Correction: Personality traits in companion dogs-Results from the VIDOPET.

[This corrects the article DOI: 10.1371/journal.pone.0195448.].

Personality traits in companion dogs-Results from the VIDOPET.

Individual behavioural differences in pet dogs are of great interest from a basic and applied research perspective. Most existing dog personality tests have specific (practical) goals in mind and so focused only on a limited aspect of dogs' personality, such as identifying problematic (aggressive or fearful) behaviours, assessing suitability as working dogs, or improving the results of adoption. Here we aimed to create a comprehensive test of personality in pet dogs that goes beyond traditional practical evaluations by exposing pet dogs to a range of situations they might encounter in everyday life. The Vienna Dog Personality Test (VIDOPET) consists of 15 subtests and was performed on 217 pet dogs. A two-step data reduction procedure (principal component analysis on each subtest followed by an exploratory factor analysis on the subtest components) yielded five factors: Sociability-obedience, Activity-independence, Novelty seeking, Problem orientation, and Frustration tolerance. A comprehensive evaluation of reliability and validity measures demonstrated excellent inter- and intra-observer reliability and adequate internal consistency of all factors. Moreover the test showed good temporal consistency when re-testing a subsample of dogs after an average of 3.8 years-a considerably longer test-retest interval than assessed for any other dog personality test, to our knowledge. The construct validity of the test was investigated by analysing the correlations between the results of video coding and video rating methods and the owners' assessment via a dog personality questionnaire. The results demonstrated good convergent as well as discriminant validity. To conclude, the VIDOPET is not only a highly reliable and valid tool for measuring dog personality, but also the first test to show consistent behavioural traits related to problem solving ability and frustration tolerance in pet dogs.

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.

The Processing of Human Emotional Faces by Pet and Lab Dogs: Evidence for Lateralization and Experience Effects.

From all non-human animals dogs are very likely the best decoders of human behavior. In addition to a high sensitivity to human attentive status and to ostensive cues, they are able to distinguish between individual human faces and even between human facial expressions. However, so far little is known about how they process human faces and to what extent this is influenced by experience. Here we present an eye-tracking study with dogs emanating from two different living environments and varying experience with humans: pet and lab dogs. The dogs were shown pictures of familiar and unfamiliar human faces expressing four different emotions. The results, extracted from several different eye-tracking measurements, revealed pronounced differences in the face processing of pet and lab dogs, thus indicating an influence of the amount of exposure to humans. In addition, there was some evidence for the influences of both, the familiarity and the emotional expression of the face, and strong evidence for a left gaze bias. These findings, together with recent evidence for the dog's ability to discriminate human facial expressions, indicate that dogs are sensitive to some emotions expressed in human faces.

Inhibitory Control, but Not Prolonged Object-Related Experience Appears to Affect Physical Problem-Solving Performance of Pet Dogs.

Human infants develop an understanding of their physical environment through playful interactions with objects. Similar processes may influence also the performance of non-human animals in physical problem-solving tasks, but to date there is little empirical data to evaluate this hypothesis. In addition or alternatively to prior experiences, inhibitory control has been suggested as a factor underlying the considerable individual differences in performance reported for many species. Here we report a study in which we manipulated the extent of object-related experience for a cohort of dogs (Canis familiaris) of the breed Border Collie over a period of 18 months, and assessed their level of inhibitory control, prior to testing them in a series of four physical problem-solving tasks. We found no evidence that differences in object-related experience explain variability in performance in these tasks. It thus appears that dogs do not transfer knowledge about physical rules from one physical problem-solving task to another, but rather approach each task as a novel problem. Our results, however, suggest that individual performance in these tasks is influenced in a complex way by the subject's level of inhibitory control. Depending on the task, inhibitory control had a positive or a negative effect on performance and different aspects of inhibitory control turned out to be the best predictors of individual performance in the different tasks. Therefore, studying the interplay between inhibitory control and problem-solving performance will make an important contribution to our understanding of individual and species differences in physical problem-solving performance.

Aging effects on discrimination learning, logical reasoning and memory in pet dogs.

