Dogs do not use their own experience with novel barriers to infer others' visual access.

Despite extensive research into the Theory of Mind abilities in non-human animals, it remains controversial whether they can attribute mental states to other individuals or whether they merely predict future behaviour based on previous behavioural cues. In the present study, we tested pet dogs (in total, N = 92) on adaptations of the 'goggles test' previously used with human infants and great apes. In both a cooperative and a competitive task, dogs were given direct experience with the properties of novel screens (one opaque, the other transparent) inserted into identical, but differently coloured, tunnels. Dogs learned and remembered the properties of the screens even when, later on, these were no longer directly visible to them. Nevertheless, they were not more likely to follow the experimenter's gaze to a target object when the experimenter could see it through the transparent screen. Further, they did not prefer to steal a forbidden treat first in a location obstructed from the experimenter's view by the opaque screen. Therefore, dogs did not show perspective-taking abilities in this study in which the only available cue to infer others' visual access consisted of the subjects' own previous experience with novel visual barriers. We conclude that the behaviour of our dogs, unlike that of infants and apes in previous studies, does not show evidence of experience-projection abilities.

Domestic dogs as a comparative model for social neuroscience: Advances and challenges.

Dogs and humans have lived together for thousands of years and share many analogous socio-cognitive skills. Dog neuroimaging now provides insight into the neural bases of these shared social abilities. Here, we summarize key findings from dog fMRI identifying neocortical brain areas implicated in visual social cognition, such as face, body, and emotion perception, as well as action observation in dogs. These findings provide converging evidence that the temporal cortex plays a significant role in visual social cognition in dogs. We further briefly review investigations into the neural base of the dog-human relationship, mainly involving limbic brain regions. We then discuss current challenges in the field, such as statistical power and lack of common template spaces, and how to overcome them. Finally, we argue that the foundation has now been built to investigate and compare the neural bases of more complex socio-cognitive phenomena shared by dogs and humans. This will strengthen and expand the role of the domestic dog as a powerful comparative model species and provide novel insights into the evolutionary roots of social cognition.

Corrigendum: Socially priming dogs in an overimitation task.

[This corrects the article DOI: 10.3389/fpsyg.2023.1063132.].

Functional mapping of the somatosensory cortex using noninvasive fMRI and touch in awake dogs.

Dogs are increasingly used as a model for neuroscience due to their ability to undergo functional MRI fully awake and unrestrained, after extensive behavioral training. Still, we know rather little about dogs' basic functional neuroanatomy, including how basic perceptual and motor functions are localized in their brains. This is a major shortcoming in interpreting activations obtained in dog fMRI. The aim of this preregistered study was to localize areas associated with somatosensory processing. To this end, we touched N = 22 dogs undergoing fMRI scanning on their left and right flanks using a wooden rod. We identified activation in anatomically defined primary and secondary somatosensory areas (SI and SII), lateralized to the contralateral hemisphere depending on the side of touch, and importantly also activation beyond SI and SII, in the cingulate cortex, right cerebellum and vermis, and the sylvian gyri. These activations may partly relate to motor control (cerebellum, cingulate), but also potentially to higher-order cognitive processing of somatosensory stimuli (rostral sylvian gyri), and the affective aspects of the stimulation (cingulate). We also found evidence for individual side biases in a vast majority of dogs in our sample, pointing at functional lateralization of somatosensory processing. These findings not only provide further evidence that fMRI is suited to localize neuro-cognitive processing in dogs, but also expand our understanding of in vivo touch processing in mammals, beyond classically defined primary and secondary somatosensory cortices.

Do dogs preferentially encode the identity of the target object or the location of others' actions?

The ability to make sense of and predict others' actions is foundational for many socio-cognitive abilities. Dogs (Canis familiaris) constitute interesting comparative models for the study of action perception due to their marked sensitivity to human actions. We tested companion dogs (N = 21) in two screen-based eye-tracking experiments, adopting a task previously used with human infants and apes, to assess which aspects of an agent's action dogs consider relevant to the agent's underlying intentions. An agent was shown repeatedly acting upon the same one of two objects, positioned in the same location. We then presented the objects in swapped locations and the agent approached the objects centrally (Experiment 1) or the old object in the new location or the new object in the old location (Experiment 2). Dogs' anticipatory fixations and looking times did not reflect an expectation that agents should have continued approaching the same object nor the same location as witnessed during the brief familiarization phase; this contrasts with some findings with infants and apes, but aligns with findings in younger infants before they have sufficient motor experience with the observed action. However, dogs' pupil dilation and latency to make an anticipatory fixation suggested that, if anything, dogs expected the agents to keep approaching the same location rather than the same object, and their looking times showed sensitivity to the animacy of the agents. We conclude that dogs, lacking motor experience with the observed actions of grasping or kicking performed by a human or inanimate agent, might interpret such actions as directed toward a specific location rather than a specific object. Future research will need to further probe the suitability of anticipatory looking as measure of dogs' socio-cognitive abilities given differences between the visual systems of dogs and primates.

