Differential use of attentional and visual communicative signaling by orangutans (Pongo pygmaeus) and gorillas (Gorilla gorilla) in response to the attentional status of a human

In this study we investigated the communicative abilities of 10 orangutans (Pongo pygmaeus) and seven western lowland gorillas (Gorilla gorilla gorilla), and particularly focused on their sensitivity to the attentional state of a human experimenter when choosing from a repertoire of both auditory and visual communication strategies. In experiment 1 a banana was placed in front of the subject's cage and a human experimenter was either present or absent. The subject's behavior was recorded for 60 sec. Both gorillas and orangutans gestured (t(16)=-3.58, P<.005) and vocalized (t(16)=-2.47, P<.05) more when the experimenter was present. In experiment 2 a human experimenter held a banana in front of the subject's cage and was oriented either toward or away from the subject. Again the subject's behavior was recorded for 60 sec. In this experiment both gorillas and orangutans gestured significantly more frequently (t(16)=3.40, P<.005) when the experimenter was oriented toward them. In addition, gorillas and orangutans used other forms of visual communication signals, such as lip pout (t(16)=3.66, P<.005), barter/trade (t(16)=2.31, P<.05), and body present (t(16)=2.31, P<.05) significantly more when an experimenter was facing them. The overall results indicate that both gorillas and orangutans are sensitive to the attentional state of a human experimenter and use appropriate communicative signals to gain that individual's attention. These results are also similar to previous findings on communicative behaviors in chimpanzees.     

Helping behaviour and regard for others in capuchin monkeys (Cebus apella)

Altruism is an evolutionary puzzle. To date, much debate has focused on whether helping others without regard to oneself is a uniquely human behaviour, with a variety of empirical studies demonstrating a lack of altruistic behaviour in chimpanzees even when the demands of behaving altruistically seem minimal. By contrast, a recent experiment has demonstrated that chimpanzees will help a human experimenter to obtain an out-of-reach object, irrespective of whether or not they are offered a reward for doing so, suggesting that the cognitions underlying altruistic behaviour may be highly sensitive to situational demands. Here, we examine the cognitive demands of other-regarding behaviour by testing the conditions under which primates more distantly related to humans--capuchin monkeys--help an experimenter to obtain an out-of-reach object. Like chimpanzees, capuchin monkeys helped human experimenters even in the absence of a reward, but capuchins systematically failed to take into account the perspective of others when they stood to obtain food for themselves. These results suggest an important role for perspective taking and inhibition in altruistic behaviour and seem to reflect a significant evolutionary development in the roots of altruism, and specifically in other-regarding behaviour, between the divergence of New World monkeys and apes.     

Use of gesture sequences in chimpanzees

Gestural communication in a group of 19 captive chimpanzees (Pan troglodytes) was observed, with particular attention paid to gesture sequences (combinations). A complete inventory of gesture sequences is reported. The majority of these sequences were repetitions of the same gestures, which were often tactile gestures and often occurred in play contexts. Other sequences combined gestures within a modality (visual, auditory, or tactile) or across modalities. The emergence of gesture sequences was ascribed to a recipient's lack of responsiveness rather than a premeditated combination of gestures to increase the efficiency of particular gestures. In terms of audience effects, the chimpanzees were sensitive to the attentional state of the recipient, and therefore used visually-based gestures mostly when others were already attending, as opposed to tactile gestures, which were used regardless of whether the recipient was attending or not. However, the chimpanzees did not use gesture sequences in which the first gesture served to attract the recipient's visual attention before they produced a second gesture that was visually-based. Instead, they used other strategies, such as locomoting in front of the recipient, before they produced a visually-based gesture.     