In laboratory dogs, aging leads to a decline in various cognitive domains such as learning, memory and behavioural flexibility. However, much less is known about aging in pet dogs, i.e. dogs that are exposed to different home environments by their caregivers. We used tasks on a touchscreen apparatus to detect differences in various cognitive functions across pet Border Collies aged from 5 months to 13 years. Ninety-five dogs were divided into five age groups and tested in four tasks: (1) underwater photo versus drawing discrimination, (2) clip art picture discrimination, (3) inferential reasoning by exclusion and (4) a memory test with a retention interval of 6 months. The tasks were designed to test three cognitive abilities: visual discrimination learning, logical reasoning and memory. The total number of sessions to reach criterion and the number of correction trials needed in the two discrimination tasks were compared across age groups. The results showed that both measures increased linearly with age, with dogs aged over 13 years displaying slower learning and reduced flexibility in comparison to younger dogs. Inferential reasoning ability increased with age, but less than 10 % of dogs showed patterns of choice consistent with inference by exclusion. No age effect was found in the long-term memory test. In conclusion, the discrimination learning tests used are suitable to detect cognitive aging in pet dogs, which can serve as a basis for comparison to help diagnose cognition-related problems and as a tool to assist with the development of treatments to delay cognitive decline.

Training for eye contact modulates gaze following in dogs.

Following human gaze in dogs and human infants can be considered a socially facilitated orientation response, which in object choice tasks is modulated by human-given ostensive cues. Despite their similarities to human infants, and extensive skills in reading human cues in foraging contexts, no evidence that dogs follow gaze into distant space has been found. We re-examined this question, and additionally whether dogs' propensity to follow gaze was affected by age and/or training to pay attention to humans. We tested a cross-sectional sample of 145 border collies aged 6 months to 14 years with different amounts of training over their lives. The dogs' gaze-following response in test and control conditions before and after training for initiating eye contact with the experimenter was compared with that of a second group of 13 border collies trained to touch a ball with their paw. Our results provide the first evidence that dogs can follow human gaze into distant space. Although we found no age effect on gaze following, the youngest and oldest age groups were more distractible, which resulted in a higher number of looks in the test and control conditions. Extensive lifelong formal training as well as short-term training for eye contact decreased dogs' tendency to follow gaze and increased their duration of gaze to the face. The reduction in gaze following after training for eye contact cannot be explained by fatigue or short-term habituation, as in the second group gaze following increased after a different training of the same length. Training for eye contact created a competing tendency to fixate the face, which prevented the dogs from following the directional cues. We conclude that following human gaze into distant space in dogs is modulated by training, which may explain why dogs perform poorly in comparison to other species in this task.

Dogs can discriminate emotional expressions of human faces.

The question of whether animals have emotions and respond to the emotional expressions of others has become a focus of research in the last decade [1-9]. However, to date, no study has convincingly shown that animals discriminate between emotional expressions of heterospecifics, excluding the possibility that they respond to simple cues. Here, we show that dogs use the emotion of a heterospecific as a discriminative cue. After learning to discriminate between happy and angry human faces in 15 picture pairs, whereby for one group only the upper halves of the faces were shown and for the other group only the lower halves of the faces were shown, dogs were tested with four types of probe trials: (1) the same half of the faces as in the training but of novel faces, (2) the other half of the faces used in training, (3) the other half of novel faces, and (4) the left half of the faces used in training. We found that dogs for which the happy faces were rewarded learned the discrimination more quickly than dogs for which the angry faces were rewarded. This would be predicted if the dogs recognized an angry face as an aversive stimulus. Furthermore, the dogs performed significantly above chance level in all four probe conditions and thus transferred the training contingency to novel stimuli that shared with the training set only the emotional expression as a distinguishing feature. We conclude that the dogs used their memories of real emotional human faces to accomplish the discrimination task.

Dogs learn to solve the support problem based on perceptual cues.

Numerous recent studies have investigated how animals solve means-end tasks and unraveled considerable variation in strategies used by different species. Domestic dogs (Canis familiaris) have typically performed comparably poorly in physical cognition tasks, but a recent study showed that they can solve the on-off condition of the support problem, where they are confronted with two boards, one with a reward placed on it and the other with a reward placed next to it. To explore which strategies dogs use to solve this task, we first tested 37 dogs with the on-off condition tested previously and then tested subjects that passed this condition with three transfer tasks. For the contact condition, the inaccessible reward was touching the second board. For the perceptual containment condition, the inaccessible reward was surrounded on three sides by the second board, but not supported by it, whereas for the gap condition, discontinuous boards were used. Unlike in the previous study, our subjects did not perform above chance level in the initial trials of the on-off condition, but 13 subjects learned to solve it. Their performance in the transfer tasks suggests that dogs can learn to solve the support problem based on perceptual cues, that they can quickly adopt new cues when old ones become unreliable, but also that some apparently inherent preferences are hard to overcome. Our study contributes to accumulating evidence demonstrating that animals typically rely on a variety of perceptual cues to solve physical cognition tasks, without developing an understanding of the underlying causal structure.

