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.     

Rhesus monkeys see who they hear: spontaneous cross-modal memory for familiar conspecifics

Rhesus monkeys gather much of their knowledge of the social world through visual input and may preferentially represent this knowledge in the visual modality. Recognition of familiar faces is clearly advantageous, and the flexibility and utility of primate social memory would be greatly enhanced if visual memories could be accessed cross-modally either by visual or auditory stimulation. Such cross-modal access to visual memory would facilitate flexible retrieval of the knowledge necessary for adaptive social behavior. We tested whether rhesus monkeys have cross-modal access to visual memory for familiar conspecifics using a delayed matching-to-sample procedure. Monkeys learned visual matching of video clips of familiar individuals to photographs of those individuals, and generalized performance to novel videos. In crossmodal probe trials, coo-calls were played during the memory interval. The calls were either from the monkey just seen in the sample video clip or from a different familiar monkey. Even though the monkeys were trained exclusively in visual matching, the calls influenced choice by causing an increase in the proportion of errors to the picture of the monkey whose voice was heard on incongruent trials. This result demonstrates spontaneous cross-modal recognition. It also shows that viewing videos of familiar monkeys activates naturally formed memories of real monkeys, validating the use of video stimuli in studies of social cognition in monkeys.     

Do Horses Have a Concept of Person?

Background

Animals'' ability for cross-modal recognition has recently received much interest. Captive or domestic animals seem able to perceive cues of human attention and appear to have a multisensory perception of humans.

Methodology/Principal Findings

Here, we used a task where horses have to remain immobile under a vocal order to test whether they are sensitive to the attentional state of the experimenter, but also whether they behave and respond differently to the familiar order when tested by a familiar or an unknown person. Horses'' response varied according to the person''s attentional state when the order was given by an unknown person: obedience levels were higher when the person giving the order was looking at the horse than when he was not attentive. More interesting is the finding that whatever the condition, horses monitored much more and for longer times the unknown person, as if they were surprised to hear the familiar order given by an unknown voice.

Conclusion/Significance

These results suggest that recognition of humans may lie in a global, integrated, multisensory representation of specific individuals, that includes visual and vocal identity, but also expectations on the individual''s behaviour in a familiar situation.     

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.     

Effect of species-specificity in auditory-visual intermodal matching in a chimpanzee (Pan troglodytes) and humans

The goal of this study was to compare the performance of a chimpanzee and humans on auditory-visual intermodal matching of conspecifics and non-conspecifics. The task consisted of matching vocal samples to facial images of the corresponding vocalizers. We tested the chimpanzee and human subjects with both chimpanzee and human stimuli to assess the involvement of species-specificity in the recognition process. All subjects were highly familiar with the stimuli. The chimpanzee subject, named Pan, had had extensive previous experience in auditory-visual intermodal matching tasks. We found clear evidence of a species-specific effect: the chimpanzee and human subjects both performed better at recognizing conspecifics than non-conspecifics. Our results suggest that Pan's early exposure to human caretakers did not seem to favor a perceptual advantage in better discriminating familiar humans compared to familiar conspecifics. The results also showed that Pan's recognition of non-conspecifics did not significantly improve over the course of the experiment. In contrast, human subjects learned to better discriminate non-conspecific stimuli, suggesting that the processing of recognition might differ across species. Nevertheless, this comparative study demonstrates that species-specificity significantly affects intermodal individual recognition of highly familiar individuals in both chimpanzee and human subjects.     

Schizophrenia as Failure of Left Hemispheric Dominance for the Phonological Component of Language

Background

T. J. Crow suggested that the genetic variance associated with the evolution in Homo sapiens of hemispheric dominance for language carries with it the hazard of the symptoms of schizophrenia. Individuals lacking the typical left hemisphere advantage for language, in particular for phonological components, would be at increased risk of the typical symptoms such as auditory hallucinations and delusions.

Methodology/Principal Findings

Twelve schizophrenic patients treated with low levels of neuroleptics and twelve matched healthy controls participated in an event-related potential experiment. Subjects matched word-pairs in three tasks: rhyming/phonological, semantic judgment and word recognition. Slow evoked potentials were recorded from 26 scalp electrodes, and a laterality index was computed for anterior and posterior regions during the inter stimulus interval. During phonological processing individuals with schizophrenia failed to achieve the left hemispheric dominance consistently observed in healthy controls. The effect involved anterior (fronto-temporal) brain regions and was specific for the Phonological task; group differences were small or absent when subjects processed the same stimulus material in a Semantic task or during Word Recognition, i.e. during tasks that typically activate more widespread areas in both hemispheres.

