Posture and reaching in tufted capuchins (Cebus apella)

This research investigated the effects of posture on lateral bias for food reaching in tufted capuchin monkeys ( Cebus apella ) by comparing hand preferences for quadrupedal and bipedal reaching. Several findings of this investigation warrant discussion. First, we found a population-level bias towards use of the right hand for bipedal reaching but not for quadrupedal reaching. Second, adults exhibited a greater right-hand preference for bipedal reaching than did immatures. Third, subjects showed a greater right-hand preference, and a greater strength of preference independent of direction, for bipedal reaching than for quadrupedal reaching. Fourth, we found a significant positive relation between the direction of hand preference for quadrupedal and bipedal reaching. We believe that capuchins provide an alternative primate model to chimpanzees for the evolution of human bipedalism and right-handedness. One implication of this model is that righthandedness emerged in hominids prior to extensive expansion of brain size and elaboration of material culture.     

The cerebellum and its contribution to complex tasks in higher primates: A comparative perspective

Many aspects of the involvement of the cerebellum in motor control and cognition are still quite unclear or relatively unexplored. In particular, very little is known about the evolution of cerebellar contribution to complex behavior in higher primate species. In this paper, we provide an overview of existing and ongoing comparative studies of the role of the cerebellum in primate behavior. In particular, we discuss evidence that great apes show greater cerebellar relative size than monkeys and that such interspecific difference is mainly explained by growth of the lateral neocerebellum in evolution with converse changes in the vermis. Furthermore, we present evidence that volumetric differences as well as lateral asymmetry of the cerebellum are related to both performance and hand preference for skilled tasks like tool use and aimed throwing. Finally we suggest future directions for this comparative research area that may offer further valuable clues into the involvement of the cerebellum in complex behavior and its evolutionary origin in primate species.     

Pattern recognition in tufted capuchin monkeys (Cebus apella): the role of the spatial organisation of stimulus parts

We report four experiments aimed at characterising the role played by the encoding of the spatial relationship between stimulus parts in pattern recognition in capuchin monkeys, as assessed by a matching to sample task. The results of the first experiment, which were also reliably replicated at different stages in the course of the study, indicated that the simultaneous rotation and/or translation of the four parts into which the stimuli were divided, but not a global rotation of the entire stimulus, impaired matching performance in capuchin monkeys. Experiments two and three showed that matching performance was not impaired following similar manipulations of a subset of one, two or three parts. In experiment four, the same task was presented to human subjects. The same pattern of results emerged for humans and monkeys in trials where all the four stimulus parts were presented. However, the matching performance of humans was affected more than that of capuchin monkeys when only a subset of stimulus parts was featured in the task. These results support the conclusion that the matching performance of capuchin monkeys is affected by the rearrangement of stimulus parts and, as such it seems to rely on global properties of the stimulus such as the spatial relationships of the component parts. However, the remarkable ability of capuchin monkeys to identify a stimulus on the basis of a subset of parts suggests that the reliance on the global properties of the stimuli may not be pervasive as it is in humans.     

Plasticity of lateralization: schooling predicts hand preference but not hand skill asymmetry in a non-industrial society

Considerable variation in the frequency of left-handedness between cultures has been reported, ranging from 0.5 to 24%. This variation in hand preference may have evolved under natural or cultural selection. It has been suggested that schooling affects handedness but as in most human societies only a selected and minor part of the population does not attend school this is difficult to test. We investigated to what extent schooling affects both hand preference and asymmetry in hand skill in a non-industrial population in the highlands of New Guinea. This provided unique opportunities because of the relatively recent establishment of a primary school in this population, and where people still live a non-industrial traditional life reflecting conditions in which handedness may have evolved. We interviewed 620 inhabitants (aged 5-70 y) to collect demographic data and school history, tested hand preference on 10 ecologically relevant activities, and measured performance of each hand on three tasks (pegboard, grip force, ball throwing). Schooled individuals were overall faster in fine motor performance, had greater grip strength and greater throwing accuracy. This suggests that there is implicit selection on the fitter part of the population to enter school. Schooling is associated with hand preference, as schooled individuals were more likely to be extremely right-handed and less likely to be strongly right-handed, but not with asymmetry of hand skill (controlled for sex and age). Developmental plasticity in hand preference but not skill asymmetry, and the weak correlations between hand preference and hand skill asymmetry indicate that they represent different aspects of brain lateralization. Furthermore, the weak correlations between hand preference and hand skill asymmetry leave room for moderating factors such as schooling, sex and age to have a differential effect on hand preference and hand skill, and each needs to be studied in its own right.     

