To unravel the causes of major depressive disorder (MDD), the third leading cause of disease burden around the world, ethological animal models have recently been proposed. Our previous studies highlighted a depressive-like profile among single- and socially-housed farm-bred cynomolgus macaques. Although phylogenetically close, cynomolgus and rhesus macaques, the two most commonly used macaque species in biomedical research, differ on several levels such as patterns of aggression, reconciliation, temperament, or dominance styles. The question of whether one captive macaque species was more vulnerable than another in the development of a pathological profile reminiscent of MDD symptoms was explored.
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. (PsycINFO Database Record (c) 2013 APA, all rights reserved).
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.
The central position and universality of music in human societies raises the question of its phylogenetic origin. One of the most important properties of music involves harmonic musical intervals, in response to which humans show a spontaneous preference for consonant over dissonant sounds starting from early human infancy. Comparative studies conducted with organisms at different levels of the primate lineage are needed to understand the evolutionary scenario under which this phenomenon emerged. Although previous research found no preference for consonance in a New World monkey species, the question remained opened for Old World monkeys. We used an experimental paradigm based on a sensory reinforcement procedure to test auditory preferences for consonant sounds in Campbells monkeys (Cercopithecus campbelli campbelli), an Old World monkey species. Although a systematic preference for soft (70 dB) over loud (90 dB) control white noise was found, Campbells monkeys showed no preference for either consonant or dissonant sounds. The preference for soft white noise validates our noninvasive experimental paradigm, which can be easily reused in any captive facility to test for auditory preferences. This would suggest that human preference for consonant sounds is not systematically shared with New and Old World monkeys. The sensitivity for harmonic musical intervals emerged probably very late in the primate lineage.
Olive baboons (Papio anubis) do acquire and use intentional requesting gestures in experimental contexts. Individuals 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.
Adverse early-life experience might lead to the expression of abnormal behaviours in animals and the predisposition to psychiatric disorder (e.g. major depressive disorder) in Humans. Common breeding processes employ weaning and housing conditions different from what happens in the wild.
Social factors play a key role in the structuring of vocal repertoires at the individual level, notably in non-human primates. Some authors suggested that, at the species level too, social life may have driven the evolution of communicative complexity, but this has rarely been empirically tested. Here, we use a comparative approach to address this issue. We investigated vocal variability, at both the call type and the repertoire levels, in three forest-dwelling species of Cercopithecinae presenting striking differences in their social systems, in terms of social organization as well as social structure. We collected female call recordings from twelve De Brazzas monkeys (Cercopithecus neglectus), six Campbells monkeys (Cercopithecus campbelli) and seven red-capped mangabeys (Cercocebus torquatus) housed in similar conditions. First, we noted that the level of acoustic variability and individual distinctiveness found in several call types was related to their importance in social functioning. Contact calls, essential to intra-group cohesion, were the most individually distinctive regardless of the species, while threat calls were more structurally variable in mangabeys, the most "despotic" of our three species. Second, we found a parallel between the degree of complexity of the species social structure and the size, diversity, and usage of its vocal repertoire. Mangabeys (most complex social structure) called twice as often as guenons and displayed the largest and most complex repertoire. De Brazzas monkeys (simplest social structure) displayed the smallest and simplest repertoire. Campbells monkeys displayed an intermediate pattern. Providing evidence of higher levels of vocal variability in species presenting a more complex social system, our results are in line with the theory of a social-vocal coevolution of communicative abilities, opening new perspectives for comparative research on the evolution of communication systems in different animal taxa.
To date, experimental and preclinical studies on neuropsychiatric conditions have almost exclusively been performed in experimentally-induced animal models and have only rarely relied upon an ethological approach where animals have been observed in more naturalistic settings. The laboratory species of choice has been the rodent while the potential of more closely-related non-human primates have remained largely underexplored.
