Theses: Novel scientific achievements

I. Demography and health

1) The prevalence of age-related cognitive decline in companion dogs across the entire adult lifespan (Chapter 7)

We tested the internal consistency of the most widely used cognitive dysfunction questionnaire’s domains. We found that five out its eight scales have not shown reliable internal consistency in a Hungarian sample. This warrants caution when the diagnosis is based on the number of signs shown within a domain. The result prompted us to create a short, seven-items scale with high internal consistency assessing cognitive decline based on the items’ positive correlation with relative age. With this survey we found that signs of cognitive decline were already detectable in dogs at 50-75% of the expected lifespan, independently from the weight and size of the dog, indicating that large dogs age faster. Visual, auditory and olfactory impairments all resulted in significantly higher occurrence of cognitive decline associated behaviours, suggesting that it is crucial to collect information about the sensory functions of aged dogs when evaluating cognitive decline with online questionnaires or behavioural tests.

Participating in dog training had beneficial effects on cognitive aging suggesting cognitive reserve or altered aging curve in trained dogs.

2) Demographics of companion dogs across age groups and identifying the key variables associated with health status (Chapter 8)

Dogs go through similar stages of development as humans, however, many owners do not consider their dog’s life stage when e.g. selecting a diet. We examine the link between the age and health of the dog, and owner and dog demographics in a cross-sectional sample. The oldest age group (>12 years old) was classified by owners more frequently as unhealthy, less often have a “normal” body condition score. There were more male and neutered dogs among them, received less activity/interaction/training with the owner, and were more likely to have experienced one or more traumatic events such as spending time in a shelter, changing owners, prolonged disease. Purebred dogs suffered from health problems at a younger age and died at an earlier age than mixed breeds. The youngest age group was more often fed raw meat (e.g. BARF), and had owners aged under 29 years, reflecting new trends. Our results partially contradict our prediction that dogs that are heavier in weight are more likely to suffer from health problems. However, they implicate a new factor, which has an impact on health regardless of breed and age, that of experiencing traumatic events during the lifespan.

The prevalence of dogs that had experienced one or more traumatic events in their

14 For the hypotheses see Chapter 5.

lifetime was high (over 40% of the sample). Our results corroborate previous research indicating that age is the strongest predictor of health status regardless of breed, height and weight, as it is in humans.

II. Cognition, emotion and face processing

3) Developing a behaviour test for assessing discrimination and reversal learning (Chapter 9)

This study aimed to develop a reversal learning task that could detect age-related changes in the learning abilities of family dogs in a short time-frame (about 1 hour).

We have met this goal, as both the reversal learning and the preceding discrimination learning tasks detected age differences, old dogs learned significantly slower than young dogs. In the reversal learning, training based on the location of stimuli was easier for the dogs than training based on the size, shape, colour of stimuli. In the latter condition, we observed a ceiling effect, as most old dogs did not learn the task in 50 trials. Therefore, we suggest that training based on objects’ location is more informative for reversal learning tasks. Overall, these results suggest that our discrimination learning and reversal learning tasks could successfully be used to investigate differences in spatial function between young and old dogs. This test has the potential for clinical state examinations, which are widely used among human clinicians but currently nonexistent in veterinary praxises.

4) Positivity effect in dogs: do old dogs experience less negative emotions? (Chapter 10)

Older people experience fewer negative emotions as their attention shifts from negative stimuli due to age-related changes in the brain, which is known as the “positivity effect”. We found that compared to young dogs, old individuals reacted slower only to the negative sounds, suggesting that an age-related positivity effect is present in dogs, similarly to humans. There was no significant difference in the latency to recover between groups. Similarities in emotional processing between humans and dogs may imply analogous changes in subcortical emotional processing in the canine brain during aging. Studying age-related differences in the processing of emotional stimuli in animals gives us more insight into the biological changes of the aging brain, affecting how older individuals perceive and process their social environment.

5) Age-related effects in looking at faces of humans and conspecifics (Chapter 11) Responsiveness to faces changes with age, either through change in perceptual processes or age-related differences in processing social stimuli. We found that independent from age, dog portraits attracted longer looking times than human profiles and short-headed dogs were more attentive to faces. In a subsequent experiment older dogs took longer to approach food placed in front of the images, due to changes in facial perception or due to a decline in sensorimotor functions, and mesocephalic dogs were

faster than dogs of other skull length types. Because dogs, at least in some contexts, rely on our faces to understand our behaviours and intentions it is important to consider for the refinement of dog-human communication, training, and welfare, how the animal’s age and other characteristics impact facial perception. Moreover, a comparison between humans and dogs might uncover previously unforeseen factors regarding age-related changes in orientation to socially relevant visual cues and explain socially inappropriate behaviour in the elderly.