The use of a displacement device negatively affects the performance of dogs (Canis familiaris) in visible object displacement tasks.

Visible and invisible displacement tasks have been used widely for comparative studies of animals' understanding of object permanence, with evidence accumulating that some species can solve invisible displacement tasks and, thus, reach Piagetian stage 6 of object permanence. In contrast, dogs appear to rely on associative cues, such as the location of the displacement device, during invisible displacement tasks. It remains unclear, however, whether dogs, and other species that failed in invisible displacement tasks, do so because of their inability to form a mental representation of the target object, or simply because of the involvement of a more salient but potentially misleading associative cue, the displacement device. Here we show that the use of a displacement device impairs the performance of dogs also in visible displacement tasks: their search accuracy was significantly lower when a visible displacement was performed with a displacement device, and only two of initially 42 dogs passed the sham-baiting control conditions. The negative influence of the displacement device in visible displacement tasks may be explained by strong associative cues overriding explicit information about the target object's location, reminiscent of an overshadowing effect, and/or object individuation errors as the target object is placed within the displacement device and moves along a spatiotemporally identical trajectory. Our data suggest that a comprehensive appraisal of a species' performance in object permanence tasks should include visible displacement tasks with the same displacement device used in invisible displacements, which typically has not been done in the past.

Lifespan development of attentiveness in domestic dogs: drawing parallels with humans.

Attention is pivotal to consciousness, perception, cognition, and working memory in all mammals, and therefore changes in attention over the lifespan are likely to influence development and aging of all of these functions. Due to their evolutionary and developmental history, the dog is being recognized as an important species for modeling human healthspan, aging and associated diseases. In this study, we investigated the normal lifespan development of attentiveness of pet dogs in naturalistic situations, and compared the resulting cross-sectional developmental trajectories with data from previous studies in humans. We tested a sample of 145 Border collies (6 months to 14 years) with humans and objects or food as attention attractors, in order to assess their attentional capture, sustained and selective attention, and sensorimotor abilities. Our results reveal differences in task relevance in sustained attentional performance when watching a human or a moving object, which may be explained by life-long learning processes involving such stimuli. During task switching we found that dogs' selective attention and sensorimotor abilities showed differences between age groups, with performance peaking at middle age. Dogs' sensorimotor abilities showed a quadratic distribution with age and were correlated with selective attention performance. Our results support the hypothesis that the development and senescence of sensorimotor and attentional control may be fundamentally interrelated. Additionally, attentional capture, sustained attention, and sensorimotor control developmental trajectories paralleled those found in humans. Given that the development of attention is similar across humans and dogs, we propose that the same regulatory mechanisms are likely to be present in both species. Finally, this cross-sectional study provides the first description of age group changes in attention over the lifespan of pet dogs.

Dogs' use of the solidity principle: revisited.

A wealth of comparative data has been accumulated over the past decades on how animals acquire and use information about the physical world. Domestic dogs have typically performed comparably poorly in physical cognition tasks, though in a recent study Kundey et al. (Anim Cogn 13:497-505, 2010) challenged this view and concluded that dogs understand that objects cannot pass through solid barriers. However, the eight subjects in the study of Kundey et al. may have solved the task with the help of perceptual cues, which had not been controlled for. Here, we tested dogs with a similar task that excluded these cues. In addition, unlike the set-up of Kundey et al., our set-up allowed the subjects to observe the effect of the solid barrier. Nevertheless, all 28 subjects failed to solve this task spontaneously and showed no evidence of learning across 50 trials. Our results therefore call into question the earlier suggestion that dogs have, or can acquire, an understanding of the solidity principle.

Brief owner absence does not induce negative judgement bias in pet dogs.

Humans in a negative emotional state are more likely to judge ambiguous stimuli as negative. In recent years, similar judgement biases have been found in some non-human animals that were exposed to long-term or short-term treatments aimed at influencing their affective states. Here we tested pet dogs in the presence and absence of their owners in a judgement bias test with an established go/no-go procedure. Even though owner absence is thought to induce a state of anxiety in dogs that have formed an attachment bond with their primary caretakers, we found no difference between the dogs' responses to ambiguous stimuli in the presence or absence of their owners. This result may be explained by the absence of anxiety in dogs that are accustomed to brief periods of separation from their owners, or by a sensitivity limit of the customary judgement bias tests in non-human animals when only a moderate, short-term state of anxiety is induced. In addition, we found significant differences between individuals and populations in the responses to ambiguous stimuli, which give impetus for further research.

Female but not male dogs respond to a size constancy violation.

