Reaching around barriers: the performance of the great apes and 3–5-year-old children

Inhibitory control has been suggested as a key predictive measure of problem-solving skills in human and nonhuman animals. However, there has yet to be a direct comparison of the inhibitory skills of the nonhuman apes and their development in human children. We compared the inhibitory skills of all great ape species, including 3–5-year-old children in a detour-reaching task, which required subjects to avoid reaching directly for food and instead use an indirect reaching method to successfully obtain the food. We tested 22 chimpanzees, 18 bonobos, 18 orangutans, 6 gorillas and 42 children. Our sample included chimpanzees, bonobos and orangutans housed in zoos (N = 27) and others housed in sanctuaries in their native habitats (N = 37). Overall, orangutans were the most skilful apes, including human children. As expected older children outperformed younger children. Sanctuary chimpanzees and bonobos outperformed their zoo counterparts whereas there was no difference between the two orangutan samples. Most zoo chimpanzees and bonobos failed to solve the original task, but improved their performance with additional training, although the training method determined to a considerable extent the level of success that the apes achieved in a transfer phase. In general, the performance of the older children was far from perfect and comparable to some of the nonhuman apes tested.     

Comparative and familial analysis of handedness in great apes

Historically, population-level handedness has been considered a hallmark of human evolution. Whether nonhuman primates exhibit population-level handedness remains a topic of considerable debate. This paper summarizes published data on handedness in great apes. Comparative analysis indicated that chimpanzees and bonobos show population-level right handedness, whereas gorillas and orangutans do not. All ape species showed evidence of population-level handedness when considering specific tasks. Familial analyses in chimpanzees indicated that offspring and maternal (but not paternal) handedness was significantly positively correlated, but this finding was contingent upon the classification criteria used to evaluate hand preference. Overall, the proportion of right handedness is lower in great apes compared with humans, and various methodological and theoretical explanations for this discrepancy are discussed.     

Chimpanzees and bonobos exhibit divergent spatial memory development

Spatial cognition and memory are critical cognitive skills underlying foraging behaviors for all primates. While the emergence of these skills has been the focus of much research on human children, little is known about ontogenetic patterns shaping spatial cognition in other species. Comparative developmental studies of nonhuman apes can illuminate which aspects of human spatial development are shared with other primates, versus which aspects are unique to our lineage. Here we present three studies examining spatial memory development in our closest living relatives, chimpanzees (Pan troglodytes) and bonobos (P. paniscus). We first compared memory in a naturalistic foraging task where apes had to recall the location of resources hidden in a large outdoor enclosure with a variety of landmarks (Studies 1 and 2). We then compared older apes using a matched memory choice paradigm (Study 3). We found that chimpanzees exhibited more accurate spatial memory than bonobos across contexts, supporting predictions from these species’ different feeding ecologies. Furthermore, chimpanzees – but not bonobos – showed developmental improvements in spatial memory, indicating that bonobos exhibit cognitive paedomorphism (delays in developmental timing) in their spatial abilities relative to chimpanzees. Together, these results indicate that the development of spatial memory may differ even between closely related species. Moreover, changes in the spatial domain can emerge during nonhuman ape ontogeny, much like some changes seen in human children.     

Physical intuitions about support relations in monkeys (Macaca fuscata) and apes (Pan troglodytes)

Nonhuman primates, like humans, have demonstrated various physical intuitions. Cacchione and Krist (2004) examined chimpanzees' intuitions about support relations with the violation-of-expectation task. They reported that the chimpanzees possessed intuitions about support, but their intuitions differed from those of humans in part; they were sensitive to "contact/no-contact" and "amount of contact" but not "type of contact" rule. To further explore intuitions about support in nonhuman primates, we conducted similar experiments on monkeys (Japanese monkeys) and apes (chimpanzees). In three experiments, we presented physically possible and impossible events of different support relations to the participants and measured their looking times. The results reveal that the chimpanzees and monkeys detect the violations of "contact/no-contact" and "amount of contact" but not "type of contact" variable. Therefore, the apes and monkeys possess similar intuitions; however, these intuitions differ in part from those of humans. The present study provides new and corroborative evidence of intuitions about support in nonhuman primates. However, this again leads to the question of distinctive understanding about support relations among primate species.     

