Age-related effects on a hierarchical structure of canine cognition.

The current study investigates whether there are statistically independent age-related influences on the canine cognitive structure and how individual factors moderate cognitive aging on both cross-sectional and longitudinal samples. A battery of seven tasks was administered to 129 pet dogs, on which exploratory and confirmatory factor analyses were employed to unveil the correlational structure underlying individual differences in cognitive performance. The best-fitting model featured a hierarchical structure with two first-order cognitive domains (individual problem solving, learning) and a second-order common factor. These higher order factors exhibited consistency over a period of at least 2.5 years. External validation linked the common factor positively to discrimination and reversal learning performance, exploration, neophilia, activity/excitability, and training level while negatively to cognitive dysfunction symptoms, suggesting that it is a good candidate for a general cognitive factor (canine g). Structural equation models identified three distinct age-related influences, operating on associative learning, on memory, and on canine g. Health status moderated the negative age-canine g relationship, with a stronger association observed in dogs with poorer health status, and no relationship for dogs in good health. On a longitudinal sample (N = 99), we showed that the direction and magnitude of change in canine g over up to 3 years is affected by various interactions between the dogs' age, communication score, baseline performance, and time elapsed since the baseline measurement. These findings underscore the presence of a general cognitive factor in dogs and reveal intriguing parallels between human and canine aging, affirming the translational value of dogs in cognition and aging research.

Alarm or emotion? intranasal oxytocin helps determine information conveyed by dog barks for adult male human listeners.

BACKGROUND: Barks play an important role in interspecific communication between dogs and humans, by allowing a reliable perception of the inner state of dogs for human listeners. However, there is growing concern in society regarding the nuisance that barking dogs cause to the surrounding inhabitants. We assumed that at least in part, this nuisance effect can be explained by particular communicative functions of dog barks. In this study we experimentally tested two separate hypotheses concerning how the content of dog barks could affect human listeners. According to the first hypothesis, barks that convey negative inner states, would especially cause stress in human listeners due to the process called interspecific empathy. Based on the second hypothesis, alarm-type dog barks cause particularly strong stress in the listener, by capitalizing on their specific acoustic makeup (high pitch, low tonality) that resembles to the parameters of a baby's cry. We tested 40 healthy, young adult males in a double-blind placebo controlled experiment, where participants received either intranasal oxytocin or placebo treatment. After an incubation period, they had to evaluate the (1) perceived emotions (happiness, fear and aggression), that specifically created dog bark sequences conveyed to them; and (2) score the annoyance level these dog barks elicited in them. RESULTS: We found that oxytocin treatment had a sensitizing effect on the participants' reactions to negative valence emotions conveyed by dog barks, as they evaluated low fundamental frequency barks with higher aggression scores than the placebo-treated participants did. On the other hand, oxytocin treatment attenuated the annoyance that noisy (atonal) barks elicited from the participants. CONCLUSIONS: Based on these results, we provide first-hand evidence that dog barks provide information to humans (which may also cause stress) in a dual way: through specific attention-grabbing functions and through emotional understanding.

Body size awareness matters when dogs decide whether to detour an obstacle or opt for a shortcut.

Body-awareness is one of the fundamental modules of self-representation. We investigated how body-awareness could contribute to dogs' decision making in a novel spatial problem where multiple solutions are possible. Family dogs (N = 68) had to obtain a treat from behind a transparent fence. They had two options: either detour around the fence (7 m), or take a shortcut through a doorway (2 m). We had three conditions: small door open, large door open, and doors closed. Our results indicated that dogs assess the size of the doorway, and if they find it too small, they decide to detour instead, while in the case of the open large door, they rather opted for the shortcut without hesitation. Shorter headed dogs tended to choose open doors more often, while longer headed dogs rather chose detours, probably because of their better peripheral vision. While body size awareness did not manifest differently in dogs with short or long heads, we showed for the first time a connection between head shape and physical cognition in dogs. We showed that dogs rely on their body-awareness in a naturalistic setting where multiple solutions exist simultaneously. Dogs make decisions without lengthy trial-and-error learning and choose between options based on their body-awareness.

Genetic distance from wolves affects family dogs' reactions towards howls.