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.     

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.     

Right-hand superiority for throwing but not for intercepting

In humans, the organization of movements performed by both upper limbs, relies significantly on a left hemisphere "praxis" system that also subsumes speech function. Right hand preference may also be an expression of this left hemisphere dependence, arising from the preferential connections of the right hand to the left hemisphere. Consequently, a manual task that maximizes the spatial complexity of a target (presumably engaging right hemisphere mechanisms), while concurrently minimizing motor-programming demands, was expected to yield a diminished disparity in preference and performance between the hands. Left and right hand accuracy were measured independently for two motor tasks in 48 normal right-handed university students. In the first task, darts were thrown overhand at a stationary target. For the second task, subjects were asked to use the open hand to block (but not catch) projectiles launched at varying trajectories and velocities. ANOVA yielded a significant Hand x Task interaction, in which the left hand did not differ from the right hand in intercepting ability, but was significantly less accurate than the right hand for throwing. A sex difference favouring males was found for both tasks; this difference was not reducible to differences in physique or athleticism.     

Manual laterality in Campbell's Monkeys (Cercopithecus c. campbelli) in spontaneous and experimental actions

Behavioural asymmetries, once thought to be exclusively human, appear to be widespread in vertebrates. A population-level bias should stem from natural selection and reflect a cerebral dominance, while individual preferences might be linked to individual characteristics. Manual laterality has been extensively investigated in non-human primates. However, despite a strong data base, no general patterns have emerged, resulting in a few explanatory theories and little consensus. This study was interested in manual laterality in 12 Campbell's monkeys (Cercopithecus c. campbelli). Several theories were examined, using both direct behavioural observations during feeding behaviour and six controlled experimental conditions, in which we varied task demands to investigate the effect of two factors. We systematically varied the individual posture (sat, tripedal, bipedal, clung) and the complexity of the task (box with or without a lid to open). Concerning the direction of preference, we found individual and action-specific preferences for experimental actions, which match previous reports. No population bias emerged and each subject appeared to react differently to the factors, hereby contradicting the theories. However, concerning the strength of preference, all individuals tended to be affected in similar ways. Spontaneous actions were less lateralized than experimental ones, and the simplest task and spontaneous category tended to show the weakest laterality. The relative complexity and novelty of these actions may account for these results.     

Between-species variation in the development of hand preference among macaques

This research examined between-species variation in the development of hand preference among Macaca. Specifically, we examined hand preference using juveniles and adults of three macaque species that differ in social and reactive tendencies in order to examine whether the correlation between temperament and handedness that has been noted within Macaca mulatta occurs between closely related species. Each of the species studied exhibited a different pattern of hand preference development. Both juvenile and adult M. mulatta exhibited group-level left-hand bias. Juvenile Macaca nemestrina were not biased towards either hand at the group-level, whereas adults exhibited a group-level left-hand bias. Neither juvenile nor adult Macaca fascicularis exhibited manual bias at the group-level. Analysis of variance indicated statistically significant main effects of species and age class on hand preference measures. Post-hoc analysis indicated greater use of the left- versus right-hand, and greater hand preference strength independent of direction, among M. mulatta and M. nemestrina than among M. fascicularis, and among adults than among juveniles. These results indicate significant between-species variation in the development of hand preference within the genus Macaca, and are inconsistent with any one single-factor theory yet offered to explain the etiology of primate laterality. We hypothesize that the relationship between handedness and temperament that has been shown within M. mulatta may generalize across closely related primate species.     