Lateralized scratching in chimpanzees (Pan troglodytes): Evidence of a functional asymmetry during arousal

This study evaluated laterality in scratching by chimpanzees (n = 89) during socially arousing circumstances. Hand use and the side of the body scratched was recorded during a baseline and experimental condition. In the experimental condition, chimpanzees were shown a video of other conspecifics sharing, fighting over, and consuming a watermelon. Self-touches were categorized as either rubs or scratches. The chimpanzees showed a significant right hand bias for rubbing and also significantly directed the rubs to the right side of the body. For scratching, the chimpanzees showed no hand preference but a significant bias for scratching on the left side of the body. These results support the view that the right hemisphere regulates the autonomic nervous system during arousal.     

What limits tool use in nonhuman primates? Insights from tufted capuchin monkeys (Sapajus spp.) and chimpanzees (Pan troglodytes) aligning three-dimensional objects to a surface

Perceptuomotor functions that support using hand tools can be examined in other manipulation tasks, such as alignment of objects to surfaces. We examined tufted capuchin monkeys’ and chimpanzees’ performance at aligning objects to surfaces while managing one or two spatial relations to do so. We presented six subjects of each species with a single stick to place into a groove, two sticks of equal length to place into two grooves, or two sticks joined as a T to place into a T-shaped groove. Tufted capuchins and chimpanzees performed equivalently on these tasks, aligning the straight stick to within 22.5° of parallel to the groove in approximately half of their attempts to place it, and taking more attempts to place the T stick than two straight sticks. The findings provide strong evidence that tufted capuchins and chimpanzees do not reliably align even one prominent axial feature of an object to a surface, and that managing two concurrent allocentric spatial relations in an alignment problem is significantly more challenging to them than managing two sequential relations. In contrast, humans from 2 years of age display very different perceptuomotor abilities in a similar task: they align sticks to a groove reliably on each attempt, and they readily manage two allocentric spatial relations concurrently. Limitations in aligning objects and in managing two or more relations at a time significantly constrain how nonhuman primates can use hand tools.     

Keeping track of time: evidence for episodic-like memory in great apes

Episodic memory, as defined by Tulving, can be described in terms of behavioural elements (what, where and when information) but it is also accompained by an awareness of one’s past (chronesthesia) and a subjective conscious experience (autonoetic awareness). Recent experiments have shown that corvids and rodents recall the where, what and when of an event. This capability has been called episodic-like memory because it only fulfils the behavioural criteria for episodic memory. We tested seven chimpanzees, three orangutans and two bonobos of various ages by adapting two paradigms, originally developed by Clayton and colleagues to test scrub jays. In Experiment 1, subjects were fed preferred but perishable food (frozen juice) and less preferred but non-perishable food (grape). After the food items were hidden, subjects could choose one of them either after 5 min or 1 h. The frozen juice was still available after 5 min but melted after 1 h and became unobtainable. Apes chose the frozen juice significantly more after 5 min and the grape after 1 h. In Experiment 2, subjects faced two baiting events happening at different times, yet they formed an integrated memory for the location and time of the baiting event for particular food items. We also included a memory task that required no temporal encoding. Our results showed that apes remember in an integrated fashion what, where and when (i.e., how long ago) an event happened; that is, apes distinguished between different events in which the same food items were hidden in different places at different times. The temporal control of their choices was not dependent on the familiarity of the platforms where the food was hidden. Chimpanzees’ and bonobos’ performance in the temporal encoding task was age-dependent, following an inverted U-shaped distribution. The age had no effect on the performance of the subjects in the task that required no temporal encoding.     

A competitive nonverbal false belief task for children and apes

A nonverbal false belief task was administered to children (mean age 5 years) and two great ape species: chimpanzees (Pan troglodytes) and bonobos (Pan paniscus). Because apes typically perform poorly in cooperative contexts, our task was competitive. Two versions were run: in both, a human competitor witnessed an experimenter hide a reward in one of two containers. When the competitor then left the room (version A) or turned around (version B), the experimenter switched the locations of the containers. The competitor returned and reached with effort, but unsuccessfully, towards the incorrect container. Children displayed an understanding of the competitor's false belief by correctly choosing the other container to find the reward. Apes did not. However, in version A (but not version B), apes looked more often at the unchosen container in false belief trials than in true belief control trials, possibly indicating some implicit or uncertain understanding that needs to be investigated further.     

