Cognitive and sensory capacity each contribute to the canine spatial bias.

Dogs interpret cues as being about location, which human infants would relate to objects. This spatial bias could shed light on the evolution of object-centered thought, however, research needs to rule out that this is not a by-product of dogs' weaker (compared to humans) visual capacities. In this study, we used a data set in which dogs were tested in two types of learning tasks (discrimination and reversal learning) with two types of rewarded cues (location and object features). In both tasks, dogs displayed spatial bias, that is, faster learning when the rewarded cue was a location. We investigated how sensory and cognitive capacity each contributes to this spatial bias. To this end, an estimate for general cognitive ability (g) was obtained from a battery of tests for some of the dogs. Cephalic index, a feature targeted in breeding and linked to differences in visual capacity, correlated negatively with the expression of spatial bias only in the easier discrimination learning task, while a negative correlation between g factor and spatial bias scores emerged in the more difficult reversal learning task. We conclude that dogs' spatial bias cannot be reduced to a sensory limitation and is easier to overcome with greater cognitive capacity.

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.

Sleep-physiological correlates of brachycephaly in dogs.

The shape of the cranium is one of the most notable physical changes induced in domestic dogs through selective breeding and is measured using the cephalic index (CI). High CI (a ratio of skull width to skull length > 60) is characterized by a short muzzle and flat face and is referred to as brachycephaly. Brachycephalic dogs display some potentially harmful changes in neuroanatomy, and there are implications for differences in behavior, as well. The path from anatomy to cognition, however, has not been charted in its entirety. Here, we report that sleep-physiological markers of white-matter loss (high delta power, low frontal spindle frequency, i.e., spindle waves/s), along with a spectral profile for REM (low beta, high delta) associated with low intelligence in humans, are each linked to higher CI values in the dog. Additionally, brachycephalic subjects spent more time sleeping, suggesting that the sleep apnea these breeds usually suffer from increases daytime sleepiness. Within sleep, more time was spent in the REM sleep stage than in non-REM, while REM duration was correlated positively with the number of REM episodes across dogs. It is currently not clear if the patterns of sleep and sleep-stage duration are mainly caused by sleep-impairing troubles in breathing and thermoregulation, present a juvenile-like sleeping profile, or are caused by neuro-psychological conditions secondary to the effects of brachycephaly, e.g., frequent REM episodes are known to appear in human patients with depression. While future studies should more directly address the interplay of anatomy, physiology, and behavior within a single experiment, this represents the first description of how the dynamics of the canine brain covary with CI, as measured in resting companion dogs using a non-invasive sleep EEG methodology. The observations suggest that the neuroanatomical changes accompanying brachycephaly alter neural systems in a way that can be captured in the sleep EEG, thus supporting the utility of the latter in the study of canine brain health and function.

Investigating responses to object-labels in the domestic dog (Canis familiaris).

Since the dawn of comparative cognitive research, dogs were suspected to possess some capacity for responding to human spoken language. Neuroimaging studies have supported the existence of relevant mechanisms, but convincing behavioral performance is rare, with only few exceptional dogs worldwide demonstrating a lexicon of object-labels they respond to. In the present study we aimed to investigate if and how a capacity for processing verbal stimuli is expressed in dogs (N = 20), whose alleged knowledge of verbal labels is only backed-up by owner reports taken at face value, and concerning only a few words (on average 5). Dogs were tested in a two-choice paradigm with familiar objects. The experiment was divided into a cue-control condition (objects visible to the owner vs. shielded by a panel, thereby controlling the owner's ability to emit cues to the dog) and a response type condition (fetching vs. looking). Above chance performance in fetching and looking at the named object emerged on the level of the sample as a whole. Only one individual performed reliably above chance, but the group-level effect did not depend on this data point. The presence of the panel also had no influence, which supports that performance was not driven by non-verbal cues from the owners. The group-level effect suggests that in typical dogs object-label learning is an instable process, either due to the animals primarily engaging in contextual learning or possibly analogous to the early stages of implicit, statistical learning of words in humans and opposed to the rapid mapping reported in exceptional dogs with larger passive vocabulary.

Free will strikes back: Steady-state movement-related cortical potentials are modulated by cognitive control.

In psychology and neuroscience, opposition to free will has asserted that any degree of perceived self-control or choice is a mere epiphenomenon which provides no meaningful influence on action. The present research tested the validity of this conclusion by designing a paradigm in which the potential effect of self-monitoring on motor output could be investigated. Using a repetitive finger tapping task that evokes automatic patterns in participants tapping responses, we have obtained evidence that (1) participants may voluntarily reduce the predictability of their tapping patterns (2) by exercising cognitive control that (3) modulates response-locked steady-state movement-related potentials over primary and supplementary motor areas. These findings challenge the most radical accounts of the nonexistence of free will and instead provide support for a more balanced model of human behaviour in which cognitive control may constrain automatic response tendencies in response preparation and action execution.