Conclusions/Significance

We show for the first time how the deficit of lateralization in the schizophrenic brain is specific for the phonological component of language. This loss of hemispheric dominance would explain typical symptoms, e.g. when an individual''s own thoughts are perceived as an external intruding voice. The change can be interpreted as a consequence of “hemispheric indecision”, a failure to segregate phonological engrams in one hemisphere.     

Kin discrimination in sticklebacks is mediated by social learning rather than innate recognition

Theory predicts several advantages for animals to recognize kin. These include inbreeding avoidance and an increase in inclusive fitness. In shoaling species, kin recognition may lead to an increased amount of altruism among shoal members. Adult, non‐reproductive three‐spined sticklebacks, Gasterosteus aculeatus, prefer to shoal with kin. This preference was shown for familiar as well as for unfamiliar individuals. However, whether it is based on learned cues of familiar individuals or on innate mechanisms like self‐referent phenotype matching or ‘true’ kin recognition through recognition alleles remains unknown. In our experiments, juvenile fish were given the choice between shoals that differed in relatedness and familiarity. The number of testfish who joined each group indicated that sticklebacks prefer to shoal with familiar kin when the alternative shoal was composed of unfamiliar non‐kin. When one shoal consisted of familiar kin while the second consisted of familiar non‐kin testfish did not show any preference. Kin recognition in sticklebacks is thus most likely mediated by social learning.     

Evidence of social niche construction: persistent and repeated social interactions generate stronger personalities in a social spider

While there are now a number of theoretical models predicting how consistent individual differences in behaviour may be generated and maintained, so far, there are few empirical tests. The social niche specialization hypothesis predicts that repeated social interactions among individuals may generate among-individual differences and reinforce within-individual consistency through positive feedback mechanisms. Here, we test this hypothesis using groups of the social spider Stegodyphus mimosarum that differ in their level of familiarity. In support of the social niche specialization hypothesis, individuals in groups of spiders that were more familiar with each other showed greater repeatable among-individual variation in behaviour. Additionally, individuals that were more familiar with each other exhibited lower within-individual variation in behaviour, providing one of the first examples of how the social environment can influence behavioural consistency. Our study demonstrates the potential for the social environment to generate and reinforce consistent individual differences in behaviour and provides a potentially general mechanism to explain this type of behavioural variation in animals with stable social groups.     

Does emotional state influence motor lateralization in California sea lions (<Emphasis Type="Italic">Zalophus californianus</Emphasis>)?

Motor lateralization is a behavioural asymmetry between the left and the right side of an individual due to hemispheric specialization. The right hemisphere controls the left side of the body and the left hemisphere the right side. The right hemisphere processes negative emotions such as fear and frustration, and on the contrary, the left hemisphere processes positive emotions such as happiness. This study, conducted at Parc Asterix Delphinarium (Plailly, France), tested the influence of supposedly positive, negative and neutral emotional situations on four California sea lions’ (Zalophus californianus) motor lateralization while performing a known exercise, here climbing on a stool. Latency between the caretakers’ command and the animals’ response was recorded. The results showed an interindividual variability in the effect of the supposed emotional situations on their motor lateralization and their response latency. The nature and the strength of this effect require deeper investigation by further studies, on a larger number of individuals and contexts.     

Dreaming and unilateral brain lesions: A multiple lesion case analysis.

Lesions causing cessation of dreaming are thought to be more frequently left hemispheric than right hemispheric. However, reports of this phenomenon have not excluded epileptic cases and have not reported handedness, etiology of the lesion, lesion location, comorbidity, gender, age, and so forth, on a case-by-case basis. Some authors were also concerned about aphasia being a cause of dream loss and its lateralization, but they never measured its impact statistically. The present investigation reviews cases of post lesion dream cessation that answered to strict criteria for testing hemispheric lateralization and the effect of aphasia on it. In the 31 subjects, left hemisphere lesions were significantly more frequent than right, as predicted, but the left hemisphere lesions were very often associated with aphasia. Nonaphasic cases of total dream loss had lesions equally often in the right and in the left hemisphere. It is proposed that aphasia deprives patients of a second dream-encoding system, which is important enough to induce amnesia of dream occurrence. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Individual voice recognition in a territorial frog (Rana catesbeiana)