III. Personality and intraspecific relationships

6) Age-related changes in human-based personality traits and associations with owner and dog demographics (Chapter 12)

Human personality traits change across the lifespan, and that significant life events and educational experiences can influence personality traits. People tend to show increased self-confidence, warmth, self-control, and emotional stability with age. We found on a large sample with more than 10,000 individuals that older dogs were calmer, less trainable, less social, and less bold than younger dogs. These traits are analogous to the human traits Emotional Stability, Openness/Intellect, Agreeableness, Extraversion.

Other variables, including the dog’s sex and neutered status, owner’s gender, age, education, previous experience with dogs, the number of people and dogs in the household, and purpose of keeping the dogs also had detectable effects on the traits.

7) Interventions to increase play and training motivation may alleviate the negative effects of aging (Chapter 13)

Inconsistencies about the canine personality traits may be due to the different methods were used to obtain the trait scores. The Dog Personality Questionnaire has been shown to demonstrate reliability and validity, therefore it is a suitable means for investigating the replicability of previous results. We found that three of the five factors showed significant age effects. Activity/Excitability decreased with age. Aggressiveness towards animals showed a quadratic developmental trajectory peaking in dogs aged 6 to 10 years. Whilst Responsiveness to training also decreased, only dogs older than 12 years differed significantly from the other groups. When the models were re-run including the other explanatory variables, the age group was no longer significant for this trait. The amount of time spent interacting/playing with the owner partially mediated the relationship between age and Responsiveness to training, implying that interventions to increase play and training motivation may alleviate the negative effects of aging on dogs’ trainability.

8) The relationship between age, personality, dominance and leadership in a group of dogs (Chapter 14)

We obtained high-resolution spatio-temporal GPS trajectory data (823,148 data points) from six dogs belonging to the same household and their owner during fourteen, 30-40 min unleashed walks. A directional correlation analysis quantified interactions between

pairs of dogs that run loops jointly. We found that dogs play the role of the leader about 50-85% of the time, i.e. the leader and follower roles in a given pair are dynamically interchangeable. However, on a longer timescale, tendencies to lead differ consistently.

The network constructed from these loose leader-follower relations is hierarchical.

According to our results, the collective motion of a dog group is influenced by age and the underlying hierarchical social network. Leader/dominant dogs are older, more trainable, controllable, and aggressive than follower/subordinate dogs. Leader dogs exert a disproportionate influence on the decisions about running away and turning back to the owner during walks. Findings could pave the way for automated animal personality and human social interaction measurements.

9) Chapter 15. Dominance status and age in companion dogs sharing the same household

We examined how owners perceive dominance in dogs, and what different behaviours and personality types are used to describe dominant and subordinate individuals with a questionnaire study. According to the owners, dogs rated as dominant (87%) have priority access to resources (resting place, food, and rewards), undertake certain tasks (defend and lead the group, bark more), display dominance (win fights, and mark over the other’s urine, the other dog licks their mouth), share certain personality traits (smarter, more aggressive and impulsive), and are older than their partner dog. In 66%

of the dog dyads, the older individual was dominant. The newly developed questionnaire is more reliable in assessing dominance than previous attempts, therefore a useful mean for assessing age-related changes in social ranks.

IV. Steps towards understanding the mechanisms of aging

10) Age related differences in the spindling activity of the sleeping brain (Chapter 16) The dog brain is still relatively unknown compared to the brains of other model animals such as rodents. We found a different course of aging in the fast and slow canine sleep spindles (brief trains of rhythmic activity, 0.5-6 seconds long, 9-16 Hz, which appear in the EEG signal of humans and other mammals during non-REM sleep). Slow and central spindles follow human-like aging trends. Frontal fast spindles continue to increase in density with age, which seems to be unique to dogs, although human adolescent development is also characterized by increased density. Our findings support the argument that sigma bursts in the canine non-REM sleep are analogous to human sleep spindles and suggest that in dogs, slow and fast spindles display different trajectories related to age.

11) The genetic background of longevity based on whole-genome sequence data of two methuselah dogs (Chapter 17)

We identified more than 7500 novel SNP mutations in two methuselah dogs (with a lifespan of 22 and 27 years) when compared to three publicly available canine databases

with SNP information from 850 dogs. Based on in silico analysis, we identified 670 missense mutations across 472 genes and several genetic pathways that are primary candidates for age-related research in dogs (and their homologs in humans) in future studies. Based on their gene ontologies, these genes were related – among others – to immune response and the nervous system in general. A link between extreme longevity and the regulation of gene transcription/translation suggests that one crucial genetic requirement of extreme longevity lies within the fine-tuning – i.e. the superior calibration – of RNA (and thereof protein) production of an organism. This phenomenon defines an interesting direction for future research aiming to better understand longevity.