Wait wait,don't tell me: Handedness questionnaires do not predict hand preference for grasping

Handedness questionnaires are a common screening tool in psychology and neuroscience, used whenever a participant's performance on a given task may conceivably be affected by their laterality. Two widely-used examples of such questionnaires are the Edinburgh Handedness Inventory and the Waterloo Handedness Questionnaire. Both instruments ask respondents to report their hand preference for performing a variety of common tasks (e.g., throwing a ball, or opening a drawer). Here we combined questions from the two instruments (E-WHQ; 22 questions total) and asked participants to report their preferred hand for each via a five-point scale. The purpose of this study was to determine whether responses on the E-WHQ are accurate, reliable, and/or predictive of hand-preference for a simple grasp-to-construct task. Regarding accuracy, handedness scores were 5% lower when participants used a scrambled response key versus a consistent one. Test-retest reliability of the questionnaire was weak, with any given inventory item eliciting a different response from 34% of respondents upon retesting. Neither was the E-WHQ predictively useful—although both left- and right-handers preferred their dominant hands, E-WHQ score did not correlate with overall percentage of dominant-hand grasps in either group. We conclude that the E-WHQ is unsuited for predicting hand preference for grasping.     

Local advantage in the visual processing of hierarchical stimuli following manipulations of stimulus size and element numerosity in monkeys (Cebus apella)

Previous studies suggest that monkeys process local elements of hierarchical visual patterns more quickly and more accurately than they process the global shape. These results could be indicative of differences between relatively high visual functions of humans and non-human primates. It is, however, important to rule out that relatively low-level factors can explain these differences. We addressed this issue with two experiments carried out on capuchin monkeys (Cebus apella) using matching-to-sample tasks featuring hierarchical stimuli. The first experiment assessed whether manipulations of stimulus size can affect the local advantage so far observed in this New World monkey species. An overall local versus global advantage still emerges in capuchins, irrespectively of the amplitude of the visual angle subtended by the hierarchical shapes. Moreover, a local-to-global interference, indicative of a strong local advantage, was observed for the first time. In the second experiment, we manipulated size and numerosity of the local elements of hierarchical patterns, mimicking procedures that in human perception relegate the local elements to texture and enhance a global advantage. Our results show that in capuchin monkeys, a local advantage emerges clearly even when these procedures are used. These results are of interest since extensive neurophysiological research is carried out on non-human primate vision, often taking for granted a similarity of visual skills in human and non-human primates. These behavioural results show that this assumption is not always warranted and that more research is needed to clarify the differences in the processes involved in basic visual skills among primates.     

Brain lateralisation and motor learning: Selective effects of dominant and non-dominant hand practice on the early acquisition of throwing skills

Findings from neurosciences indicate that the two brain hemispheres are specialised for the processing of distinct movement features. How this knowledge can be useful in motor learning remains unclear. Two experiments were conducted to investigate the influence of initial practice with the dominant vs non-dominant hand on the acquisition of novel throwing skills. Within a transfer design two groups practised a novel motor task with the same amount of practice on each hand, but in opposite hand-order. In Experiment 1, participants acquired the position throw in basketball, which places high demands on throwing accuracy. Participants practising this task with their non-dominant hand first, before changing to the dominant hand, showed better skill acquisition than participants practising in opposite order. In Experiment 2 participants learned the overarm throw in team handball, which requires great throwing strength. Participants initially practising with their dominant hand benefited more from practice than participants beginning with their non-dominant hand. These results indicate that spatial accuracy tasks are learned better after initial practice with the non-dominant hand, whereas initial practice with the dominant hand is more efficient for maximum force production tasks. The effects are discussed in terms of brain lateralisation and bilateral practice schedules.     