Some territorial animals display low levels of aggression towards a familiar territorial neighbour in its usual territory, but exhibit high levels of aggression towards neighbours in novel locations and unfamiliar individuals. Here, we report results from a field playback study that investigated whether territorial males of the North American bullfrog (Rana catesbeiana) could discriminate between the acoustic signals of simulated neighbours and strangers in the absence of contextual cues associated with a specific location. Following repeated exposures to synthetic bullfrog calls from a particular location, subjects responded significantly less aggressively to a familiar call, compared with an unfamiliar one, when both calls were broadcast from familiar and novel locations, indicating that bullfrogs could recognize a neighbour's calls independently of the contextual cues provided by the direction of the neighbour's territory. Subjects responded equally aggressively to unfamiliar calls broadcast from either a familiar or a novel location, which indicates that they could perceive unfamiliar calls as those of a stranger, regardless of where the stranger was encountered. Together, these two results provide evidence that a frog possesses a capacity for individual voice recognition.     

Mother goats do not forget their kids' calls

Parent-offspring recognition is crucial for offspring survival. At long distances, this recognition is mainly based on vocalizations. Because of maturation-related changes to the structure of vocalizations, parents have to learn successive call versions produced by their offspring throughout ontogeny in order to maintain recognition. However, because of the difficulties involved in following the same individuals over years, it is not clear how long this vocal memory persists. Here, we investigated long-term vocal recognition in goats. We tested responses of mothers to their kids' calls 7-13 months after weaning. We then compared mothers' responses to calls of their previous kids with their responses to the same calls at five weeks postpartum. Subjects tended to respond more to their own kids at five weeks postpartum than 11-17 months later, but displayed stronger responses to their previous kids than to familiar kids from other females. Acoustic analyses showed that it is unlikely that mothers were responding to their previous kids simply because they confounded them with the new kids they were currently nursing. Therefore, our results provide evidence for strong, long-term vocal memory capacity in goats. The persistence of offspring vocal recognition beyond weaning could have important roles in kin social relationships and inbreeding avoidance.     

Recognition of halftone and contour figures under their lateralization and masking

Recognition of shape of natural objects was studied during lateralized tachistoscopic presentation and different degree of noise-like ("rain drops") masking in 15 healthy subjects. Two sets of figures were used: halftone and contour ones. In all masking conditions, the mean group data showed a significantly better recognition of contour images by the left hemisphere as compared to the right hemisphere. The probability of correct response decreased with increase in the degree of masking. Contour figures were recognized significantly better than halftone figures. Gender differences in recognition were revealed. Male subjects displayed no hemispheric preference in recognition of both types of stimuli in both masking conditions. Possible neurophysiological mechanisms and functional significance of the findings are discussed.     

Language-related hemispheric asymmetry in healthy subjects and patients with temporal lobe epilepsy as studied by event-related brain potentials and intracarotid amobarbital test

There are current attempts to replace the WADA test for pre-surgical evaluation of hemispheric language capabilities by one of the methods of functional brain imaging. Recent PET and fMRI studies using verbal cognitive tasks like verb generation, semantic monitoring or semantic (`deep') encoding of words showed asymmetries of activation in the fronto-lateral cortex. In a previous ERP study subjects were required to indicate whether pronounceable non-words and abstract geometric figures were presented for the first time (`new item') or whether they had been shown before (`old item'). Group analyses of this study showed significant material-specific hemispheric asymmetries with ERPs being more negative-going in recordings of the posterior part of the left hemisphere with verbal material (CP5/6) but more negative-going in recordings of the right hemisphere with the spatial material (P7/8). The aim of the present study was to test statistically ERP lateralization effects in individual healthy subjects as well as WADA-tested patients suffering from seizures of the mesio-temporal lobe (MTL). In all subjects ERP lateralization with verbal material was tested in the electrode pair CP5/6, and ERP lateralization with figures in the electrode pair P7/8. Statistical analyses of single trials showed that in 20 out of 24 subjects ERPs with verbal material started to be more negative-going in CP5 as compared to CP6 in the period between 100 and 200 ms after stimulus onset or the subsequent time epoch (200–300 ms). In one subject not CP5/6 but the closely adjacent electrode pair P7/P8 showed this verbal material-related hemispheric effect. In patients language dominance as indicated by ERPs was not always consistent with the data of the WADA test. In one patient with left MTL seizures ERPs with verbal material and figures were found to be significantly lateralized to the right hemisphere although the WADA test assigned this patient to have a language-dominant left hemisphere.     