Visual and auditory conditional position discrimination in chimpanzees (Pan troglodytes)

Chimpanzee cognition has been studied predominantly through the visual modality, and much less through the auditory modality. The aim of this study was to explore possible differences in chimpanzees’ processing of visual and auditory stimuli. We developed a new conditional position discrimination (CPD) task requiring the association between a stimulus (from either the auditory or the visual modality), and a spatial position (left or right). The stimuli consisted of the face and voice of two individuals well known to the subjects (one chimpanzee and one human). Six chimpanzees participated in both the visual and the auditory conditions. We found contrasting results between the two conditions: the subjects acquired the CPD more easily in the visual than in the auditory condition. This supports previous findings on the difficulties encountered by chimpanzees in learning tasks involving auditory stimuli. Our experiments also revealed individual differences: the chimpanzee with the most extensive experience in symbolic visual matching tasks showed good performance in both conditions. In contrast, the chimpanzee expert in an auditory-visual intermodal matching task showed no sign of learning in either condition. Future work should focus on finding the most appropriate procedure for exploring chimpanzees’ auditory-visual cognitive skills.     

Response facilitation in the four great apes: is there a role for empathy?

Contagious yawning is a form of response facilitation found in humans and other primates in which observing a model yawning enhances the chance that the observer will also yawn. Because contagious yawning seems to be more easily triggered when models are conspecifics or have a strong social bond with the observer, it has been proposed that contagious yawning is linked to empathy. A possible way to test this hypothesis is to analyze whether individuals’ responses differ when they observe models yawning or performing different involuntary (i.e., nose wiping, scratching) and voluntary (i.e., hand closing, wrist shaking) actions that are not linked to empathy. In this study, we tested the four great ape species with two different setups by exposing them to a human experimenter repeatedly performing these actions online, and video-recorded conspecifics repeatedly performing these actions on a screen. We examined which behaviors were subject to response facilitation, whether response facilitation was triggered by both human models and video-recorded conspecifics, and whether all species showed evidence of response facilitation. Our results showed that chimpanzees yawned significantly more when and shortly after watching videos of conspecifics (but not humans) yawning than in control conditions, and they did not do so as a response to increased levels of anxiety. For all other behaviors, no species produced more target actions when being exposed to either model than under control conditions. Moreover, the individuals that were more “reactive” when watching yawning videos were not more reactive when exposed to other actions. Since, at least in chimpanzees, (1) subjects only showed response facilitation when they were exposed to yawning and (2) only if models were conspecifics, it appears that contagious yawning is triggered by unique mechanisms and might be linked to empathy.     

Effect of others' attentional states on vocalizations in Japanese monkeys (Macaca fuscata)

We investigated the effects of other's attentional states on vocalizations in monkeys. The subjects were 14 Japanese monkeys (Macaca fuscata), which vocalized spontaneously in the feeding context. In the initial experiment, an experimenter moved towards and away from the subject monkeys. The monkeys vocalized more frequently when the experimenter moved away rather than towards them. To examine the effects of the experimenter's body orientations and moving directions separately, additional experiments were conducted. When the experimenter stood facing towards and facing away from the subject monkeys, the monkeys vocalized more frequently when the experimenter stood facing away rather than facing towards. When the experimenter moved towards and away from the subject monkeys while facing them, the monkeys vocalized more frequently when the experimenter moved away from them rather than towards them. These results suggested that the monkeys vocalized more frequently when the situation changed to that where the monkeys were not likely get food from the experimenter. It seems that monkeys recognize the attentional states of others by body orientation and modify their vocalizing behavior accordingly.     