Sylvian fissure asymmetry in capuchin monkeys (Cebus apella)

Asymmetries of the sylvian fissure (SF) are believed to reflect an enlargement of the posterior temporal lobe, particularly a region that corresponds to part of Wernicke's area in humans. In nonhuman primates the homologue to the region may be involved in the discrimination and processing of species-specific vocalisations. As capuchin monkeys are large-brained, socially complex primates with a rich vocal repertoire, it was hypothesised that they would display asymmetry of the SF. We used high-resolution 3T MRI scans to investigate this asymmetry in 17 brown capuchin monkeys (Cebus apella; 9 males, 8 females). Results indicated a trend towards population-level leftward asymmetry in the lateral region of the SF. Post hoc analyses revealed significant sex differences in SF asymmetry, with females displaying a population-level leftward asymmetry of the lateral region of the SF. Age was a significant mediator of the effects of sex on asymmetry of the lateral region of the SF. These results provide evidence that capuchin monkeys display sex differences in the asymmetry of the SF and show developmental changes in hemispheric lateralisation.     

Assessment of hand preference in two language-trained chimpanzees (Pan troglodytes): A multimethod analysis

Abstract

The nonhuman primate literature concludes that monkeys and apes do not exhibit handedness preferences at the population level. This discrepancy between human and nonhuman primate findings may be due to differences in the methods of assessment of handedness, lack of reliability between various measures of handedness, and a paucity of studies involving great apes. This paper presents the results of extensive hand preference studies with two language-trained chimpanzees (Pan troglodytes). Both naturalistic and experimental paradigms are described. In particular, various methodologic factors involved in handedness assessment, including the use of a hand preference measure previously used with human subjects were examined. Both chimpanzees exhibited a right-hand preference for fine motor tasks requiring manual dexterity.     

Hand clasping, arm folding, and handedness: relationships and strengths of preference

We investigated via a survey the relationship between hand clasping, arm folding, and handedness. We aimed to provide new data on degree of preference for each of these lateralities. We also examined the relative importance of thumb position versus interdigitisation of the fingers in determining one's comfort in a hand-clasping position. We explored this in the context of the fact that sensory acuity is greater for the thumb than other fingers, suggesting that preference for how the fingers are intermeshed may be more influenced by thumb than finger position. Lastly we performed an exploratory analysis to determine if self-reported menstrual phase-known to influence turning bias-also influences hand clasping, arm folding or the strength of one's handedness. Our study suggests that lateral preferences for hand clasping, arm folding, and handedness are independent. However, the degrees of lateral preference for hand clasping and arm folding are correlated. Our exploration of the relative importance of thumbs versus fingers to hand clasping revealed some trends that were not statistically significant, but worth future exploration. Our data on menstrual phase showed a reduced strength of preference for arm folding in mid-luteal females versus non-mid-luteal females.     

Posture and laterality in the bushbaby (Galago senegalensis)

A colony of adult bushbabies was assessed for hand preference in order to determine what the proportion of preference for the left and right might be for the population and whether hand preference for individuals was reliable. 25 animals were tested in an apparatus demanding a vertical stance. The population bias was expressed in a distribution skewed toward a left-hand bias. With 16 animals available for retesting, the test-retest reliability coefficient was 0.651, significant at the 0.01 level. When 12 of the original subjects were tested in an apparatus demanding a quadrupedal stance, hand preference shifted to a bimodal distribution. Test-retest reliability was 0.864, significant at the 0.01 level. Significant correlations were not found between two types of test nor between the two retests. Neither sex nor length of laboratory residence served to predict hand preference. These results were discussed with the view that the postural adjustments required by a bipedal stance may have shaped the development of handedness in humans.     

