Cross-modal individual recognition in domestic horses (Equus caballus) extends to familiar humans

It has recently been shown that some non-human animals can cross-modally recognize members of their own taxon. What is unclear is just how plastic this recognition system can be. In this study, we investigate whether an animal, the domestic horse, is capable of spontaneous cross-modal recognition of individuals from a morphologically very different species. We also provide the first insights into how cross-modal identity information is processed by examining whether there are hemispheric biases in this important social skill. In our preferential looking paradigm, subjects were presented with two people and playbacks of their voices to determine whether they were able to match the voice with the person. When presented with familiar handlers subjects could match the specific familiar person with the correct familiar voice. Horses were significantly better at performing the matching task when the congruent person was standing on their right, indicating marked hemispheric specialization (left hemisphere bias) in this ability. These results are the first to demonstrate that cross-modal recognition in animals can extend to individuals from phylogenetically very distant species. They also indicate that processes governed by the left hemisphere are central to the cross-modal matching of visual and auditory information from familiar individuals in a naturalistic setting.     

When and how well can human‐socialized capuchins match actions demonstrated by a familiar human?

Capuchin monkeys have provided uneven evidence of matching actions they observe others perform. In accord with theories emphasizing the attentional salience of object movement and spatial relationships, we predicted that human-reared monkeys would better match events in which a human demonstrator moved an object into a new relation with another object or surface than other kinds of actions. Three human-reared capuchins were invited repeatedly by a familiar human to perform a fixed set of actions upon objects or upon their bodies, using the "Do as I do" procedure. Actions directed at the body were matched less reliably than actions involving objects, and actions were matched best when the monkey looked at the demonstration for at least 2 sec and performed its action within a few seconds after the demonstration. The most commonly matched actions were those that one monkey performed relatively often when the experiment began. One monkey partially reproduced three novel actions (out of 48 demonstrations), all three involving moving or placing objects, and two of which it also performed following other demonstrations. These findings contribute convergent evidence that capuchin monkeys display social facilitation of activity, enhanced interest in particular objects and emulation of spatial outcomes. This pattern can support the development of shared manipulative skills, as evident in traditions of foraging and tool use in natural settings. The findings do not suggest that human rearing substantively altered capuchins' ability or interest in matching the actions of a familiar human, although visual attention to the human demonstrator may have been greater in these monkeys than in normally reared monkeys.     

Artificially generated cultural variation between two groups of captive monkeys, Colobus guereza kikuyuensis

The majority of studies of social learning in primates have tested subjects in isolation and investigated the effects of learning over very short periods of time. We aimed to test for social learning in two social groups of colobus monkeys, Colobus guereza kikuyuensis. Subjects were shown video footage of familiar monkeys either pushing or pulling a plastic flap to obtain a food reward, while they were given simultaneous access to the same apparatus. Action frequencies showed a significant difference between the two groups, with the pull group performing a higher proportion of pulls to pushes, compared with the push group. Copying persisted even in later sessions during which the demonstration footage was not being shown. We conclude that we successfully generated two contrasting behavioural traditions in these groups of monkeys. We do not know how long this contrast in behaviour would have persisted had we been able to continue testing for an even longer period of time, but further studies using similar designs and even longer test periods would have the power to confirm whether stable behavioural variation can be sustained between groups of monkeys, supported by social transmission.     

Vocal Repertoire of Golden-backed Uakaris (<Emphasis Type="Italic">Cacajao melanocephalus</Emphasis>): Call Structure and Context