Modulation of visual processing by attention and emotion: windows on causal interactions between human brain regions

Visual processing is not determined solely by retinal inputs. Attentional modulation can arise when the internal attentional state (current task) of the observer alters visual processing of the same stimuli. This can influence visual cortex, boosting neural responses to an attended stimulus. Emotional modulation can also arise, when affective properties (emotional significance) of stimuli, rather than their strictly visual properties, influence processing. This too can boost responses in visual cortex, as for fear-associated stimuli. Both attentional and emotional modulation of visual processing may reflect distant influences upon visual cortex, exerted by brain structures outside the visual system per se. Hence, these modulations may provide windows onto causal interactions between distant but interconnected brain regions. We review recent evidence, noting both similarities and differences between attentional and emotional modulation. Both can affect visual cortex, but can reflect influences from different regions, such as fronto-parietal circuits versus the amygdala. Recent work on this has developed new approaches for studying causal influences between human brain regions that may be useful in other cognitive domains. The new methods include application of functional magnetic resonance imaging (fMRI) and electroencephalography (EEG) measures in brain-damaged patients to study distant functional impacts of their focal lesions, and use of transcranial magnetic stimulation concurrently with fMRI or EEG in the normal brain. Cognitive neuroscience is now moving beyond considering the putative functions of particular brain regions, as if each operated in isolation, to consider, instead, how distinct brain regions (such as visual cortex, parietal or frontal regions, or amygdala) may mutually influence each other in a causal manner.     

Hemispheric Asymmetry in the Auditory Facilitation Effect in Dual-Stream Rapid Serial Visual Presentation Tasks

Even though auditory stimuli do not directly convey information related to visual stimuli, they often improve visual detection and identification performance. Auditory stimuli often alter visual perception depending on the reliability of the sensory input, with visual and auditory information reciprocally compensating for ambiguity in the other sensory domain. Perceptual processing is characterized by hemispheric asymmetry. While the left hemisphere is more involved in linguistic processing, the right hemisphere dominates spatial processing. In this context, we hypothesized that an auditory facilitation effect in the right visual field for the target identification task, and a similar effect would be observed in the left visual field for the target localization task. In the present study, we conducted target identification and localization tasks using a dual-stream rapid serial visual presentation. When two targets are embedded in a rapid serial visual presentation stream, the target detection or discrimination performance for the second target is generally lower than for the first target; this deficit is well known as attentional blink. Our results indicate that auditory stimuli improved target identification performance for the second target within the stream when visual stimuli were presented in the right, but not the left visual field. In contrast, auditory stimuli improved second target localization performance when visual stimuli were presented in the left visual field. An auditory facilitation effect was observed in perceptual processing, depending on the hemispheric specialization. Our results demonstrate a dissociation between the lateral visual hemifield in which a stimulus is projected and the kind of visual judgment that may benefit from the presentation of an auditory cue.     

Audiovisual integration of speech falters under high attention demands

One of the most commonly cited examples of human multisensory integration occurs during exposure to natural speech, when the vocal and the visual aspects of the signal are integrated in a unitary percept. Audiovisual association of facial gestures and vocal sounds has been demonstrated in nonhuman primates and in prelinguistic children, arguing for a general basis for this capacity. One critical question, however, concerns the role of attention in such multisensory integration. Although both behavioral and neurophysiological studies have converged on a preattentive conceptualization of audiovisual speech integration, this mechanism has rarely been measured under conditions of high attentional load, when the observers' attention resources are depleted. We tested the extent to which audiovisual integration was modulated by the amount of available attentional resources by measuring the observers' susceptibility to the classic McGurk illusion in a dual-task paradigm. The proportion of visually influenced responses was severely, and selectively, reduced if participants were concurrently performing an unrelated visual or auditory task. In contrast with the assumption that crossmodal speech integration is automatic, our results suggest that these multisensory binding processes are subject to attentional demands.     

The acquisition of stone-tool use in captive chimpanzees

In order to investigate the acquisition of stone-tool use to crack nuts, experiments were conducted with five captive chimpanzees, employing combinations of trial-and-error, and three types of observation learning of varied difficulty. Two adults and one sub-adult succeeded in acquiring this behavior in the tests where tool use was demonstrated by the experimenter, or by a successful chimpanzee. Analysis of their behavior patterns showed the adults' and sub-adult's process to success to be divided into three stages; these can be characterized as trial-and-error, understanding of the method, and learning the technique, respectively. A factor for distinguishing success from failure is whether or not a subject observes demonstrations with interest in the behavior itself. This interest, in turn, depends on the intensity of the desire for nuts. When released, the successful chimpanzees practiced the same behavior in a group of chimpanzees, and the behavior newly diffused to an infant. Unlike the adults, the infant did not go through the staged process but reached the solution through goal-directed trial-and-error.     