The “Sh-Ape Bias” in Non-Linguistic Categorization: Comparisons between Children and Other Apes

ABSTRACT

Children show a bias toward information about shape when labeling or determining category membership for novel objects. The body of work with human children suggests that the shape bias is not restricted to linguistic contexts but is highly contingent on task demands. Testing nonhumans could provide additional information about the salience of shape cues in the absence of linguistic relevance. In order to assess the salience of shape versus color using an identical task in children and apes, we presented two adult zoo-housed chimpanzees (Pan troglodytes) and 56 three–five-year-old children with a relational matching task in which samples and comparison stimuli matched on either shape or color. Whereas children of all ages performed above chance on the task, chimpanzees performed at close to chance levels overall. However, closer inspection revealed that, whereas children performed better on shape (86%) versus color trials (78.5%), chimpanzees showed the opposite pattern, performing at chance on shape trials (49%) and above chance on color trials (72%). Children also made quicker responses on shape versus color trials, whereas chimpanzees showed the opposite pattern. Whereas shape is a highly salient cue for Western children, color may be a more salient natural cue in nonhuman primates’ natural environments. Thus, the shape bias does not appear to be an evolutionarily ancient bias when assigning category membership.     

Encouraging pointing with the right hand,but not the left hand,gives right-handed 3-year-olds a linguistic advantage

Previous research has shown a strong positive association between right-handed gesturing and vocabulary development. However, the causal nature of this relationship remains unclear. In the current study, we tested whether gesturing with the right hand enhances linguistic processing in the left hemisphere, which is contralateral to the right hand. We manipulated the gesture hand children used in pointing tasks to test whether it would affect their performance. In either a linguistic task (verb learning) or a non-linguistic control task (memory), 131 typically developing right-handed 3-year-olds were encouraged to use either their right hand or left hand to respond. While encouraging children to use a specific hand to indicate their responses had no effect on memory performance, encouraging children to use the right hand to respond, compared to the left hand, significantly improved their verb learning performance. This study is the first to show that manipulating the hand with which children are encouraged to gesture gives them a linguistic advantage. Language lateralization in healthy right-handed children typically involves a dominant left hemisphere. Producing right-handed gestures may therefore lead to increased activation in the left hemisphere which may, in turn, facilitate forming and accessing lexical representations. It is important to note that this study manipulated gesture handedness among right-handers and does therefore not support the practice of encouraging children to become right-handed in manual activities.

Research Highlights

• Right-handed 3-year-olds were instructed to point to indicate their answers exclusively with their right or left hand in either a memory or verb learning task.
• Right-handed pointing was associated with improved verb generalization performance, but not improved memory performance.
• Thus, gesturing with the right hand, compared to the left hand, gives right-handed 3-year-olds an advantage in a linguistic but not a non-linguistic task.
• Right-handed pointing might lead to increased activation in the left hemisphere and facilitate forming and accessing lexical representations.

     

Monkeys perform as well as apes and humans in a size discrimination task

Whether the cognitive competences of monkeys and apes are rather similar or whether the larger-brained apes outperform monkeys in cognitive experiments is a highly debated topic. Direct comparative analyses are therefore essential to examine similarities and differences among species. We here compared six primate species, including humans, chimpanzees, bonobos, gorillas (great apes), olive baboons, and long-tailed macaques (Old World monkeys) in a task on fine-grained size discrimination. Except for gorillas, subjects of all taxa (i.e. humans, apes, and monkeys) were able to discriminate three-dimensional cubes with a volume difference of only 10 % (i.e. cubes of 50 and 48 mm side length) and performed only slightly worse when the cubes were presented successively. The minimal size discriminated declined further with increasing time delay between presentations of the cubes, highlighting the difficulty to memorize exact size differences. The results suggest that differences in brain size, as a proxy for general cognitive abilities, did not account for variation in performance, but that differential socio-ecological pressures may better explain species differences. Our study highlights the fact that differences in cognitive abilities do not always map neatly onto phylogenetic relationships and that in a number of cognitive experiments monkeys do not fare significantly worse than apes, casting doubt on the assumption that larger brains per se confer an advantage in such kinds of tests.     

Performance on the Hamilton search task,and the influence of lateralization,in captive orange-winged Amazon parrots (Amazona amazonica)

Psittacines are generally considered to possess cognitive abilities comparable to those of primates. Most psittacine research has evaluated performance on standardized complex cognition tasks, but studies of basic cognitive processes are limited. We tested orange-winged Amazon parrots (Amazona amazonica) on a spatial foraging assessment, the Hamilton search task. This task is a standardized test used in human and non-human primate studies. It has multiple phases, which require trial and error learning, learning set breaking, and spatial memory. We investigated search strategies used to complete the task, cognitive flexibility, and long-term memory for the task. We also assessed the effects of individual strength of motor lateralization (foot preference) and sex on task performance. Almost all (92 %) of the parrots acquired the task. All had significant foot preferences, with 69 % preferring their left foot, and showed side preferences contralateral to their preferred limb during location selection. The parrots were able to alter their search strategies when reward contingencies changed, demonstrating cognitive flexibility. They were also able to remember the task over a 6-month period. Lateralization had a significant influence on learning set acquisition but no effect on cognitive flexibility. There were no sex differences. To our knowledge, this is the first cognitive study using this particular species and one of the few studies of cognitive abilities in any Neotropical parrot species.     