Kea, bird of versatility. Kea parrots (Nestor notabilis) show high behavioural flexibility in solving a demonstrated sequence task.

Social learning is an important aspect of dealing with the complexity of life. The transmission of information via the observation of other individuals is a cost-effective way of acquiring information. It is widespread within the animal kingdom but may differ strongly in the social learning mechanisms applied by the divergent species. Here we tested eighteen Kea (Nestor notabilis) parrots on their propensity to socially learn, and imitate, a demonstrated sequence of steps necessary to open an apparatus containing food. The demonstration by a conspecific led to more successful openings by observer birds, than control birds without a demonstration. However, all successful individuals showed great variation in their response topography and abandoned faithfully copying the task in favour of exploration. While the results provide little evidence for motor imitation they do provide further evidence for kea's propensity towards exploration and rapidly shifting solving strategies, indicative of behavioural flexibility. Supplementary Information: The online version contains supplementary material available at 10.1007/s10336-023-02127-y.

Investigating belief understanding in children in a nonverbal ambiguous displacement and communication setting.

Finding ways to investigate false belief understanding nonverbally is not just important for preverbal children but also is the only way to assess theory of mind (ToM)-like abilities in nonhuman animals. In this preregistered study, we adapted the design from a previous study on pet dogs to investigate false belief understanding in children and to compare it with belief understanding of those previously tested dogs. A total of 32 preschool children (aged 5-6 years) saw the displacement of a reward and obtained nonverbal cueing of the empty container from an adult communicator holding either a true or false belief. In the false belief condition, when the communicator did not know the location of the reward, children picked the baited container, but not the cued container, more often than the empty one. In the true belief condition, when the communicator witnessed the displacement yet still cued the wrong container, children performed randomly. The children's behavior pattern was at odds with that of the dogs tested in a previous study, which picked the cued container more often when the human communicator held a false belief. In addition to species comparisons, because our task does not require verbal responses or relational sentence understanding, it can also be used in preverbal children. The children in our study behaved in line with the existing ToM literature, whereas most (but not all) dogs from the previously collected sample, although sensitive to differences between the belief conditions, deviated from the children. This difference suggests that using closely matched paradigms and experimental procedures can reveal decisive differences in belief processing between species. It also demonstrates the need for a more comprehensive exploration and direct comparison of the various aspects of false belief processing and ToM in different species to understand the evolution of social cognition.

Dogs Rely On Visual Cues Rather Than On Effector-Specific Movement Representations to Predict Human Action Targets.

The ability to predict others' actions is one of the main pillars of social cognition. We investigated the processes underlying this ability by pitting motor representations of the observed movements against visual familiarity. In two pre-registered eye-tracking experiments, we measured the gaze arrival times of 16 dogs (Canis familiaris) who observed videos of a human or a conspecific executing the same goal-directed actions. On the first trial, when the human agent performed human-typical movements outside dogs' specific motor repertoire, dogs' gaze arrived at the target object anticipatorily (i.e., before the human touched the target object). When the agent was a conspecific, dogs' gaze arrived to the target object reactively (i.e., upon or after touch). When the human agent performed unusual movements more closely related to the dogs' motor possibilities (e.g., crawling instead of walking), dogs' gaze arrival times were intermediate between the other two conditions. In a replication experiment, with slightly different stimuli, dogs' looks to the target object were neither significantly predictive nor reactive, irrespective of the agent. However, when including looks at the target object that were not preceded by looks to the agents, on average dogs looked anticipatorily and sooner at the human agent's action target than at the conspecific's. Looking times and pupil size analyses suggest that the dogs' attention was captured more by the dog agent. These results suggest that visual familiarity with the observed action and saliency of the agent had a stronger influence on the dogs' looking behaviour than effector-specific movement representations in anticipating action targets.

A pilot study into the effects of PTSD-assistance dogs' work on their salivary cortisol levels and their handlers' Quality of life.