Wood mice aggressiveness and flight response to human handling: Effect of individual and environmental factors

Numerous studies have examined human disturbance repercussions on wildlife, mainly focused on the effects on behaviour, reproductive success and population dynamics. However, few studies have addressed the behaviour of prey species during and after human capture and handling and how this may correlate to individual characteristics or variation in their physical environment they inhabit. We explored wood mouse’s fleeing and aggressive behaviours in response to captures by human in their natural habitat. Eighty‐seven wood mice were caught using Sherman live traps. For each trapped individual, aggressiveness was measured as the total number of bites inflicted upon the investigator during handling time. Afterwards, each mouse was released in a two‐metre radius partially covered vegetation area that allowed visual mouse tracking by the observer and flight behaviour was registered by individual one‐zero focal sampling technique during 2 min. Both aggressiveness and fleeing behaviour were analysed regarding individual (sex, reproductive status, age) and environmental factors (habitat and season). Males, adults and breeding individuals showed heightened aggression levels. Higher aggressiveness levels were found in wood mice occupying scrubland and during summer and autumn. The flight response was exclusively explained by reproductive status, whereby breeding individuals spent more time on fast escape than nonbreeding ones. These results indicate that both individual and environmental factors seem to influence defensive behaviours in the wood mouse during and after being captured by a human. Since human disturbance shares many aspects with the predation risk, behavioural responses found to captures may likely be influenced by previous experience of individuals with predators as well as to seasonal and habitat features conditioning predators’ densities but also protection against them.     

Maintenance of delay of gratification by four chimpanzees (Pan troglodytes): the effects of delayed reward visibility, experimenter presence, and extended delay intervals

Previous research in our laboratory has demonstrated that chimpanzees can delay gratification by inhibiting consumption of available food items for as long as 3 min as an experimenter transfers additional food items from a transparent container to a bowl placed in front of the subject. In this study, we examined the influence of the visibility of the food source, as well as the presence of the experimenter, on four chimpanzees' self-control in this paradigm. In Experiment 1 an experimenter transferred 15 preferred food items between a distant opaque container and a bowl placed in front of the subject. In Experiment 2 we tested the chimpanzees with an automated system that (in the absence of the experimenter) transferred up to 36 highly preferred food items from a universal food dispenser to a container located either inside or outside of the subject's enclosure. There were no differences in self-directed behaviors or attentiveness to the food items between the self-imposed and externally imposed delay conditions. A final experiment with the automated paradigm indicated that individuals could delay gratification for up to 11min in order to obtain all 36 food items.     

Attentional Demands Influence Vocal Compensations to Pitch Errors Heard in Auditory Feedback

Auditory feedback is required to maintain fluent speech. At present, it is unclear how attention modulates auditory feedback processing during ongoing speech. In this event-related potential (ERP) study, participants vocalized/a/, while they heard their vocal pitch suddenly shifted downward a ½ semitone in both single and dual-task conditions. During the single-task condition participants passively viewed a visual stream for cues to start and stop vocalizing. In the dual-task condition, participants vocalized while they identified target stimuli in a visual stream of letters. The presentation rate of the visual stimuli was manipulated in the dual-task condition in order to produce a low, intermediate, and high attentional load. Visual target identification accuracy was lowest in the high attentional load condition, indicating that attentional load was successfully manipulated. Results further showed that participants who were exposed to the single-task condition, prior to the dual-task condition, produced larger vocal compensations during the single-task condition. Thus, when participants’ attention was divided, less attention was available for the monitoring of their auditory feedback, resulting in smaller compensatory vocal responses. However, P1-N1-P2 ERP responses were not affected by divided attention, suggesting that the effect of attentional load was not on the auditory processing of pitch altered feedback, but instead it interfered with the integration of auditory and motor information, or motor control itself.     