The study of vocal behavior can reveal important aspects of how and why a species communicates in relation to ecological and social challenges. We here focus on vocal communication in golden-backed uakaris (Cacajao melanocephalus), diurnal, pitheciine monkeys that exhibit fission-fusion social organization and typically inhabit dense forests that limit the potential for visual communication. Moreover, the species spends little time engaged in tactile or olfactory communication, e.g., social grooming and scent marking, respectively. Hence, vocalizations may be very important for the coordination of social organization in these monkeys. We 1) categorized golden-backed uakari vocalizations, 2) ascertained their behavioral context, and 3) investigated whether golden-backed uakari calls can encode information about the signaler. We observed the monkeys during 2 wet seasons in the flooded igapó forest of Jaú National Park, Brazil. We showed that golden-backed uakaris have 9 call types in their vocal repertoire, all distinguishable by ear and from analysis of spectrograms. Some calls, e.g., play-specific calls, were used only in particular behavioral contexts, and by individuals of specific age, whereas others were emitted under a range of situations. The structure of the loud tchó call varied among individuals, and according to behavioral context, i.e., whether individuals were foraging/feeding, traveling, or performing agonistic interactions. This knowledge of the species’ vocal repertoire is valuable for surveying the monkeys acoustically in habitats where visual surveys are difficult.     

Cross-modal representation of human caretakers in squirrel monkeys

We tested whether squirrel monkeys have cross-modal representations of their human caretakers with a 0-delay symbolic matching-to-sample procedure. We first trained the monkeys to match photographs of two of their caretakers. After reaching criterion, they were exposed to two test sessions. In these sessions 32 all-reinforced test trials were interspersed among the training trials. In the test trials, a voice, either matching (congruent condition) or mismatching (incongruent condition) with the sample photographs, was played back after the sample stimulus disappeared. The monkeys' matching accuracies in the incongruent condition were lower than in the match condition. Post hoc analyses revealed that the presentation of the primary caretaker's voice interfered with performance in test trials where the secondary caretaker's face was presented (incongruent condition). This suggests that our subjects recalled their primary caretaker's representation upon hearing the appropriate voice.     

Metabolic Changes in the Visual Cortex of Binocular Blindness Macaque Monkeys: A Proton Magnetic Resonance Spectroscopy Study

Purpose

To evaluate proton magnetic resonance spectroscopy (¹H-MRS) in a study of cross-modal plasticity in the visual cortex of binocular blindness macaque monkeys.

Materials and Methods

Four healthy neonatal macaque monkeys were randomly divided into 2 groups, with 2 in each group. Optic nerve transection was performed in both monkeys in the experimental group (group B) to obtain binocular blindness. Two healthy macaque monkeys served as a control group (group A). After sixteen months post-procedure, ¹H-MRS was performed in the visual cortex of all monkeys. We compared the peak areas of NAA, Cr, Cho, Glx and Ins and the ratios of NAA/Cr, Cho/Cr, Glx/Cr and Ins/Cr of each monkey in group B with group A.

Results

The peak area of NAA and the NAA/Cr ratio in the visual cortex of monkey 4 in group B were found to be dramatically decreased, the peak area of NAA slightly decreased and the NAA/Cr ratio clearly decreased in visual cortex of monkey 3 in group B than those in group A. The peak area of Ins and the Ins/Cr ratio in the visual cortex of monkey 4 in group B slightly increased. The peak area of Cho and the Cho/Cr ratio in the visual cortex of all monkeys in group B dramatically increased compared with group A. The peak area of Glx in the visual cortex of all monkeys in group B slightly increased compared with group A.

Conclusions

¹H-MRS could detect biochemical and metabolic changes in the visual cortex and therefore this technique can be used to provide valuable information for investigating the mechanisms of cross-modal plasticity of binocular blindness in a macaque monkey model.     

Individual recognition through olfactory–auditory matching in lemurs

Individual recognition can be facilitated by creating representations of familiar individuals, whereby information from signals in multiple sensory modalities become linked. Many vertebrate species use auditory–visual matching to recognize familiar conspecifics and heterospecifics, but we currently do not know whether representations of familiar individuals incorporate information from other modalities. Ring-tailed lemurs (Lemur catta) are highly visual, but also communicate via scents and vocalizations. To investigate the role of olfactory signals in multisensory recognition, we tested whether lemurs can recognize familiar individuals through matching scents and vocalizations. We presented lemurs with female scents that were paired with the contact call either of the female whose scent was presented or of another familiar female from the same social group. When the scent and the vocalization came from the same individual versus from different individuals, females showed greater interest in the scents, and males showed greater interest in both the scents and the vocalizations, suggesting that lemurs can recognize familiar females via olfactory–auditory matching. Because identity signals in lemur scents and vocalizations are produced by different effectors and often encountered at different times (uncoupled in space and time), this matching suggests lemurs form multisensory representations through a newly recognized sensory integration underlying individual recognition.     