Shared and unique features of mammalian sleep spindles - insights from new and old animal models.

Sleep spindles are phasic events observed in mammalian non-rapid eye movement sleep. They are relevant today in the study of memory consolidation, sleep quality, mental health and ageing. We argue that our advanced understanding of their mechanisms has not exhausted the utility and need for animal model work. This is both because some topics, like cognitive ageing, have not yet been addressed sufficiently in comparative efforts and because the evolutionary history of this oscillation is still poorly understood. Comparisons across species often are either limited to referencing the classical cat and rodent models, or are over-inclusive, uncritically including reports of sleep spindles in rarely studied animals. In this review, we discuss the emergence of new (dog and sheep) models for sleep spindles and compare the strengths and shortcomings of new and old models based on the three validation criteria for animal models - face, predictive, and construct validity. We conclude that an emphasis on cognitive ageing might dictate the future of comparative sleep spindle studies, a development that is already becoming visible in studies on dogs. Moreover, reconstructing the evolutionary history of sleep spindles will require more stringent criteria for their identification, across more species. In particular, a stronger emphasis on construct and predictive validity can help verify if spindle-like events in other species are actual sleep spindles. Work in accordance with such stricter validation suggests that sleep spindles display more universally shared features, like defining frequency, than previously thought.

Human Expressions of Object Preference Affect Dogs' Perceptual Focus, but Not Their Action Choices.

Inspired by work on infants, we investigated whether dogs' behaviors are guided by human displays of preference, contrasting with the animals' own choices. In a rewarded fetching task, dogs override their own interest toward "disgusting" objects and retrieve what the owner prefers. However, in previous research, both objects were inherently neutral to the dogs and they might have chosen the owner's object because a "happy owner" predicts a positive outcome. If dogs are indeed able to override their own interests, we expected them to fetch the owner's object even if (1) they would prefer another one and (2) do not receive a reward for it. Two objects were compared, a toy (hoop) and a bracelet. After establishing that the toy was preferred by all dogs in an initial test of preference, we applied a two-choice procedure to test if either fetching or looking at the objects from a distance would be affected by the owner's choice. In Study 1, the owner demonstrated happiness toward the bracelet and disgust toward the toy with both facial and body gestures accompanied by verbalizations. Then the owner asked the dog to fetch, without providing additional guiding cues. All dogs fetched the toy, indicating that their own choice was not overcome by the positive emotional state signaled by the owner. To avoid direct contact with the objects, in Study 2 we placed the objects on an unreachable spot after the emotion demonstration and measured the duration of looking at the objects. In the "bracelet" (non-matching) group the owners demonstrated happiness toward the bracelet and disgust toward the toy, similar to Study 1. In the "toy" (matching) group the owners showed happiness toward the toy and disgust toward the bracelet. When the objects were placed on the unreachable spot, dogs looked at both objects for the same amount of time in the non-matching group, but longer at the toy in the matching group. Although the studies did not demonstrate that dogs override their own preferences for an object, the results suggested that the owners' expressed preference was perceived by the dogs and guided their perceptual focus.

A Preliminary Study toward a Rapid Assessment of Age-Related Behavioral Differences in Family Dogs.

Over the last few years, several efforts have been undertaken to characterize the aging process in dogs. In the present study, we evaluate a short protocol measuring dogs' cognitive, social, and physical capacities. Our aim was to develop a feasible test battery, with minimal pre-training requirements, no complex devices, and which is set outdoors (i.e., a specific testing room is not needed). As ageing in dogs is usually associated with a decrease in activity, we also assessed the personality trait activity/excitability with a dog personality questionnaire. Four subtests proved sensitive to the dogs' age. In particular, old dogs displayed less approaching and following behaviors toward an unknown but friendly human, showed both less avoidance and interest toward a novel object, looked less at the owner when faced with an unsolvable problem, and performed worse on the short-term memory task. Previous test procedures for investigating age-related changes involve expensive and/or complicated devices and extensive pre-training. The main advantage of the proposed battery is to reduce costs and efforts in veterinary assessments. Further tests in same-breed, large samples and between dogs with mild and severe cognitive impairments will be needed in order to further validate the battery.

Reliability of Family Dogs' Sleep Structure Scoring Based on Manual and Automated Sleep Stage Identification.