Consistency of dogs’ reactions to threatening cues of an unfamiliar person

Reliability is one of the most important aspects of the behaviour observations measuring personality traits in animals. The most fundamental way to test reliability is the assessment of the test–retest consistency. On the other hand, in situations where social interaction between a human participant and the animal subject is at the scope of the study, the behaviour of the humans in the test situation should be restricted by a set of rules. However, if more than one experimenter participates in the observations, the similarity of the behaviour of different persons is an important aspect of the reliability of the study.In our first study we investigated the consistency of dogs’ behaviour during approach by a person in a friendly and in a threatening way, repeating the test either immediately after the first test or at least 6 months later. We found that the dogs’ sensitivity to the human's behavioural cues in this situation proved to be consistent over repetition when the second test was performed approximately 1 year after the first test, but it was not the case when the time elapsed between test occasions was a few seconds. The detailed analysis indicated that dogs performing extreme behaviour (friendly or threatening) tended to show more conservative responses than dogs showing intermediate reactions when the stranger approached threateningly. Nonetheless, the reaction of the dogs failed to be in accordance with the opinion of the owners about the dogs’ behaviour in similar situations in everyday life.In the second study we examined the consistency of the dogs’ behaviour in the same situation when confronted with two different unfamiliar persons immediately after each other. The consistency of the dogs’ response to the two experimenters was found to be reliably high.In sum, this test procedure proved to be reliable enough to be a valuable measure of a definite part of the personality characters of dogs.     

Dominance and Immunity in Chimpanzees (Pan troglodytes)

The study reported here examined the effect of dominance status on serum immunoglobulin (IgG and IgM) levels in chimpanzees living in five captive colonies. Blood samples were collected from each individual twice, and agonistic and grooming interactions were observed. After initial group observations, members of four of the five groups were caged singly. Thereafter blood samples were again taken. Both IgG and IgM levels of the animals living in groups were significantly negatively correlated with their dominance status in all five groups. The higher-ranked chimpanzees were likely to show lower levels of IgG and IgM. No such consistent correlation was found between individual Ig levels and frequency of aggressive behaviour or grooming. On transfer to isolated conditions, Ig levels of the chimpanzees did not correlate with their previous dominance status in the groups. Being of high rank is a biological cost for colony-living chimpanzees with regard to immunity levels.     

On the Problem of Cooperation of the Reactions of Hands: II. Cooperation of Hand Reactions to Auditory and Visual Stimuli in Patients with Focal Brain Lesions

The cooperation of responses of hands to auditory and visual stimuli with a warning signal was studied in patients with focal lesions of the visual or auditory nerves or the cerebral cortex, parastem tumors, tumors of the cerebellum or the spinal cord, inflammation processes in the brain tunics, or some chronic neurological disorders. The cooperation of hand reactions to auditory and visual stimuli was compared for healthy subjects and the patients in order to determine the morphological structures involved. The patients with focal lesions, like the healthy subjects, showed a strong positive correlation between the response times of the left and right hands; an individual variation of this correlation in multiple tests was attributed to constitutional characteristics of the subject.     

Vocal-auditory functions in the chimpanzee: Vowel perception

The perception of vowels was studied in chimpanzees and humans, using a reaction time task in which reaction times for discrimination of vowels were taken as an index of similarity between vowels. Vowels used were five synthetic and natural Japanese vowels and eight natural French vowels. The chimpanzees required long reaction times for discrimination of synthetic [i] from [u] and [e] from [o], that is, they need long latencies for discrimination between vowels based on differences in frequency of the second formant. A similar tendency was observed for discrimination of natural [i] from [u]. The human subject required long reaction times for discrimination between vowels along the first formant axis. These differences can be explained by differences in auditory sensitivity between the two species and the motor theory of speech perception. A vowel, which is pronounced by different speakers, has different acoustic properties. However, humans can perceive these speech sounds as the same vowel. The phenomenon of perceptual constancy in speech perception was studied in chimpanzees using natural vowels and a synthetic [o]- [a] continuum. The chimpanzees ignored the difference in the sex of the speakers and showed a capacity for vocal tract normalization.     