Visual recognition in infant pigtailed macaques after a 24-hour delay

Comparative studies of memory in monkey and human subjects suggest similarities in visual recognition memory across human and nonhuman primates. In order to investigate developmental aspects of visual recognition memory in monkey infants, the familiarization-novelty procedure, developed for use with human infants, was employed with pigtailed monkey infants to study long-delay recognition memory. Subjects were familiarized with a black-and-white abstract pattern. Twenty-four hours later they were tested with the familiar pattern paired with a novel one. Results indicated a significant visual preference for the novel stimulus, providing evidence for recognition memory. These results parallel those obtained with human infants, suggesting further similarities in the development of visual recognition memory.     

Neural Substrate of Initiation of Cross-Modal Working Memory Retrieval

Cross-modal working memory requires integrating stimuli from different modalities and it is associated with co-activation of distributed networks in the brain. However, how brain initiates cross-modal working memory retrieval remains not clear yet. In the present study, we developed a cued matching task, in which the necessity for cross-modal/unimodal memory retrieval and its initiation time were controlled by a task cue appeared in the delay period. Using functional magnetic resonance imaging (fMRI), significantly larger brain activations were observed in the left lateral prefrontal cortex (l-LPFC), left superior parietal lobe (l-SPL), and thalamus in the cued cross-modal matching trials (CCMT) compared to those in the cued unimodal matching trials (CUMT). However, no significant differences in the brain activations prior to task cue were observed for sensory stimulation in the l-LPFC and l-SPL areas. Although thalamus displayed differential responses to the sensory stimulation between two conditions, the differential responses were not the same with responses to the task cues. These results revealed that the frontoparietal-thalamus network participated in the initiation of cross-modal working memory retrieval. Secondly, the l-SPL and thalamus showed differential activations between maintenance and working memory retrieval, which might be associated with the enhanced demand for cognitive resources.     

Which senses play a role in nonhuman primate food selection? A comparison between squirrel monkeys and spider monkeys

In order to optimize foraging efficiency and avoid toxicosis, animals must be able to detect, discriminate, and learn about the predictive signals of potential food. Primates are typically regarded as animals that rely mainly on their highly developed visual systems, and little is known about the role that the other senses may play in food selection. It was therefore the aim of the present study to assess which senses are involved in the evaluation of food by two species of New World primates: the squirrel monkey and the spider monkey. To this end, six animals per species were repeatedly presented with both familiar and novel food items, and their behavior was videotaped and analyzed. To obtain a further indication of the relative importance of visual and chemosensory cues, the animals were also presented with familiar food items that were experimentally modified in color, odor, or both color and odor. The results demonstrate that squirrel monkeys and spider monkeys use olfactory, gustatory, and tactile cues in addition to visual information to evaluate novel food, whereas they mainly inspect familiar food items visually prior to consumption. Our findings also show that in both species the use of nonvisual cues decreased rapidly with repeated presentations of novel food, suggesting a fast multimodal learning process. Further, the two species clearly differ in their relative use of nonvisual cues when evaluating novel or modified food, with spider monkeys relying more on olfactory cues than squirrel monkeys, and squirrel monkeys relying more on tactile cues compared to spider monkeys.     

Amnesia and neglect: beyond the Delay-Brion system and the Hebb synapse.