Domestication dramatically changes behaviour, including communication, as seen in the case of dogs (Canis familiaris) and wolves (Canis lupus). We tested the hypothesis that domestication may affect an ancient, shared communication form of canids, the howling which seems to have higher individual variation in dogs: the perception and usage of howls may be affected by the genetic relatedness of the breeds to their last common ancestor with wolves ('root distance') and by other individual features like age, sex, and reproductive status. We exposed 68 purebred dogs to wolf howl playbacks and recorded their responses. We identified an interaction between root distance and age on the dogs' vocal and behavioural responses: older dogs from more ancient breeds responded longer with howls and showed more stress behaviours. Our results suggest that domestication impacts vocal behaviour significantly: disintegrating howling, a central, species-specific communication form of canids and gradually eradicating it from dogs' repertoire.

The acoustic bases of human voice identity processing in dogs.

Speech carries identity-diagnostic acoustic cues that help individuals recognize each other during vocal-social interactions. In humans, fundamental frequency, formant dispersion and harmonics-to-noise ratio serve as characteristics along which speakers can be reliably separated. The ability to infer a speaker's identity is also adaptive for members of other species (like companion animals) for whom humans (as owners) are relevant. The acoustic bases of speaker recognition in non-humans are unknown. Here, we tested whether dogs can recognize their owner's voice and whether they rely on the same acoustic parameters for such recognition as humans use to discriminate speakers. Stimuli were pre-recorded sentences spoken by the owner and control persons, played through loudspeakers placed behind two non-transparent screens (with each screen hiding a person). We investigated the association between acoustic distance of speakers (examined along several dimensions relevant in intraspecific voice identification) and dogs' behavior. Dogs chose their owner's voice more often than that of control persons', suggesting that they can identify it. Choosing success and time spent looking in the direction of the owner's voice were positively associated, showing that looking time is an index of the ease of choice. Acoustic distance of speakers in mean fundamental frequency and jitter were positively associated with looking time, indicating that the shorter the acoustic distance between speakers with regard to these parameters, the harder the decision. So, dogs use these cues to discriminate their owner's voice from unfamiliar voices. These findings reveal that dogs use some but probably not all acoustic parameters that humans use to identify speakers. Although dogs can detect fine changes in speech, their perceptual system may not be fully attuned to identity-diagnostic cues in the human voice.

Separation-related behavior of dogs shows association with their reactions to everyday situations that may elicit frustration or fear.

Separation related disorder in dogs is a multi-faceted phenomenon. Dogs can react to the absence of their owner due to different inner states such as fear, panic or frustration. We hypothesized that dogs that are prone to frustration or fearfulness in other contexts would show a different behavioral response to separation from the owner. We investigated the association between inner states in different contexts and separation behaviors by combining a questionnaire with a separation test. Fear-related questionnaire components were rather associated with whining and the absence of barking. Dogs that received higher scores in the demanding component of the questionnaire, which might be in association of the frustration threshold of the dog, barked more and were more likely to scratch the door. Finally, dogs that were more prone to phobic reactions whined somewhat more and tried to escape. We provide empirical support for the assumption that separation-related behavioral responses of dogs might be triggered by different emotions.

Occurrences of non-linear phenomena and vocal harshness in dog whines as indicators of stress and ageing.

During social interactions, acoustic parameters of tetrapods' vocalisations reflect the emotional state of the caller. Higher levels of spectral noise and the occurrence of irregularities (non-linear phenomena NLP) might be negative arousal indicators in alarm calls, although less is known about other distress vocalisations. Family dogs experience different levels of stress during separation from their owner and may vocalise extensively. Analysing their whines can provide evidence for the relationship between arousal and NLP. We recorded 167 family dogs' separation behaviour including vocalisations, assessed their stress level based on behaviour and tested how these, their individual features, and owner reported separation-related problems (SRP) relate to their whines' (N = 4086) spectral noise and NLP. Dogs with SRP produced NLP whines more likely. More active dogs and dogs that tried to escape produced noisier whines. Older dogs' whines were more harmonic than younger ones', but they also showed a higher NLP ratio. Our results show that vocal harshness and NLP are associated with arousal in contact calls, and thus might function as stress indicators. The higher occurrence of NLP in older dogs irrespective to separation stress suggests loss in precise neural control of the larynx, and hence can be a potential ageing indicator.

Dogs (Canis familiaris) recognize their own body as a physical obstacle.

