towards a human recipient preferentially when the latter was facing them. We used here a novel setup that allows subjects to move around an experimenter and to use different modalities (visual and acoustic) to communicate. We found that when the recipient was not facing them, mangabeys moved to a position in the visual field of their recipient rather than using attention-getters. Interestingly, unlike apes, they did not elaborate their communication visually or acoustically when the experimenter did not respond favourably to their begging. However, our results may suggest that begging gestures were goal-directed, since mangabeys inhibited them when the experimenter was not available to answer immediately (i.e. give a reward). Overall, red-capped mangabeys' interspecific visual communication presented intentionality features, but their use of begging gestures was less flexible than that of great apes in similar situations.

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.

Visual laterality responses to different emotive stimuli by red-capped mangabeys, Cercocebus torquatus torquatus.

Hemispheric asymmetry in emotional perception has been put forward by different theories as the right hemisphere theory or the valence theory. But no consensus was found about the role played by both hemispheres. So, in order to test the different theories, we investigated preferential use of one eye in red-capped mangabeys, at the individual as well as at the group level. In this study we investigated the influence of the emotional value of stimuli on the direction and strength of visual preference of 14 red-capped mangabeys. Temporal stability of the bias of use of a given eye was evaluated by comparing our current results to those obtained 2.5 months previously. Two experimental devices, a tube and a box, tested five different stimuli: four food types varying in palatability and a neutral stimulus. The subjects' food preferences were evaluated before testing the laterality. The mangabeys used their left eyes predominantly at the group level for the tube task. The majority of the subjects showed a visual preference at the individual level for the box task, but this bias was not present at the group level. As the palatability of the stimuli increased, the number of lateralized subjects and the number of subjects using preferentially their left eye increased. Similarly, the strength of laterality was related to food preference. Strength of laterality was significantly higher for subjects using their left eye than for subjects using their right eye. Preferential use of a given eye was stable over short periods 2.5 months later. Our data agree with reports on visual laterality for other species. Our results support the valence theory of a hemispheric sharing of control of emotions in relation to their emotional value.

Socially dependent auditory laterality in domestic horses (Equus caballus).

Laterality is now known to be an ubiquitous phenomenon among the vertebrates. Particularly, laterality of auditory processing has been demonstrated in a variety of species, especially songbirds and primates. Such a hemispheric specialization has been shown to depend on factors such as sound structure, species specificity and types of stimuli. Much less is known on the possible influence of social familiarity although a few studies suggest such an influence. Here we tested the influence of the degree of familiarity on the laterality of the auditory response in the domestic horse. This species is known for its social system and shows visible reactions to sounds, with one or two ears moving towards a sound source. By comparing such responses to the playback of different conspecific whinnies (group member, neighbor and stranger), we could demonstrate a clear left hemisphere (LH) preference for familiar neighbor calls while no preference was found for group member and stranger calls. Yet, we found an opposite pattern of ear side preference for neighbor versus stranger calls. These results are, to our knowledge, the first to demonstrate auditory laterality in an ungulate species. They open further lines of thought on the influence of the social "value" of calls and the listener's arousal on auditory processing and laterality.

Horse (Equus caballus) whinnies: a source of social information.

Many animal species that rely mainly on calls to communicate produce individual acoustic structures, but we wondered whether individuals of species better known as visual communicants, with small vocal repertoires, would also exhibit individual distinctiveness in calls. Moreover, theoretical advances concerning the evolution of social intelligence are usually based on primate species data, but relatively little is known about the social cognitive capacities of non-primate mammals. However, some non-primate species demonstrate auditory recognition of social categories and possess mental representation of their social network. Horses (Equus caballus) form stable social networks and although they display a large range of visual signals, they also use long-distance whinny calls to maintain contact. Here, we investigated the potential existence of individual acoustic signatures in whinny calls and the ability of horses to discriminate by ear individuals varying in their degree of familiarity. Our analysis of the acoustic structure of whinnies of 30 adult domestic horses (ten stallions, ten geldings, ten mares) revealed that some of the frequency and temporal parameters carried reliable information about the caller's sex, body size and identity. However, no correlations with age were found. Playback experiments evaluated the behavioural significance of this variability. Twelve horses heard either control white noise or whinnies emitted by group members, familiar neighbours or unfamiliar horses. While control sounds did not induce any particular response, horses discriminated the social category of the callers and reacted with a sound-specific behaviour (vigilance and attraction varied with familiarity). Our results support the existence of social knowledge in horses and suggest a process of vocal coding/decoding of information.