Hippocampal damage in people causes impairments of episodic memory, but in rats it causes impairments of spatial learning. Experiments in macaque monkeys show that these two kinds of impairment are functionally similar to each other. After any lesion that interrupts the Delay-Brion system (hippocampus, fornix, mamillary bodies and anterior thalamus) monkeys are impaired in scene-specific memory, where an event takes place against a background that is specific to that event. Scene-specific memory in the monkey corresponds to human episodic memory, which is the memory of a unique event set in a particular scene, as opposed to scene-independent human knowledge, which is abstracted from many different scenes. However, interruption of the Delay-Brion system is not sufficient to explain all of the memory impairments that are seen in amnesic patients. To explain amnesia the specialized function of the hippocampus in scene memory needs to be considered alongside the other, qualitatively different functional specializations of other memory systems of the temporal lobe, including the perirhinal cortex and the amygdala. In all these specialized areas, however, including the hippocampus, there is no fundamental distinction between memory systems and perceptual systems. In explaining memory disorders in amnesia it is also important to consider them alongside the memory disorders of neglect patients. Neglect patients fail to represent in memory the side of the world that is contralateral to the current fixation point, in both short- and long-term memory retrieval. Neglect was produced experimentally by unilateral visual disconnection in the monkey, confirming the idea that visual memory retrieval is retinotopically organized; patients with unilateral medial temporal-lobe removals showed lateralized memory impairments for half-scenes in the visual hemifield contralateral to the removal. Thus, in scene-memory retrieval the Delay-Brion system contributes to the retrieval of visual memories into the retinotopically organized visual cortex. This scene memory interpretation of hippocampal function needs to be contrasted with the cognitive-map hypothesis. The cognitive-map model of hippocampal function shares some common assumptions with the Hebb-synapse model of association formation, and the Hebb-synapse model can be rejected on the basis of recent evidence that monkeys can form direct associations in memory between temporally discontiguous events. Our general conclusion is that the primate brain encompasses widespread and powerful memory mechanisms which will continue to be poorly understood if theory and experimentation continue to concentrate too much, as they have in the past, on the hippocampus and the Hebb synapse.     

Retention of social recognition after hibernation in Belding's ground squirrels

The retention of social memory during long periods of separation, such as hibernation or migration, has not been well documented, despite evidence for long-term social relationships in migrating species or in long-lived sedentary species. We investigated the ability of captive Belding's ground squirrels, Spermophilus beldingi, to remember previously familiar individuals as well as littermates after 9 months of isolation. Before hibernation, young ground squirrels discriminated between odours of familiar and unfamiliar individuals, as shown by greater investigation of a novel individual's odour. The following spring, these yearlings did not respond differentially to odours of previously familiar and unfamiliar individuals, suggesting that memory for familiar conspecifics was lost during hibernation. In contrast, both female and male yearlings continued to discriminate between odours of littermates and previously familiar nonlittermates. Thus, recognition of close kin was maintained during prolonged social isolation, but recognition of familiar, unrelated individuals was not. If re-establishment of familiarity is not costly or if adults rarely interact with the same individuals in successive years, then selection may not favour retention of individual memories of particular conspecifics over the winter. Even though males rarely encounter kin after dispersal, yearling males did recognize their siblings, suggesting that the relative costs of maintaining kin-recognition abilities year-round may be low. Possible mechanisms underlying the formation and maintenance of individual and kin recognition are discussed. Copyright 2000 The Association for the Study of Animal Behaviour.     

Japanese macaques form a cross-modal representation of their own species in their first year of life

We tested whether infant Japanese macaques (Macaca fuscata) have a cross-modal representation of their own species. We presented monkeys with a photograph of either a monkey or a human face on an LCD monitor after playing back a vocalization of one of those two species. The subjects looked at the monitor longer when a human face was presented after the monkey vocalization than when the same face was presented after human vocalization. This suggests that monkeys recall and expect a monkey’s face upon hearing a monkey’s voice.     

Social and nonsocial content differentially modulates visual attention and autonomic arousal in Rhesus macaques