Differences between sexes in cognitive processes are widespread in humans and permeate many, if not most, cognitive domains. In animal cognition research, however, possible sex differences are still often neglected. Here, we provide striking evidence for a sex-specific response in an object permanence task in domestic dogs (Canis familiaris). Female dogs responded with significantly increased looking times to a violation of expectancy--a ball 'magically' changing size while temporarily occluded. By contrast, male dogs, irrespective of their neuter status, did not respond to the size constancy violation. These results indicate that sex differences in basic cognitive processes may extend to mammals in general, and call for increased consideration of possible sex effects when analysing and interpreting data in animal cognition.

Imitation and traditions in wild banded mongooses.

Evidence has accumulated in recent years indicating that traditions are not a unique feature of human societies but may be common in primates and some other mammals. However, most documented cases remain contentious because observational studies of free-living animals suffer from interpretive weaknesses, whereas social diffusion experiments performed in captivity may not reflect conditions found in nature. Here we use experiments under natural conditions to demonstrate that wild banded mongooses (Mungos mungo) pass preferences for one of two possible foraging techniques on to the next generation through contextual imitation. Notably, both techniques coexisted within the same groups and were transmitted concurrently between adults and pups, which form close one-to-one associations during the period of pup dependency. This experimental demonstration of a foraging tradition in wild mammals provides critical evidence to support previous accounts of traditions in nonhuman animals based on distribution patterns of natural behaviors. Moreover, our data provide the first experimental demonstration of imitation in wild mammals and, contrary to common assumption, show that social learning need not lead to an increased behavioral homogeneity within groups.

Do anvil-using banded mongooses understand means-end relationships? A field experiment.

Tool use and the associated need to choose appropriate objects for a particular task are thought to have selected for specialized cognitive abilities such as means-end comprehension. Several studies on large-brained tool-using primates and birds have demonstrated understanding of causal relationships to some extent. However, a comprehensive appraisal of this hypothesis requires testing for means-end comprehension also in non-tool-users as well as in small-brained tool users. Moreover, the results of captive studies do not answer the question whether such cognitive abilities are relevant to an animal in its natural environment. Here I presented wild banded mongooses Mungos mungo, small-brained carnivores that regularly use anvils to open food items with a hard shell, with a transfer test involving novel anvil objects. I found no evidence for means-end comprehension or a heuristic strategy used for anvil choice in this species. Instead, recognition of suitable anvils appears to be learned by trial and error separately for different categories of anvils. These data suggest that, at least for the anvil-choice task investigated here, the need to choose suitable objects has not selected for specialized cognitive abilities in banded mongooses, a finding that may extend to a large range of proto-tool users. Furthermore, this study adds to growing evidence that animals subjected to the selection pressures and trade-offs of their natural environment may get by with cognitively more simple strategies than sometimes suggested by captive studies or plausibility arguments.

'Nasty neighbours' rather than 'dear enemies' in a social carnivore.

Territorial animals typically respond less aggressively to neighbours than to strangers. This 'dear enemy effect' has been explained by differing familiarity or by different threat levels posed by neighbours and strangers. In most species, both the familiarity and the threat-level hypotheses predict a stronger response to strangers than to neighbours. In contrast, the threat-level hypothesis predicts a stronger response to neighbours than to strangers in species with intense competition between neighbours and with residents outnumbering strangers, as commonly found in social mammals such as the banded mongoose (Mungos mungo). The familiarity hypothesis predicts reduced aggression towards neighbours also in these species. We exposed free-living banded mongoose groups to translocated scent marks of neighbouring groups and strangers. Groups vocalized more and inspected more samples in response to olfactory cues of the neighbours than to the strangers. Our results support the threat-level hypothesis and contradict the familiarity hypothesis. We suggest that increased aggression towards neighbours is more common in social species with intense competition between neighbours, as opposed to reduced aggression towards neighbours typical for most solitary species.

Hypoxia-induced downregulation of beta-adrenergic receptors in rat heart.