Auditory attention--focusing the searchlight on sound

Some fifty years after the first physiological studies of auditory attention, the field is now ripening, with exciting recent insights into the psychophysics, psychology, and neural basis of auditory attention. Current research seeks to unravel the complex interactions of pre-attentive and attentive processing of the acoustic scene, the role of auditory attention in mediating receptive-field plasticity in both auditory spatial and auditory feature processing, the contrasts and parallels between auditory and visual attention pathways and mechanisms, the interplay of bottom-up and top-down attentional mechanisms, the influential role of attention, goals, and expectations in shaping auditory processing, and the orchestration of diverse attentional effects at multiple levels from the cochlea to the cortex.     

A direct comparison of scan and focal sampling methods for measuring wild chimpanzee feeding behaviour

Focal sampling is the most accurate method for measuring primate activity budgets but is sometimes impractical. An alternative is scan sampling, in which the behaviour of the group is recorded at regular intervals. The simplest technique is to record whether at least 1 animal is engaged in the behaviour of interest. By direct comparison with focal data collected simultaneously on the same population, we assess the validity of this simple group level sampling method for studying chimpanzee (Pan troglodytes schweinfurthii) feeding behaviour. In a 13-month study at Kanyawara, Kibale National Park, Uganda, group level scan sampling provided statistically similar measures of broad diet composition to those produced by focal data, despite considerable seasonal variation. Monthly means of the percentage of time spent consuming non-fig fruit calculated from group level scan sampling were highly correlated with those from focal sampling. This validates previous methodology used to identify periods of high energy availability. However, group level scans tended to overestimate the percentage of observation time spent feeding, particularly for adult males. We conclude that this method of group level scan sampling provides valuable data for characterizing broad diet choice in chimpanzees and other species, but may be of limited use for estimating individual feeding time.     

How Abnormal Is the Behaviour of Captive,Zoo-Living Chimpanzees?

BACKGROUND: Many captive chimpanzees (Pan troglodytes) show a variety of serious behavioural abnormalities, some of which have been considered as possible signs of compromised mental health. The provision of environmental enrichments aimed at reducing the performance of abnormal behaviours is increasing the norm, with the housing of individuals in (semi-)natural social groups thought to be the most successful of these. Only a few quantitative studies of abnormal behaviour have been conducted, however, particularly for the captive population held in zoological collections. Consequently, a clear picture of the level of abnormal behaviour in zoo-living chimpanzees is lacking. METHODS: We present preliminary findings from a detailed observational study of the behaviour of 40 socially-housed zoo-living chimpanzees from six collections in the United States of America and the United Kingdom. We determined the prevalence, diversity, frequency, and duration of abnormal behaviour from 1200 hours of continuous behavioural data collected by focal animal sampling. RESULTS, CONCLUSION AND SIGNIFICANCE: Our overall finding was that abnormal behaviour was present in all sampled individuals across six independent groups of zoo-living chimpanzees, despite the differences between these groups in size, composition, housing, etc. We found substantial variation between individuals in the frequency and duration of abnormal behaviour, but all individuals engaged in at least some abnormal behaviour and variation across individuals could not be explained by sex, age, rearing history or background (defined as prior housing conditions). Our data support a conclusion that, while most behaviour of zoo-living chimpanzees is 'normal' in that it is typical of their wild counterparts, abnormal behaviour is endemic in this population despite enrichment efforts. We suggest there is an urgent need to understand how the chimpanzee mind copes with captivity, an issue with both scientific and welfare implications.