The sophisticated analysis of gestures and vocalizations, including assessment of their emotional valence, helps group-living primates efficiently navigate their social environment. Deficits in social information processing and emotion regulation are important components of many human psychiatric illnesses, such as autism, schizophrenia and social anxiety disorder. Analyzing the neurobiology of social information processing and emotion regulation requires a multidisciplinary approach that benefits from comparative studies of humans and animal models. However, many questions remain regarding the relationship between visual attention and arousal while processing social stimuli. Using noninvasive infrared eye-tracking methods, we measured the visual social attention and physiological arousal (pupil diameter) of adult male rhesus monkeys (Macaca mulatta) as they watched social and nonsocial videos. We found that social videos, as compared to nonsocial videos, captured more visual attention, especially if the social signals depicted in the videos were directed towards the subject. Subject-directed social cues and nonsocial nature documentary footage, compared to videos showing conspecifics engaging in naturalistic social interactions, generated larger pupil diameters (indicating heightened sympathetic arousal). These findings indicate that rhesus monkeys will actively engage in watching videos of various kinds. Moreover, infrared eye tracking technology provides a mechanism for sensitively gauging the social interest of presented stimuli. Adult male rhesus monkeys' visual attention and physiological arousal do not always trend in the same direction, and are likely influenced by the content and novelty of a particular visual stimulus. This experiment creates a strong foundation for future experiments that will examine the neural network responsible for social information processing in nonhuman primates. Such studies may provide valuable information relevant to interpreting the neural deficits underlying human psychiatric illnesses such as autism, schizophrenia and social anxiety disorder.     

Squirrel monkey chuck call: vocal response to playback chucks based on acoustic structure and affiliative relationship with the caller

Adult female squirrel monkeys (genus Saimiri) that are socially familiar often exchange the chuck vocalization, which differs acoustically across individuals. We used behavioral observations, vocalization playback experiments, and analysis of the acoustic properties of vocalizations to investigate the effect of caller identity and acoustic structure on vocal response to playback chucks in two all-female social groups (n=10 females). Females were most likely to respond with a chuck to the playback chucks of their closely affiliated partners compared to those of nonaffiliated group members. This shows for the first time that the chuck stimulus alone is sufficient to elicit a chuck response from a female's affiliated partner. Additionally, females responded with a chuck mostly to familiar playback chucks from their own group and least to playbacks of silent controls. Unfamiliar playback chucks from the same species and a different squirrel monkey species elicited chuck responses intermediate between familiar chucks and silent controls. Post-hoc discriminant function analyses provide preliminary evidence that females are most likely to respond to unfamiliar chucks when those chucks are close in acoustic structure to familiar chucks from their own social group. These results provide a provisional explanation for error in the squirrel monkey signal processing system, in which unfamiliar chucks never heard before nevertheless elicit a chuck response if they are similar in acoustic structure to familiar group chucks.     

Is Working More Costly than Waiting in Monkeys?

We studied how value for instrumental action is discounted by predicted effort and delay. The monkeys were trained to perform instrumental trials that required a bar release when a visual target changed from red-to-green. There were two trial conditions. In delay trials, after the monkeys performed one instrumental trial correctly a reward was delivered 0–7 seconds later. In work trials, the monkeys had to perform 0, 1, or 2 additional instrumental trials to obtain a reward. The lengths of trials in delay matched the time it took to complete work trials. The length of delay or number of trials was indicated by a visual cue presented throughout the trial. Our hypothesis was that the monkeys would all show temporal discounting of reward in the delay trials, and that in the work trials the monkeys’ performance might reflect an additional cost due to working. The error rate increased linearly as remaining cost increased for all 8 monkeys. For 4 monkeys the error rate was significantly larger in work trials than in delay trials (effort sensitive monkeys). For the other 4 monkeys there was no significant difference in error rate (effort insensitive monkeys). Since the error rate has an inverse relation with value for action, these results suggest that value is discounted hyperbolically by effort as well as by delay. Error rates generally increased as the testing sessions progressed and the total reward accumulated (i.e., effect of reward devaluation). The relative impact of delay and effort on error rates was reasonably stable within subjects. Thus, within the monkey population there seems to be a significant dichotomy in the sensitivity governing whether working is more costly than waiting, possibly arising from a constitutional or genetic trait.     