To test the desensitization hypothesis of cardiac beta-adrenergic receptors (beta-AR) in chronic hypoxia, the effect of 1, 3, 7, 15, and 21 days of exposure to hypobaric hypoxia (380 Torr) was evaluated in Wistar rats. Exposure to hypoxia for 1-15 days did not induce any change in right and left ventricular beta-AR density (Bmax) determined with [125I]iodocyanopindolol or in antagonist affinity. After 21 days, Bmax decreased by 24% in the left ventricle. In contrast, no change in beta-AR was shown in the right hypertrophied ventricle. Agonist affinity in the left ventricle was not altered, as shown by the analysis of displacement curves of isoproterenol (normoxia 185 +/- 26 nM, hypoxia 170 +/- 11 nM). Moreover, there was no significant decrease in adenylate cyclase activity (pmol.mg-1.min-1) in the left ventricle. In the right ventricle, a 21-day exposure to hypoxia led to a decrease in basal and maximal activity when stimulated by isoproterenol. A decrease in tissue norepinephrine content was observed after 7 days of hypoxia. In conclusion, these data support the beta-AR downregulation hypothesis as one of the mechanisms of myocardial adaptation to high altitude occurring after 2-3 wk of exposure to hypoxia. The regulation pathways of beta-AR may differ between left nonhypertrophied and right hypertrophied ventricles. No evidence of profound abnormality of signal transduction was shown.

Species differences in myocardial beta-adrenergic receptor regulation in response to hyperthyroidism.

The coupling between myocardial beta-adrenergic receptors, adenylate cyclase activity, and the in vivo cardiac response to catecholamines is controversial in hyperthyroidism. The possibility of species differences in beta-adrenoceptor regulation after thyroxine treatment was studied in dogs and in rats. In dogs instrumented with a left ventricular (LV) pressure micromanometer, hyperthyroidism was induced by L-thyroxine (0.5 mg/kg/day i.v. for 10 days). After hyperthyroidism, heart rate was increased to 167 +/- 10 beats/min (control, 107 +/- 8 beats/min; p less than 0.005) with an increase of peak LV dP/dt from 4,243 +/- 471 to 6,105 +/- 862 mm Hg/sec (p less than 0.01). LV response to injection of increasing doses of isoproterenol and dobutamine was not significantly different before and after induction of the hyperthyroid state, as shown by the unchanged slopes of the LV peak dP/dt versus the log of the dose of isoproterenol and dobutamine. Bmax of beta-receptors measured in crude membranes using 3H-CGP 12177 and in homogenates using 125I-cyanopindolol was not increased in hyperthyroid animals as compared with a control group. Basal adenylate cyclase activity was not different in control and hyperthyroid dogs (32 +/- 3 versus 29 +/- 3 pmol/mg/min), and maximal adenylate cyclase activity response to isoproterenol was similar in control and hyperthyroid dogs. In contrast, in rats subjected to hyperthyroidism (0.5 mg/kg/day i.p. L-thyroxine for 10 days), Bmax of adrenoceptors measured using the same methods was significantly increased as compared with control (+72.5% using 3H-CGP 12177 and +41% using 125I-cyanopindolol, but adenylate cyclase activity was not increased in hyperthyroid rats. We conclude that both adenylate cyclase activity and LV response to catecholamines are not increased by thyroxine-induced hyperthyroidism in dogs and that, in contrast with rats, beta-adrenergic density is not increased in hyperthyroid dogs. This indicates a species difference in myocardial beta-adrenoceptor regulation in response to hyperthyroidism.

Beta-adrenoceptors and adenylate cyclase activity in hypertrophied and failing rabbit left ventricle.

Beta-adrenoceptor density and affinity, studied by H3-CGP 12177 binding, and adenylate cyclase activity were measured in 12 left ventricles of rabbits with heart failure and compared to 13 left ventricles of control (C) rabbits. Heart failure (HF) was induced by a double volume (aortic insufficiency) plus pressure (aortic stenosis 14 days later) overload. Left ventricular mass was increased in HF by 67% above C. Saturation curves with CGP 12177 showed a 36% decrease in beta-adrenoceptor density (C = 61.5 +/- 5.4 fmol/mg prot., P less than 0.05) but competition curves with isoproterenol were not different in HF and C. Basal and Gpp(NH)p stimulated adenylate cyclase activity were decreased by 36% and 22% respectively in rabbits with heart failure as compared with control animals and cAMP production was significantly smaller in failing left ventricles than in control left ventricles both after NaF stimulation (C: 161.3 +/- 24.9 pmols/mg/min; HF: 98.8 +/- 7.0 pmols/mg/min; P less than 0.05) and even more after forskolin stimulation (C: 159.1 +/- 23.9 and HF: 60.8 +/- 7.3 pmols/mg/min; P less than 0.01). Although isoproterenol stimulated ACA was smaller in HF than in C, EC50 was similar in both groups (1.6 x 10(-7) M). We conclude that in the early stage of heart failure in the rabbit, although adrenoceptor density is decreased, there are no changes of affinity of beta-adrenoceptors for isoproterenol and the major alteration of cAMP production appears to lie down-stream the receptor level with a markedly impaired stimulation of adenylate cyclase activity by forskolin.