Assistance dogs for people with Posttraumatic Stress Disorder (PTSD) support their handlers by performing tasks that are supposed to mitigate the effects of their mental disability. This study examined the Quality of Life (QoL) of PTSD-assistance dogs' handlers in Austria and Germany using a qualitative online questionnaire based on the Capability Approach. To correspondingly explore whether the involved assistance dogs experience distress triggered by their daily schedules, we measured their salivary cortisol values. These were compared to the cortisol levels of companion dogs without special tasks, as well as diabetic-signal dogs that have a similar workload. Our results showed that people suffering from PTSD-symptoms can improve their QoL with the aid of their assistance dog. However, being accompanied by an assistance dog creates new social barriers. Surprisingly, we found significantly lower salivary cortisol levels in PTSD-assistance dogs compared to the control groups. We conclude that a positive relationship between PTSD-assistance dogs and their handlers can reduce stress on both sides, and that training well tuned to the requirements of an assistance dog can prevent stress in their daily lives.

Quantifying Isoprenoids in the Ergosterol Biosynthesis by Gas Chromatography-Mass Spectrometry.

The ergosterol pathway is a promising target for the development of new antifungals since its enzymes are essential for fungal cell growth. Appropriate screening assays are therefore needed that allow the identification of potential inhibitors. We developed a whole-cell screening method, which can be used to identify compounds interacting with the enzymes of isoprenoid biosynthesis, an important part of the ergosterol biosynthesis pathway. The method was validated according to the EMEA guideline on bioanalytical method validation. Aspergillus fumigatus hyphae and Saccharomyces cerevisiae cells were lysed mechanically in an aqueous buffer optimized for the enzymatic deconjugation of isoprenoid pyrophosphates. The residual alcohols were extracted, silylated and analyzed by GC-MS. The obtained isoprenoid pattern provides an indication of the inhibited enzyme, due to the accumulation of specific substrates. By analyzing terbinafine-treated A. fumigatus and mutant strains containing tunable gene copies of erg9 or erg1, respectively, the method was verified. Downregulation of erg9 resulted in a high accumulation of intracellular farnesol as well as elevated levels of geranylgeraniol and isoprenol. The decreased expression of erg1 as well as terbinafine treatment led to an increased squalene content. Additional analysis of growth medium revealed high farnesyl pyrophosphate levels extruded during erg9 downregulation.

Dogs' expectations about occlusion events: from expectancy violation to exploration.

Previous research on human infants has shown that violations of basic physical regularities can stimulate exploration, which may represent a type of hypothesis testing aimed at acquiring knowledge about new causal relationships. In this study, we examined whether a similar connection between expectancy violation and exploration exists in nonhuman animals. Specifically, we investigated how dogs react to expectancy violations in the context of occlusion events. Throughout three experiments, dogs exhibited longer looking times at expectancy-inconsistent events than at consistent ones. This finding was further supported by pupil size analyses in the first two eye-tracking experiments. Our results suggest that dogs expect objects to reappear when they are not obstructed by a screen and consider the size of the occluding screen in relation to the occluded object. In Experiment 3, expectancy violations increased the dogs' exploration of the target object, similar to the findings with human infants. We conclude that expectancy violations can provide learning opportunities for nonhuman animals as well.

Two-action task, testing imitative social learning in kea (Nestor notabilis).

Social learning is an adaptive way of dealing with the complexity of life as it reduces the risk of trial-and-error learning. Depending on the type of information acquired, and associations formed, several mechanisms within the larger taxonomy of social learning can be distinguished. Imitation is one such process within this larger taxonomy, it is considered cognitively demanding and is associated with high-fidelity response matching. The present study reproduced a 2002 study conducted by Heyes and Saggerson, which successfully illustrated motor imitation in budgerigars (Melopsittacus undulatus). In our study, eighteen kea (Nestor notabilis) that observed a trained demonstrator remove a stopper from a test box (1) took less time from hopping on the box to feeding (response duration) in session one and (2) were faster in making a vertical removal response on the stopper once they hopped on the box (removal latency) in session one than non-observing control group individuals. In contrast to the budgerigars (Heyes and Saggerson, Ani Behav. 64:851-859, 2002) the present study could not find evidence of motor imitation in kea. The results do illustrate, however, that there were strong social effects on exploration rates indicating motivational and attentional shifts. Furthermore, the results may suggest a propensity toward emulation in contrast to motor imitation or alternatively selectivity in the application of imitation.