Social Suppressive Behavior Is Organized by the Spatiotemporal Integration of Multiple Cortical Regions in the Japanese Macaque

Under social conflict, monkeys develop hierarchical positions through social interactions. Once the hierarchy is established, the dominant monkey dominates the space around itself and the submissive monkey tries not to violate this space. Previous studies have shown the contributions of the frontal and parietal cortices in social suppression, but the contributions of other cortical areas to suppressive functions remain elusive. We recorded neural activity in large cortical areas using electrocorticographic (ECoG) arrays while monkeys performed a social food-grab task in which a target monkey was paired with either a dominant or a submissive monkey. If the paired monkey was dominant, the target monkey avoided taking food in the shared conflict space, but not in other areas. By contrast, when the paired monkey was submissive, the target monkey took the food freely without hesitation. We applied decoding analysis to the ECoG data to see when and which cortical areas contribute to social behavioral suppression. Neural information discriminating the social condition was more evident when the conflict space was set in the area contralateral to the recording hemisphere. We found that the information increased as the social pressure increased during the task. Before food presentation, when the pressure was relatively low, the parietal and somatosensory–motor cortices showed sustained discrimination of the social condition. After food presentation, when the monkey faced greater pressure to make a decision as to whether it should take the food, the prefrontal and visual cortices started to develop buildup responses. The social representation was found in a sustained form in the parietal and somatosensory–motor regions, followed by additional buildup form in the visual and prefrontal cortices. The representation was less influenced by reward expectation. These findings suggest that social adaptation is achieved by a higher-order self-regulation process (incorporating motor preparation/execution processes) in accordance with the embodied social contexts.     

Long-term memory for affiliates in ravens

Complex social life requires individuals to recognize and remember group members and, within those, to distinguish affiliates from nonaffiliates. Whereas long-term individual recognition has been demonstrated in some nonhuman animals, memory for the relationship valence to former group members has received little attention. Here we show that adult, pair-housed ravens not only respond differently to the playback of calls from previous group members and unfamiliar conspecifics but also discriminate between familiar birds according to the relationship valence they had to those subjects up to three years ago as subadult nonbreeders. The birds' distinction between familiar and unfamiliar individuals is reflected mainly in the number of calls, whereas their differentiation according to relationship valence is reflected in call modulation only. As compared to their response to affiliates, ravens responded to nonaffiliates by increasing chaotic parts of the vocalization and lowering formant spacing, potentially exaggerating the perceived impression of body size. Our findings indicate that ravens remember relationship qualities to former group members even after long periods of separation, confirming that their sophisticated social knowledge as nonbreeders is maintained into the territorial breeding stage.     

Crows cross-modally recognize group members but not non-group members

Recognizing other individuals by integrating different sensory modalities is a crucial ability of social animals, including humans. Although cross-modal individual recognition has been demonstrated in mammals, the extent of its use by birds remains unknown. Herein, we report the first evidence of cross-modal recognition of group members by a highly social bird, the large-billed crow (Corvus macrorhynchos). A cross-modal expectancy violation paradigm was used to test whether crows were sensitive to identity congruence between visual presentation of a group member and the subsequent playback of a contact call. Crows looked more rapidly and for a longer duration when the visual and auditory stimuli were incongruent than when congruent. Moreover, these responses were not observed with non-group member stimuli. These results indicate that crows spontaneously associate visual and auditory information of group members but not of non-group members, which is a demonstration of cross-modal audiovisual recognition of group members in birds.     

Ecological and Social Factors Affecting the Vocal Behavior of Adult Female Squirrel Monkeys

Focal recordings of the vocalizations of squirrel monkeys, Saimiri sciureus, occupying an undisturbed Peruvian habitat were collected to evaluate the importance of both the ecological and social functions of female vocal behavior. The rates and sequences of six call types were examined by context: single, double, and multiple chuck, peep, tweet, and tweet-chuck. In contrast to laboratory studies, our findings emphasize the primacy of ecological functions in the wild, where calling permits females to operate as a convoy of spatially separated individuals in an arboreal habitat where visual contact is limited. Chuck calls are probably best interpreted as contact calls. The rate of chucks and tweet-chucks increased when the nearest adult female was > 5 m away. However, call production did not predict a change in the spatial separation between a female and her nearest adult female. During travel, the rate of single and double chucks was greater and the rate of multiple chucks was reduced. No direct relationship was found between foraging activities and vocal behavior. Although secondary, social factors did have a subtle effect on vocal behavior: the larger the social alliance of a female, the lower the rate and repetitiveness of her chuck vocalizations. We also consider the role of variations in vocalization rates among primates and the differing conclusions of field and captive studies of squirrel monkey vocal behavior.