Instant messages vs. speech: hormones and why we still need to hear each other

Human speech evidently conveys an adaptive advantage, given its apparently rapid dissemination through the ancient world and global use today. As such, speech must be capable of altering human biology in a positive way, possibly through those neuroendocrine mechanisms responsible for strengthening the social bonds between individuals. Indeed, speech between trusted individuals is capable of reducing levels of salivary cortisol, often considered a biomarker of stress, and increasing levels of urinary oxytocin, a hormone involved in the formation and maintenance of positive relationships. It is not clear, however, whether it is the uniquely human grammar, syntax, content and/or choice of words that causes these physiological changes, or whether the prosodic elements of speech, which are present in the vocal cues of many other species, are responsible. In order to tease apart these elements of human communication, we examined the hormonal responses of female children who instant messaged their mothers after undergoing a stressor. We discovered that unlike children interacting with their mothers in person or over the phone, girls who instant messaged did not release oxytocin; instead, these participants showed levels of salivary cortisol as high as control subjects who did not interact with their parents at all. We conclude that the comforting sound of a familiar voice is responsible for the hormonal differences observed and, hence, that similar differences may be seen in other species using vocal cues to communicate.     

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.     

Female butterflies prefer males bearing bright iridescent ornamentation

Butterflies are among nature's most colorful animals, and provide a living showcase for how extremely bright, chromatic and iridescent coloration can be generated by complex optical mechanisms. The gross characteristics of male butterfly colour patterns are understood to function for species and/or sex recognition, but it is not known whether female mate choice promotes visual exaggeration of this coloration. Here I show that females of the sexually dichromatic species Hypolimnas bolina prefer conspecific males that possess bright iridescent blue/ultraviolet dorsal ornamentation. In separate field and enclosure experiments, using both dramatic and graded wing colour manipulations, I demonstrate that a moderate qualitative reduction in signal brightness and chromaticity has the same consequences as removing the signal entirely. These findings validate a long-held hypothesis, and argue for the importance of intra- versus interspecific selection as the driving force behind the exaggeration of bright, iridescent butterfly colour patterns.     

Hemispheric specialization in dogs for processing different acoustic stimuli

Considerable experimental evidence shows that functional cerebral asymmetries are widespread in animals. Activity of the right cerebral hemisphere has been associated with responses to novel stimuli and the expression of intense emotions, such as aggression, escape behaviour and fear. The left hemisphere uses learned patterns and responds to familiar stimuli. Although such lateralization has been studied mainly for visual responses, there is evidence in primates that auditory perception is lateralized and that vocal communication depends on differential processing by the hemispheres. The aim of the present work was to investigate whether dogs use different hemispheres to process different acoustic stimuli by presenting them with playbacks of a thunderstorm and their species-typical vocalizations. The results revealed that dogs usually process their species-typical vocalizations using the left hemisphere and the thunderstorm sounds using the right hemisphere. Nevertheless, conspecific vocalizations are not always processed by the left hemisphere, since the right hemisphere is used for processing vocalizations when they elicit intense emotion, including fear. These findings suggest that the specialisation of the left hemisphere for intraspecific communication is more ancient that previously thought, and so is specialisation of the right hemisphere for intense emotions.     

Bottlenose dolphins exchange signature whistles when meeting at sea

The bottlenose dolphin, Tursiops truncatus, is one of very few animals that, through vocal learning, can invent novel acoustic signals and copy whistles of conspecifics. Furthermore, receivers can extract identity information from the invented part of whistles. In captivity, dolphins use such signature whistles while separated from the rest of their group. However, little is known about how they use them at sea. If signature whistles are the main vehicle to transmit identity information, then dolphins should exchange these whistles in contexts where groups or individuals join. We used passive acoustic localization during focal boat follows to observe signature whistle use in the wild. We found that stereotypic whistle exchanges occurred primarily when groups of dolphins met and joined at sea. A sequence analysis verified that most of the whistles used during joins were signature whistles. Whistle matching or copying was not observed in any of the joins. The data show that signature whistle exchanges are a significant part of a greeting sequence that allows dolphins to identify conspecifics when encountering them in the wild.