Not here,there! Possible referential gesturing during allogrooming by wild bonnet macaques, <Emphasis Type="Italic">Macaca radiata</Emphasis>

Intentional referential gestures, a fundamental building block of symbolic human language, have been reported from a range of species, including non-human primates. While apes are known to spontaneously use intentional gestures, only captive macaques, amongst non-ape primates, appear to intentionally display learnt gestures. On the other hand, referential gestures have so far been reported only in chimpanzees, amongst non-human primates. We document here, for the first time, potentially referential gesturing, used intentionally as well, in a monkey species, the bonnet macaque Macaca radiata, in the wild. Bonnet macaques use four distinct actions during allogrooming, possibly to indicate a particular body part intended to be groomed. These acts were successful in drawing the recipients’ attention to the indicated part, which they began to groom subsequently. This study enriches our understanding of non-ape primate gestural communication and adds to the growing evidence for early human language-like capacities in non-human species.     

Chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) quantify split solid objects

Recent research suggests that gorillas’ and orangutans’ object representations survive cohesion violations (e.g., a split of a solid object into two halves), but that their processing of quantities may be affected by them. We assessed chimpanzees’ (Pan troglodytes) and bonobos’ (Pan paniscus) reactions to various fission events in the same series of action tasks modelled after infant studies previously run on gorillas and orangutans (Cacchione and Call in Cognition 116:193–203, 2010b). Results showed that all four non-human great ape species managed to quantify split objects but that their performance varied as a function of the non-cohesiveness produced in the splitting event. Spatial ambiguity and shape invariance had the greatest impact on apes’ ability to represent and quantify objects. Further, we observed species differences with gorillas performing lower than other species. Finally, we detected a substantial age effect, with ape infants below 6 years of age being outperformed by both juvenile/adolescent and adult apes.     

Bonobos and orangutans,but not chimpanzees,flexibly plan for the future in a token-exchange task

Non-human animals, including great apes, have been suggested to share some of the skills for planning that humans commonly exhibit. A crucial difference between human and non-human planning may relate to the diversity of domains and needs in which this skill is expressed. Although great apes can save tools for future use, there is little evidence yet that they can also do so in other contexts. To investigate this question further, we presented the apes with a planning token-exchange task that differed from standard tool-use tasks. Additionally, we manipulated the future outcome of the task to investigate planning flexibility. In the Exchange condition, subjects had to collect, save and transport tokens because they would need them 30 min later to exchange them for food with a human, i.e., “bring-back” response. In the Release condition, the collection and transport of tokens were not needed as no exchange took place after 30 min. Out of 13 subjects, eight solved the task at least once in the Exchange condition, with chimpanzees appearing less successful than the other species. Importantly, three individuals showed a clear differential response between conditions by producing more “bring-back” responses in the Exchange than in the Release conditions. Those bonobo and orangutan individuals hence adapted their planning behavior according to changing needs (i.e., they brought tokens back significantly more often when they would need them). Bonobos and orangutans, unlike chimpanzees, planned outside the context of tool-use, thus challenging the idea that planning in these species is purely domain-specific.     

Short-Term Kinesthetic Training for Sensorimotor Rhythms: Effects in Experts and Amateurs

The authors’ aim was to examine whether short-term kinesthetic training affects the level of sensorimotor rhythm (SMR) in different frequency band: alpha (8–12 Hz), lower beta (12.5–16 Hz) and beta (16.5–20 Hz) during the execution of a motor imagery task of closing and opening the right and the left hand by experts (jugglers, practicing similar exercises on an everyday basis) and amateurs (individuals not practicing any sports). It was found that the performance of short kinesthetic training increases the power of alpha rhythm when executing imagery tasks only in the group of amateurs. Therefore, kinesthetic training may be successfully used as a method increasing the vividness of motor imagery, for example, in tasks involving the control of brain–computer interfaces based on SMR.     

Primates do not spontaneously use shape properties for object individuation: a competence or a performance problem?