Mental representations of one's own body provide useful reference when negotiating physical environmental challenges. Body-awareness is a neuro-ontogenetic precursor for higher order self-representation, but there is a lack of an ecologically valid experimental approach to it among nonhuman species. We tested dogs (N = 32) in the 'body as an obstacle' task. They had to pick up and give an object to their owner, whilst standing on a small mat. In the test condition we attached the object to the mat, thus the dogs had to leave the mat because otherwise they could not lift the object. Dogs came off the mat more frequently and sooner in the test condition, than in the main control condition, where the object was attached to the ground. This is the first convincing evidence of body awareness through the understanding of the consequence of own actions in a species where previously no higher-order self-representation capacity was found. We urge for an ecologically valid approach, and following of bottom-up methods, in studying modularly constructed self-representation.

Adult, intensively socialized wolves show features of attachment behaviour to their handler.

Dogs' attachment towards humans might be the core of their social skillset, yet the origins of their ability to build such a bond are still unclear. Here we show that adult, hand-reared wolves, similarly to dogs, form individualized relationship with their handler. During separation from their handler, wolves, much like family dogs, showed signs of higher-level stress and contact seeking behaviour, compared to when an unfamiliar person left them. They also used their handler as a secure base, suggesting that the ability to form interspecific social bonds could have been present already in the common ancestor of dogs and wolves. We propose that their capacity to form at least some features of attachment with humans may stem from the ability to form social bond with pack members. This might have been then re-directed to humans during early domestication, providing the basis for the evolution of other socio-cognitive abilities in dogs.

Comparing the tractability of young hand-raised wolves (Canis lupus) and dogs (Canis familiaris).

Dogs live in 45% of households, integrated into various human groups in various societies. This is certainly not true for wolves. We suggest that dogs' increased tractability (meant as individual dogs being easier to control, handle and direct by humans, in contrast to trainability defined as performance increase due to training) makes a crucial contribution to this fundamental difference. In this study, we assessed the development of tractability in hand-raised wolves and similarly raised dogs. We combined a variety of behavioural tests: fetching, calling, obeying a sit signal, hair brushing and walking in a muzzle. Wolf (N = 16) and dog (N = 11) pups were tested repeatedly, between the ages of 3-24 weeks. In addition to hand-raised wolves and dogs, we also tested mother-raised family dogs (N = 12) for fetching and calling. Our results show that despite intensive socialization, wolves remained less tractable than dogs, especially in contexts involving access to a resource. Dogs' tractability appeared to be less context dependent, as they followed human initiation of action in more contexts than wolves. We found no evidence that different rearing conditions (i.e. intensive socialization vs. mother rearing) would affect tractability in dogs. This suggests that during domestication dogs might have been selected for increased tractability, although based on the current data we cannot exclude that the differential speed of development of dogs and wolves or the earlier relocation of wolves to live as a group explains some of the differences we found.

Artificial sounds following biological rules: A novel approach for non-verbal communication in HRI.

Emotionally expressive non-verbal vocalizations can play a major role in human-robot interactions. Humans can assess the intensity and emotional valence of animal vocalizations based on simple acoustic features such as call length and fundamental frequency. These simple encoding rules are suggested to be general across terrestrial vertebrates. To test the degree of this generalizability, our aim was to synthesize a set of artificial sounds by systematically changing the call length and fundamental frequency, and examine how emotional valence and intensity is attributed to them by humans. Based on sine wave sounds, we generated sound samples in seven categories by increasing complexity via incorporating different characteristics of animal vocalizations. We used an online questionnaire to measure the perceived emotional valence and intensity of the sounds in a two-dimensional model of emotions. The results show that sounds with low fundamental frequency and shorter call lengths were considered to have a more positive valence, and samples with high fundamental frequency were rated as more intense across all categories, regardless of the sound complexity. We conclude that applying the basic rules of vocal emotion encoding can be a good starting point for the development of novel non-verbal vocalizations for artificial agents.

Repetition enhancement to voice identities in the dog brain.