Functionally analogous body- and animacy-responsive areas are present in the dog (Canis familiaris) and human occipito-temporal lobe.

Comparing the neural correlates of socio-cognitive skills across species provides insights into the evolution of the social brain and has revealed face- and body-sensitive regions in the primate temporal lobe. Although from a different lineage, dogs share convergent visuo-cognitive skills with humans and a temporal lobe which evolved independently in carnivorans. We investigated the neural correlates of face and body perception in dogs (N = 15) and humans (N = 40) using functional MRI. Combining univariate and multivariate analysis approaches, we found functionally analogous occipito-temporal regions involved in the perception of animate entities and bodies in both species and face-sensitive regions in humans. Though unpredicted, we also observed neural representations of faces compared to inanimate objects, and dog compared to human bodies in dog olfactory regions. These findings shed light on the evolutionary foundations of human and dog social cognition and the predominant role of the temporal lobe.

Socially priming dogs in an overimitation task.

Overimitation - the copying of another's unnecessary or irrelevant actions toward a goal - is largely considered to be uniquely human. Recent studies, however, have found evidence of this behavior in dogs. Humans seem to overimitate more or less depending on social factors, such as the cultural origin of the demonstrator. Like humans, dogs may have social motivations behind their overimitation, since they have been shown to copy irrelevant actions more from their caregivers than from strangers. By using priming methodology, this study aimed to investigate whether dogs' overimitation can be facilitated via the experimental manipulation of their attachment-based motivations. To test this, we invited caregivers to demonstrate goal-irrelevant and relevant actions to their dog, following either a dog-caregiver relationship prime, a dog-caregiver attention prime, or no prime. Our results showed no significant main effect of priming on copying behavior for either relevant or irrelevant actions, but we found a trend that unprimed dogs copied the least actions overall. Additionally, dogs copied their caregiver's relevant actions more often and more faithfully as the number of trials increased. Our final finding was that dogs were much more likely to copy irrelevant actions after (rather than before) already achieving the goal. This study discusses the social motivations behind dog imitative behavior, and has potential methodological implications regarding the influence of priming on dog behavioral studies.

Validation of a New Coil Array Tailored for Dog Functional Magnetic Resonance Imaging Studies.

Comparative neuroimaging allows for the identification of similarities and differences between species. It provides an important and promising avenue, to answer questions about the evolutionary origins of the brain´s organization, in terms of both structure and function. Dog functional magnetic resonance imaging (fMRI) has recently become one particularly promising and increasingly used approach to study brain function and coevolution. In dog neuroimaging, image acquisition has so far been mostly performed with coils originally developed for use in human MRI. Since such coils have been tailored to human anatomy, their sensitivity and data quality is likely not optimal for dog MRI. Therefore, we developed a multichannel receive coil (K9 coil, read "canine") tailored for high-resolution functional imaging in canines, optimized for dog cranial anatomy. In this paper we report structural (n = 9) as well as functional imaging data (resting-state, n = 6; simple visual paradigm, n = 9) collected with the K9 coil in comparison to reference data collected with a human knee coil. Our results show that the K9 coil significantly outperforms the human knee coil, improving the signal-to-noise ratio (SNR) across the imaging modalities. We noted increases of roughly 45% signal-to-noise in the structural and functional domain. In terms of translation to fMRI data collected in a visual flickering checkerboard paradigm, group-level analyses show that the K9 coil performs better than the knee coil as well. These findings demonstrate how hardware improvements may be instrumental in driving data quality, and thus, quality of imaging results, for dog-human comparative neuroimaging.

Canine perspective-taking.

An important question in the study of canine cognition is how dogs understand humans, given that they show impressive abilities for interacting and communicating with us. In this review, we describe and discuss studies that have investigated dogs' perspective-taking abilities. There is solid evidence that dogs are not only sensitive to the gaze of others, but also their attention. We specifically address the question whether dogs have the ability to take the perspective of others and thus come to understand what others can or cannot perceive. From the latter, they may then infer what others know and use this representation to anticipate what others do next. Still, dogs might simply rely on directly observable cues and on what they themselves can perceive when they assess what others can perceive. And instead of making inferences from representations of others' mental states, they may have just learned that certain behaviours of ours lead to certain outcomes. However, recent research seems to challenge this low-level explanation. Dogs have solved several perspective-taking tasks instantly and reliably across a large number of variations, including geometrical gaze-following, stealing in the dark, concealing information from others, and Guesser/Knower differentiation. In the latter studies, dogs' choices between two human informants were strongly influenced by cues related to the humans' visual access to the food, even when the two informants behaved identically. And finally, we review a recent study that found dogs reacting differently to misleading suggestions of human informants that have either a true or false belief about the location of food. We discuss this surprising result in terms of the comprehension of reality-incongruent mental states, which is considered as a hallmark of Theory of Mind acquisition in human development. Especially on the basis of the latter findings, we conclude that pet dogs might be sensitive to what others see, know, intend, and believe. Therefore, this ability seems to have evolved not just in the corvid and primate lineages, but also in dogs.