Effects of pattern redundancy and hierarchical grouping on global-local visual processing in monkeys (Cebus apella) and humans (Homo sapiens)

Using a Matching-To-Sample (MTS) procedure we assessed the effects of stimulus redundancy, defined on the basis of the information-theory approach to shape goodness proposed by Garner (1974) [20], and grouping on the processing of hierarchical visual patterns in capuchin monkeys and humans. In a first experiment, the MTS performance of both capuchin monkeys and humans benefitted from stimulus redundancy. Moreover, a local advantage in capuchins was observed with visual patterns that required grouping at both global and local level. In a second experiment we eliminated the requirement to group at the local level. This was done to determine if the effects of redundancy would have been evident in condition more similar to those used in previous studies of global-local processing in a comparative context. The benefits of stimulus redundancy emerged again in both species but were confined to local processing in monkeys and to global processing in humans. A local advantage was observed in both species. In a third experiment, the reduction of the size of the stimuli and the increase of the quantity of the local elements produced a shift to global dominance in humans but the local dominance in monkeys was preserved. The implications of these results are discussed in relation to other similarities and differences in higher visual functions in humans and monkeys.     

Looking at eye dominance from a different angle: Is sighting strength related to hand preference?

Sighting dominance (the behavioural preference for one eye over the other under monocular viewing conditions) has traditionally been thought of as a robust individual trait. However, Khan and Crawford (2001) have shown that, under certain viewing conditions, eye preference reverses as a function of horizontal gaze angle. Remarkably, the reversal of sighting from one eye to the other depends on which hand is used to reach out and grasp the target. Their procedure provides an ideal way to measure the strength of monocular preference for sighting, which may be related to other indicators of hemispheric specialisation for speech, language and motor function. Therefore, we hypothesised that individuals with consistent side preferences (e.g., right hand, right eye) should have more robust sighting dominance than those with crossed lateral preferences. To test this idea, we compared strength of eye dominance in individuals who are consistently right or left sided for hand and foot preference with those who are not. We also modified their procedure in order to minimise a potential image size confound, suggested by Banks et al. (2004) as an explanation of Khan and Crawford’s results. We found that the sighting dominance switch occurred at similar eccentricities when we controlled for effects of hand occlusion and target size differences. We also found that sighting dominance thresholds change predictably with the hand used. However, we found no evidence for relationships between strength of hand preference as assessed by questionnaire or by pegboard performance and strength of sighting dominance. Similarly, participants with consistent hand and foot preferences did not show stronger eye preference as assessed using the Khan and Crawford procedure. These data are discussed in terms of indirect relationships between sighting dominance, hand preference and cerebral specialisation for language and motor control.     

A mechatronic platform for behavioral analysis on nonhuman primates

In this work we present a new mechatronic platform for measuring behavior of nonhuman primates, allowing high reprogrammability and providing several possibilities of interactions. The platform is the result of a multidisciplinary design process, which has involved bio-engineers, developmental neuroscientists, primatologists, and roboticians to identify its main requirements and specifications. Although such a platform has been designed for the behavioral analysis of capuchin monkeys (Cebus apella), it can be used for behavioral studies on other nonhuman primates and children. First, a state-of-the-art principal approach used in nonhuman primate behavioral studies is reported. Second, the main advantages of the mechatronic approach are presented. In this section, the platform is described in all its parts and the possibility to use it for studies on learning mechanism based on intrinsic motivation discussed. Third, a pilot study on capuchin monkeys is provided and preliminary data are presented and discussed.     

Lateralized preferences and right-left discrimination in the monkey: choice of mirror-image shape, position of recovered food and hand usage.

Rhesus monkeys were tested for lateral preferences during mirror-image shape discrimination and food recovery from a row of pellets. Position of recovered food was unrelated to hand preference or mirror-image preference. There was no significant difference in the number of individuals preferring right and left lateral mirror-image shapes. Individuals tended to retain the same mirror-image preference to the same degree upon repeated testing. Animals of greater weight had stronger preferences. In all these respects, the features of mirror-image preference resembled those previously described for hand preference during a simple reaching task. The strength of different lateral preferences expressed by each animal were not significantly related thus failing to support the concept that asymmetric bodily responses can serve as cues for right-left discrimination in the environment. However, when the direction as well as strength of preference was considered, there appeared to be a tendency for animals to prefer the mirror-image shape whose reward bias was opposite to that of the preferred hand. This finding might have been due to a positional bias though there was evidence against this possibility.