In the human speech signal, cues of speech sounds and voice identities are conflated, but they are processed separately in the human brain. The processing of speech sounds and voice identities is typically performed by non-primary auditory regions in humans and non-human primates. Additionally, these processes exhibit functional asymmetry in humans, indicating the involvement of distinct mechanisms. Behavioural studies indicate analogue side biases in dogs, but neural evidence for this functional dissociation is missing. In two experiments, using an fMRI adaptation paradigm, we presented awake dogs with natural human speech that either varied in segmental (change in speech sound) or suprasegmental (change in voice identity) content. In auditory regions, we found a repetition enhancement effect for voice identity processing in a secondary auditory region - the caudal ectosylvian gyrus. The same region did not show repetition effects for speech sounds, nor did the primary auditory cortex exhibit sensitivity to changes either in the segmental or in the suprasegmental content. Furthermore, we did not find evidence for functional asymmetry neither in the processing of speech sounds or voice identities. Our results in dogs corroborate former human and non-human primate evidence on the role of secondary auditory regions in the processing of suprasegmental cues, suggesting similar neural sensitivity to the identity of the vocalizer across the mammalian order.

On the Face of It: No Differential Sensitivity to Internal Facial Features in the Dog Brain.

Dogs are looking at and gaining information from human faces in a variety of contexts. Next to behavioral studies investigating the topic, recent fMRI studies reported face sensitive brain areas in dogs' temporal cortex. However, these studies used whole heads as stimuli which contain both internal (eyes, nose, mouth) and external facial features (hair, chin, face-outline). Behavioral studies reported that (1) recognition of human faces by dogs requires visibility of head contour and that (2) dogs are less successful in recognizing their owners from 2D pictures than from real human heads. In contrast, face perception in humans heavily depends on internal features and generalizes to 2D images. Whether putative face sensitive regions in dogs have comparable properties to those of humans has not been tested so far. In two fMRI experiments, we investigated (1) the location of putative face sensitive areas presenting only internal features of a real human face vs. a mono-colored control surface and (2) whether these regions show higher activity toward live human faces and/or static images of those faces compared to scrambled face images, all with the same outline. In Study 1 (n = 13) we found strong activity for faces in multiple regions, including the previously described temporo-parietal and occipital regions when the control was a mono-colored, homogeneous surface. These differences disappeared in Study 2 (n = 11) when we compared faces to scrambled faces, controlling for low-level visual cues. Our results do not support the assumption that dogs rely on a specialized brain region for processing internal facial characteristics, which is in line with the behavioral findings regarding dogs inability to recognize human faces based on these features.

Interspecific voice discrimination in dogs.

BACKGROUND AND AIMS: Conspecific individual recognition using vocal cues has been shown in a wide range of species but there is no published evidence that dogs are able to recognize their owner based on his/her voice alone (interspecific individual recognition). METHODS: In our test, dogs had to rely on vocal cues to find their hidden owner in a two-way choice task. From behind an opaque screen, both the owner and a control person uttered neutral speech (reading sentences from a receipt) before the dogs were allowed to make their choice. Correct choices were reinforced by food and by verbal praise. RESULTS: During the six-choice trials, dogs chose their owner's voice significantly more often than the control person's voice. There was no effect of learning throughout the trials, and dogs did not show side preference. DISCUSSION: Thus, dogs are able to discriminate interspecific voices, suggesting that they are able to identify their owner based on vocal cues alone. This experimental design allows exploration of the role of individual acoustic parameters (such as fundamental frequency) in voice discrimination.

Biologically Inspired Emotional Expressions for Artificial Agents.

A special area of human-machine interaction, the expression of emotions gains importance with the continuous development of artificial agents such as social robots or interactive mobile applications. We developed a prototype version of an abstract emotion visualization agent to express five basic emotions and a neutral state. In contrast to well-known symbolic characters (e.g., smileys) these displays follow general biological and ethological rules. We conducted a multiple questionnaire study on the assessment of the displays with Hungarian and Japanese subjects. In most cases participants were successful in recognizing the displayed emotions. Fear and sadness were most easily confused with each other while both the Hungarian and Japanese participants recognized the anger display most correctly. We suggest that the implemented biological approach can be a viable complement to the emotion expressions of some artificial agents, for example mobile devices.

Differential effects of speech situations on mothers' and fathers' infant-directed and dog-directed speech: An acoustic analysis.