Emulative learning of a two-step task in free-ranging domestic pigs.

Previous research showed that young domestic pigs learn through observation of conspecifics by using social learning mechanisms like social facilitation, enhancement effects, and even object movement re-enactment. The latter suggests some form of emulative learning in which the observer learns about the object's movements and affordances. As it remains unclear whether pigs need a social agent to learn about objects, we provided 36 free-ranging domestic pigs with varying degrees of social to non-social demonstrations on how to solve a two-step manipulative foraging task: observers watched either a conspecific or a human demonstrator, or self-moving objects ("ghost control"), or a ghost control accompanied by an inactive conspecific bystander. In addition, 22 subjects that were previously tested without any demonstrator were used as a non-observer control. To solve the task, the subjects had to first remove a plug from its recess to then be able to slide a cover to the side, which would lay open a food compartment. Observers interacted longer with the relevant objects (plugs) and were more successful in solving the task compared to non-observers. We found no differences with regard to success between the four observer groups, indicating that the pigs mainly learned about the apparatus rather than about the actions. As the only common feature of the different demonstrations was the movement of the plug and the cover, we conclude the observer pigs learned primarily by emulation, suggesting that social agents are not necessary for pigs when learning through observation.

Unwilling or unable? Using three-dimensional tracking to evaluate dogs' reactions to differing human intentions.

The extent to which dogs (Canis familiaris) as a domesticated species understand human intentions is still a matter of debate. The unwilling-unable paradigm has been developed to examine whether nonhuman animals are sensitive to intentions underlying human actions. In this paradigm, subjects tended to wait longer in the testing area when presented with a human that appeared willing but unable to transfer food to them compared to an unwilling (teasing) human. In the present study, we conducted the unwilling-unable paradigm with dogs using a detailed behavioural analysis based on machine-learning driven three-dimensional tracking. Throughout two preregistered experiments, we found evidence, in line with our prediction, that dogs reacted more impatiently to actions signalling unwillingness to transfer food rather than inability. These differences were consistent through two different samples of pet dogs (total n = 96) and they were evident also in the machine-learning generated three-dimensional tracking data. Our results therefore provide robust evidence that dogs distinguish between similar actions (leading to the same outcome) associated with different intentions. However, their reactions did not lead to any measurable preference for one experimenter over the other in a subsequent transfer phase. We discuss different cognitive mechanisms that might underlie dogs' performance in this paradigm.

How to improve data quality in dog eye tracking.

Pupil-corneal reflection (P-CR) eye tracking has gained a prominent role in studying dog visual cognition, despite methodological challenges that often lead to lower-quality data than when recording from humans. In the current study, we investigated if and how the morphology of dogs might interfere with tracking of P-CR systems, and to what extent such interference, possibly in combination with dog-unique eye-movement characteristics, may undermine data quality and affect eye-movement classification when processed through algorithms. For this aim, we have conducted an eye-tracking experiment with dogs and humans, and investigated incidences of tracking interference, compared how they blinked, and examined how differential quality of dog and human data affected the detection and classification of eye-movement events. Our results show that the morphology of dogs' face and eye can interfere with tracking methods of the systems, and dogs blink less often but their blinks are longer. Importantly, the lower quality of dog data lead to larger differences in how two different event detection algorithms classified fixations, indicating that the results of key dependent variables are more susceptible to choice of algorithm in dog than human data. Further, two measures of the Nyström & Holmqvist (Behavior Research Methods, 42(4), 188-204, 2010) algorithm showed that dog fixations are less stable and dog data have more trials with extreme levels of noise. Our findings call for analyses better adjusted to the characteristics of dog eye-tracking data, and our recommendations help future dog eye-tracking studies acquire quality data to enable robust comparisons of visual cognition between dogs and humans.