Several recent studies have documented that non-human primates can individuate objects according to property and/or kind information in much the same way as human infants do from around one year of age when they begin to acquire language. Some studies suggest, however, that only some properties are used for the individuation of food items: color, but not shape. The present study investigated whether these findings reveal a true competence problem with shape properties in the food domain or whether they merely reveal a performance problem (e.g., lack of attention to shapes). We tested 25 great apes (chimpanzees, bonobos and gorillas) in two food individuation tasks. We manipulated subjects’ experience with differences in color and shape properties of food items. Results indicated (i) that all subjects, regardless of their prior experience, solved the color-based object individuation task and (ii) that only the group with previous experience with different shape properties succeeded in the shape-based individuation task. Great apes can thus be primed to take shape into account for individuating food objects, and this results clearly speaks in favor of a performance (rather than a competence) problem in using shape for object individuation of food items.     

Influence of personality,age, sex,and estrous state on chimpanzee problem-solving success

Despite the importance of individual problem solvers for group- and individual-level fitness, the correlates of individual problem-solving success are still an open topic of investigation. In addition to demographic factors, such as age or sex, certain personality dimensions have also been revealed as reliable correlates of problem-solving by animals. Such correlates, however, have been little-studied in chimpanzees. To empirically test the influence of age, sex, estrous state, and different personality factors on chimpanzee problem-solving, we individually tested 36 captive chimpanzees with two novel foraging puzzles. We included both female (N = 24) and male (N = 12) adult chimpanzees (aged 14–47 years) in our sample. We also controlled for the females’ estrous state—a potential influence on cognitive reasoning—by testing cycling females both when their sexual swelling was maximally tumescent (associated with the luteinizing hormone surge of a female’s estrous cycle) and again when it was detumescent. Although we found no correlation between the chimpanzees’ success with either puzzle and their age or sex, the chimpanzees’ personality ratings did correlate with responses to the novel foraging puzzles. Specifically, male chimpanzees that were rated highly on the factors Methodical, Openness (to experience), and Dominance spent longer interacting with the puzzles. There was also a positive relationship between the latency of females to begin interacting with the two tasks and their rating on the factor Reactivity/Undependability. No other significant correlations were found, but we report tentative evidence for increased problem-solving success by the females when they had detumescent estrous swellings.     

Binaural loudness gain measured by simple reaction time

In order to yield equal loudness, different studies using scaling or matching methods have found binaural level differences between monaural and diotic presentations ranging from less than 2 dB to as much as 10 dB. In the present study, a reaction time methodology was employed to measure the binaural level difference producing equal reaction time (BLDERT). Participants had to respond to the onset of 1-kHz pure tones with sound pressure levels ranging from 45 to 85 dB, and being presented to the right, the left, or both ears. Equal RTs for monaural and diotic presentation (BLDERTs) were obtained with a level difference of approximately 5 dB. A second experiment showed that different results obtained for the left and right ear are largely due to the responding hand, with ipsilateral responses being faster than contralateral ones. A third experiment investigated the BLDERT for dichotic stimuli, tracing the transition between binaural and monaural stimulation. The results of all three RT experiments are consistent with current models of binaural loudness and contradict earlier claims of perfect binaural summation.     

Bimanual coupling effects during arm immobilization and passive movements

When humans simultaneously perform different movements with both hands, each limb movement interferes with the contralateral limb movement (bimanual coupling). Previous studies on both healthy volunteers and patients with central or peripheral nervous lesions suggested that such motor constraints are tightly linked to intentional motor programs, rather than to movement execution. Here, we aim to investigate this phenomenon, by using a circles-lines task in which, when subjects simultaneously draw lines with the right hand and circles with the left hand, both the trajectories tend to become ovals (bimanual coupling effect). In a first group, we immobilized the subjects’ left arm with a cast and asked them to try to perform the bimanual task. In a second group, we passively moved the subjects’ left arm and asked them to perform voluntary movements with their right arm only. If the bimanual coupling arises from motor intention and planning rather than spatial movements, we would expect different results in the two groups. In the Blocked group, where motor intentionality was required but movements in space were prevented by immobilization of the arm, a significant coupling effect (i.e., a significant increase of the ovalization index for the right hand lines) was found. On the contrary, in the Passive group, where movements in space were present but motor intentionality was not required, no significant coupling effect was observed. Our results confirmed, in healthy subjects, the central role of the intentional and predictive operations, already evidenced in pathological conditions, for the occurrence of bimanual coupling.