Acoustic variability and individual distinctiveness of vocal signals are expected to vary with both their communicative function and the need for individual recognition during social interactions. So far, few attempts have been made to comparatively study these features across the different call types within a species vocal repertoire. We collected recordings of the six most common call types from 14 red-capped mangabeys (Cercocebus torquatus) to assess intra- and interindividual acoustic variability, using a range of temporal and frequency parameters. Acoustic variability was highest in contact and threat calls, intermediate in food calls, and lowest in loud and alarm calls. Individual distinctiveness was high in contact, threat, loud and alarm calls, and low in food calls. In sum, calls mediating intragroup social interactions were structurally most variable and individually most distinctive, highlighting the key role that social factors must have played in the evolution of the vocal repertoire in this species. We discuss these findings in light of existing hypotheses of acoustic variability in primate vocal behavior.
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.
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 Brazzas 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.
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.
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.
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., subjects 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.
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.
Despite attempts to generalise the left hemisphere-speech association of humans to animal communication, the debate remains open. More studies on primates are needed to explore the potential effects of sound specificity and familiarity. Familiar and non-familiar nonhuman primate contact calls, bird calls and non-biological sounds were broadcast to Japanese macaques. Macaques turned their heads preferentially towards the left (right hemisphere) when hearing conspecific or familiar primates supporting hemispheric specialisation. Our results support the role of experience in brain organisation and the importance of social factors to understand laterality evolution.
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 Campbells 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.
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.
Individuals in social groups monitor many relationships by adapting their activities to the sex, age, social status, behaviour as well as the position of conspecifics. Here, we investigated the influence of the relative positions of the members of two groups of mangabeys on social visual laterality (right/left) and transversality (frontal/rear) in two contexts: (1) one-to-one interactions and (2) a one-to-many context allowing potential observation of all group members. We discuss our data in relation to (1) the influence of rank and (2) theories explaining lateralization of cerebral hemispheres. First, in one-to-one situations, members of both groups were approached more frequently from their left than from their right, and red-capped mangabeys approached a group member more frequently from their right than from their left. In one-to-many situations, red-capped mangabeys kept more group members in their right than their left frontal visual field. Conversely, the social transversality bias was the same in both contexts: the frontal field was favoured. Second, approach side and relative positions differed according to social rank. Mangabeys that were approached more frequently from their left ranked relatively high. The higher an individual ranked, the more it left other group members behind it; on the contrary dominated mangabeys generally remained below other group members. Thus, social structures, as well as relationships within a group, appear to be good candidates to explain social laterality and transversality.
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 listeners arousal on auditory processing and laterality.
The last decades evidenced auditory laterality in vertebrates, offering new important insights for the understanding of the origin of human language. Factors such as the social (e.g. specificity, familiarity) and emotional value of sounds have been proved to influence hemispheric specialization. However, little is known about the crossed effect of these two factors in animals. In addition, human-animal comparative studies, using the same methodology, are rare. In our study, we adapted the head turn paradigm, a widely used non invasive method, on 8-9-year-old schoolgirls and on adult female Campbells monkeys, by focusing on head and/or eye orientations in response to sound playbacks. We broadcast communicative signals (monkeys: calls, humans: speech) emitted by familiar individuals presenting distinct degrees of social value (female monkeys: conspecific group members vs heterospecific neighbours, human girls: from the same vs different classroom) and emotional value (monkeys: contact vs threat calls; humans: friendly vs aggressive intonation). We evidenced a crossed-categorical effect of social and emotional values in both species since only "negative" voices from same class/group members elicited a significant auditory laterality (Wilcoxon tests: monkeys, T = 0 p = 0.03; girls: T = 4.5 p = 0.03). Moreover, we found differences between species as a left and right hemisphere preference was found respectively in humans and monkeys. Furthermore while monkeys almost exclusively responded by turning their head, girls sometimes also just moved their eyes. This study supports theories defending differential roles played by the two hemispheres in primates auditory laterality and evidenced that more systematic species comparisons are needed before raising evolutionary scenario. Moreover, the choice of sound stimuli and behavioural measures in such studies should be the focus of careful attention.
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 callers 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.
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.
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 Campbells 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.
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.
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