There is growing evidence that dog-directed and infant-directed speech have similar acoustic characteristics, like high overall pitch, wide pitch range, and attention-getting devices. However, it is still unclear whether dog- and infant-directed speech have gender or context-dependent acoustic features. In the present study, we collected comparable infant-, dog-, and adult directed speech samples (IDS, DDS, and ADS) in four different speech situations (Storytelling, Task solving, Teaching, and Fixed sentences situations); we obtained the samples from parents whose infants were younger than 30 months of age and also had pet dog at home. We found that ADS was different from IDS and DDS, independently of the speakers' gender and the given situation. Higher overall pitch in DDS than in IDS during free situations was also found. Our results show that both parents hyperarticulate their vowels when talking to children but not when addressing dogs: this result is consistent with the goal of hyperspeech in language tutoring. Mothers, however, exaggerate their vowels for their infants under 18 months more than fathers do. Our findings suggest that IDS and DDS have context-dependent features and support the notion that people adapt their prosodic features to the acoustic preferences and emotional needs of their audience.

Investigating emotional contagion in dogs (Canis familiaris) to emotional sounds of humans and conspecifics.

Emotional contagion, a basic component of empathy defined as emotional state-matching between individuals, has previously been shown in dogs even upon solely hearing negative emotional sounds of humans or conspecifics. The current investigation further sheds light on this phenomenon by directly contrasting emotional sounds of both species (humans and dogs) as well as opposed valences (positive and negative) to gain insights into intra- and interspecies empathy as well as differences between positively and negatively valenced sounds. Different types of sounds were played back to measure the influence of three dimensions on the dogs' behavioural response. We found that dogs behaved differently after hearing non-emotional sounds of their environment compared to emotional sounds of humans and conspecifics ("Emotionality" dimension), but the subjects responded similarly to human and conspecific sounds ("Species" dimension). However, dogs expressed more freezing behaviour after conspecific sounds, independent of the valence. Comparing positively with negatively valenced sounds of both species ("Valence" dimension), we found that, independent of the species from which the sound originated, dogs expressed more behavioural indicators for arousal and negatively valenced states after hearing negative emotional sounds. This response pattern indicates emotional state-matching or emotional contagion for negative sounds of humans and conspecifics. It furthermore indicates that dogs recognized the different valences of the emotional sounds, which is a promising finding for future studies on empathy for positive emotional states in dogs.

Do you see what I see? The difference between dog and human visual perception may affect the outcome of experiments.

The visual sense of dogs is in many aspects different than that of humans. Unfortunately, authors do not explicitly take into consideration dog-human differences in visual perception when designing their experiments. With an image manipulation program we altered stationary images, according to the present knowledge about dog-vision. Besides the effect of dogs' dichromatic vision, the software shows the effect of the lower visual acuity and brightness discrimination, too. Fifty adult humans were tested with pictures showing a female experimenter pointing, gazing or glancing to the left or right side. Half of the pictures were shown after they were altered to a setting that approximated dog vision. Participants had difficulty to find out the direction of glancing when the pictures were in dog-vision mode. Glances in dog-vision setting were followed less correctly and with a slower response time than other cues. Our results are the first that show the visual performance of humans under circumstances that model how dogs' weaker vision would affect their responses in an ethological experiment. We urge researchers to take into consideration the differences between perceptual abilities of dogs and humans, by developing visual stimuli that fit more appropriately to dogs' visual capabilities.

Threat-level-dependent manipulation of signaled body size: dog growls' indexical cues depend on the different levels of potential danger.

Body size is an important feature that affects fighting ability; however, size-related parameters of agonistic vocalizations are difficult to manipulate because of anatomical constraints within the vocal production system. Rare examples of acoustic size modulation are due to specific features that enable the sender to steadily communicate exaggerated body size. However, one could argue that it would be more adaptive if senders could adjust their signaling behavior to the fighting potential of their actual opponent. So far there has been no experimental evidence for this possibility. We tested this hypothesis by exposing family dogs (Canis familiaris) to humans with potentially different fighting ability. In a within-subject experiment, 64 dogs of various breeds consecutively faced two threateningly approaching humans, either two men or two women of different stature, or a man and a woman of similar or different stature. We found that the dogs' vocal responses were affected by the gender of the threatening stranger and the dog owner's gender. Dogs with a female owner, or those dogs which came from a household where both genders were present, reacted with growls of lower values of the Pitch-Formant component (including deeper fundamental frequency and lower formant dispersion) to threatening men. Our results are the first to show that non-human animals react with dynamic alteration of acoustic parameters related to their individual indexical features (body size), depending on the level of threat in an agonistic encounter.