Non-invasive polysomnography recording on dogs has been claimed to produce data comparable to those for humans regarding sleep macrostructure, EEG spectra and sleep spindles. While functional parallels have been described relating to both affective (e.g., emotion processing) and cognitive (e.g., memory consolidation) domains, methodologically relevant questions about the reliability of sleep stage scoring still need to be addressed. In Study 1, we analyzed the effects of different coders and different numbers of visible EEG channels on the visual scoring of the same polysomnography recordings. The lowest agreement was found between independent coders with different scoring experience using full (3 h-long) recordings of the whole dataset, and the highest agreement within-coder, using only a fraction of the original dataset (randomly selected 100 epochs (i.e., 100 × 20 s long segments)). The identification of drowsiness was found to be the least reliable, while that of non-REM (rapid eye movement, NREM) was the most reliable. Disagreements resulted in no or only moderate differences in macrostructural and spectral variables. Study 2 targeted the task of automated sleep EEG time series classification. Supervised machine learning (ML) models were used to help the manual annotation process by reliably predicting if the dog was sleeping or awake. Logistic regression models (LogREG), gradient boosted trees (GBT) and convolutional neural networks (CNN) were set up and trained for sleep state prediction from already collected and manually annotated EEG data. The evaluation of the individual models suggests that their combination results in the best performance: ~0.9 AUC test scores.

Possible association between spindle frequency and reversal-learning in aged family dogs.

In both humans and dogs sleep spindle occurrence between acquisition and recall of a specific memory correlate with learning performance. However, it is not known whether sleep spindle characteristics are also linked to performance beyond the span of a day, except in regard to general mental ability in humans. Such a relationship is likely, as both memory and spindle expression decline with age in both species (in dogs specifically the density and amplitude of slow spindles). We investigated if spindle amplitude, density (spindles/minute) and/or frequency (waves/second) correlate with performance on a short-term memory and a reversal-learning task in old dogs (> 7 years), when measurements of behavior and EEG were on average a month apart. Higher frequencies of fast (≥ 13 Hz) spindles on the frontal and central midline electrodes, and of slow spindles (≤ 13 Hz) on the central midline electrode were linked to worse performance on a reversal-learning task. The present findings suggest a role for spindle frequency as a biomarker of cognitive aging across species: Changes in spindle frequency are associated with dementia risk and onset in humans and declining learning performance in the dog.

Correction: Assertive, trainable and older dogs are perceived as more dominant in multi-dog households.

[This corrects the article DOI: 10.1371/journal.pone.0227253.].

Assertive, trainable and older dogs are perceived as more dominant in multi-dog households.

Social dominance is an important and widely used concept, however, different interpretations have led to ambiguity in the scientific literature and in popular science. Even though in ethology dominance is an attribute of dyadic encounters, and not a characteristic of the individual, 'dominance' has often been referred to as a personality trait in animals. Since few studies have specifically examined the link between personality traits and dominance status, we investigated this in dogs living in multi-dog households using a questionnaire, which required owners to specify whether the dog had a dominant or submissive status, and comprised items of both the features of the individual (i.e. personality traits) and previous social experience (interactions with group members and strangers). Four distinct personality factors emerged from 23 behavioural items by principal component analysis, labelled as assertiveness, trainability, intraspecific aggression and independence. Binomial logistic regression was used to examine how the demographic information of the dogs and the personality factors predicted the owner's estimate of the dog' status as dominant or submissive. The personality factor assertiveness accounted for 34% of the variance in dominance status, trainability 5% and dog age contributed 4%. Dogs perceived as dominant scored more highly on the factors assertiveness and trainability, which can help explain why 'dominance' has often been suggested to be a personality trait, rather than a dyad-specific social status according to different traditions in behavioural research. Similar to the 'social dominance' trait in humans, owner ascribed dominance showed a quadratic trajectory in cross-sectional mean change across the lifespan, increasing during adulthood and then maintaining high levels until old age. Overall, our study proposes a multifactorial background of dominance relationships in pet dogs, suggesting that not only previous experience of social interactions between individuals but also age and personality traits influence owner perceived dominance status in multi-dog households.

Averaging sleep spindle occurrence in dogs predicts learning performance better than single measures.

Although a positive link between sleep spindle occurrence and measures of post-sleep recall (learning success) is often reported for humans and replicated across species, the test-retest reliability of the effect is sometimes questioned. The largest to date study could not confirm the association, however methods for automatic spindle detection diverge in their estimates and vary between studies. Here we report that in dogs using the same detection method across different learning tasks is associated with observing a positive association between sleep spindle density (spindles/minute) and learning success. Our results suggest that reducing measurement error by averaging across measurements of density and learning can increase the visibility of this effect, implying that trait density (estimated through averaged occurrence) is a more reliable predictor of cognitive performance than estimates based on single measures.

Age-related differences and sexual dimorphism in canine sleep spindles.

Non-REM bursts of activity in the sigma range (9-16 Hz) typical of sleep spindles predict learning in dogs, similar to humans and rats. Little is known, however, about the age-related changes in amplitude, density (spindles/minute) and frequency (waves/second) of canine spindles. We investigated a large sample (N = 155) of intact and neutered pet dogs of both sexes, varying in breed and age, searching for spindles in segments of non-REM sleep. We recorded EEG from both a frontal midline electrode (Fz) and a central midline electrode (Cz) in 55.5% of the dogs, in the remaining animals only the Fz electrode was active (bipolar derivation). A similar topography was observed for fast (≥13 Hz) spindle occurrence as in humans (fast spindle number, density on Cz > Fz). For fast spindles, density was higher in females, and increased with age. These effects were more pronounced among intact animals and on Fz. Slow spindle density declined and fast spindle frequency increased with age on Cz, while on Fz age-related amplitude decline was observed. The frequency of fast spindles on Fz and slow spindles on Cz was linked to both sex and neutering, suggesting modulation by sexual hormones. Intact females displayed higher frequencies than males and neutered females. Our findings support the argument that sigma bursts in the canine non-REM sleep are analogous to human sleep spindles, and suggest that slow and fast spindles display different trajectories related to age, of which an increase in frontal fast spindles is unique to dogs.

Encounters between pairs of unfamiliar dogs in a dog park.

INTRODUCTION: The aim of this study was to explore spontaneous social interactions between dyads of unfamiliar adult dogs. Although intraspecific encounters are frequent events in the life of pet dogs, the factors that might influence encounters, such as sex, dyad composition, reproductive status, age, and state of cohabitation (keeping the dogs singly or in groups), remained unexplored. METHODS: In this study, we assigned unfamiliar, non-aggressive dogs to three types of dyads defined by sex and size. We observed their unrestrained, spontaneous behaviors in an unfamiliar dog park, where only the two dogs, the owners, and experimenter were present. RESULTS: We found that the dogs, on average, spent only 17% of the time (less than 1 min) in proximity. Sex, dyad composition, reproductive status, and age influenced different aspects of the interactions in dyads. Female dogs were more likely to initiate the first contact in their dyad but later approached the partner less frequently, were less likely to move apart, and displayed less scent marking. Following and moving apart were more frequent in male-male interactions. Neutered dogs spent more time following the other dog and sniffed other dogs more frequently. The time companion dogs spent in proximity and number of approaches decreased with age. CONCLUSION: The study provides guidance for dog owners about the outcomes of intraspecific encounters based on the dog's age, sex, and reproductive status, as well as the sex of the interacting partner.

Sex, skull length, breed, and age predict how dogs look at faces of humans and conspecifics.

The gaze of other dogs and humans is informative for dogs, but it has not been explored which factors predict face-directed attention. We used image presentations of unfamiliar human and dog heads, facing the observer (portrait) or facing away (profile), and measured looking time responses. We expected dog portraits to be aversive, human portraits to attract interest, and tested dogs of different sex, skull length and breed function, which in previous work had predicted human-directed attention. Dog portraits attracted longer looking times than human profiles. Mesocephalic dogs looked at portraits longer than at profiles, independent of the species in the image. Overall, brachycephalic dogs and dogs of unspecified breed function (such as mixed breeds) displayed the longest looking times. Among the latter, females observed the images for longer than males, which is in line with human findings on sex differences in processing faces. In a subsequent experiment, we tested whether dog portraits functioned as threatening stimuli. We hypothesized that dogs will avoid food rewards or approach them more slowly in the presence of a dog portrait, but found no effect of image type. In general, older dogs took longer to approach food placed in front of the images and mesocephalic dogs were faster than dogs of other skull length types. The results suggest that short-headed dogs are more attentive to faces, while sex and breed function predict looking times through complex interactions.

Author Correction: EEG Transients in the Sigma Range During non-REM Sleep Predict Learning in Dogs.

A correction to this article has been published and is linked from the HTML and PDF versions of this paper. The error has not been fixed in the paper.

EEG Transients in the Sigma Range During non-REM Sleep Predict Learning in Dogs.

Sleep spindles are phasic bursts of thalamo-cortical activity, visible in the cortex as transient oscillations in the sigma range (usually defined in humans as 12-14 or 9-16 Hz). They have been associated with sleep-dependent memory consolidation and sleep stability in humans and rodents. Occurrence, frequency, amplitude and duration of sleep spindles co-vary with age, sex and psychiatric conditions. Spindle analogue activity in dogs has been qualitatively described, but never quantified and related to function. In the present study we used an adjusted version of a detection method previously validated in children to test whether detections in the dogs show equivalent functional correlates as described in the human literature. We found that the density of EEG transients in the 9-16 Hz range during non-REM sleep relates to memory and is characterized by sexual dimorphism similarly as in humans. The number of transients/minute was larger in the learning condition and for female dogs, and correlated with the increase of performance during recall. It can be concluded that in dogs, automatic detections in the 9-16 Hz range, in particular the slow variant (<13 Hz), are functional analogues of human spindles.