Publications by authors named "Eniko Kubinyi"

62 Publications

Variants That Differentiate Wolf and Dog Populations Are Enriched in Regulatory Elements.

Genome Biol Evol 2021 Apr;13(4)

KTH Royal Institute of Technology, School of Chemistry, Biotechnology and Health, Science for Life Laboratory, Stockholm, Sweden.

Research on the genetics of domestication most often focuses on the protein-coding exons. However, exons cover only a minor part (1-2%) of the canine genome, whereas functional mutations may be located also in regions beyond the exome, in regulatory regions. Therefore, a large proportion of phenotypical differences between dogs and wolves may remain genetically unexplained. In this study, we identified variants that have high allelic frequency differences (i.e., highly differentiated variants) between wolves and dogs across the canine genome and investigated the potential functionality. We found that the enrichment of highly differentiated variants was substantially higher in promoters than in exons and that such variants were enriched also in enhancers. Several enriched pathways were identified including oxytocin signaling, carbohydrate digestion and absorption, cancer risk, and facial and body features, many of which reflect phenotypes of potential importance during domestication, including phenotypes of the domestication syndrome. The results highlight the importance of regulatory mutations during dog domestication and motivate the functional annotation of the noncoding part of the canine genome.
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http://dx.doi.org/10.1093/gbe/evab076DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8086526PMC
April 2021

Shorter headed dogs, visually cooperative breeds, younger and playful dogs form eye contact faster with an unfamiliar human.

Sci Rep 2021 Apr 29;11(1):9293. Epub 2021 Apr 29.

Senior Family Dog Project, Department of Ethology, Eötvös Loránd University, Budapest, Hungary.

Forming eye contact is important in dog-human communication. In this study we measured what factors affect dogs' propensity for forming eye contact with an experimenter. We investigated the effect of [1] cephalic index (head shape's metric, indicator of higher visual acuity at the centre of the visual field), [2] breed function (visual cooperativeness), [3] age and [4] playfulness with strangers in 125 companion dogs. Cephalic index was measured individually and analysed as a continuous variable. Results showed that [1] dogs with a higher cephalic index (shorter head) established eye contact faster. Since cephalic index is highly variable even within a breed, using artificial head shape groups or breed average cephalic index values is not recommended. [2] Breed function also affected dogs' performance: cooperative breeds and mongrels established eye contact faster than dogs from non-cooperative breeds. [3] Younger dogs formed eye contact faster than older ones. [4] More playful dogs formed eye contact faster. Our results suggest that several factors affect dogs' interspecific attention, and therefore their visual communication ability.
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http://dx.doi.org/10.1038/s41598-021-88702-wDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8084920PMC
April 2021

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

Sci Rep 2021 Feb 24;11(1):4468. Epub 2021 Feb 24.

Department of Ethology, Eötvös Loránd University, Budapest, Hungary.

During social interactions, acoustic parameters of tetrapods' vocalisations reflect the emotional state of the caller. Higher levels of spectral noise and the occurrence of irregularities (non-linear phenomena NLP) might be negative arousal indicators in alarm calls, although less is known about other distress vocalisations. Family dogs experience different levels of stress during separation from their owner and may vocalise extensively. Analysing their whines can provide evidence for the relationship between arousal and NLP. We recorded 167 family dogs' separation behaviour including vocalisations, assessed their stress level based on behaviour and tested how these, their individual features, and owner reported separation-related problems (SRP) relate to their whines' (N = 4086) spectral noise and NLP. Dogs with SRP produced NLP whines more likely. More active dogs and dogs that tried to escape produced noisier whines. Older dogs' whines were more harmonic than younger ones', but they also showed a higher NLP ratio. Our results show that vocal harshness and NLP are associated with arousal in contact calls, and thus might function as stress indicators. The higher occurrence of NLP in older dogs irrespective to separation stress suggests loss in precise neural control of the larynx, and hence can be a potential ageing indicator.
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http://dx.doi.org/10.1038/s41598-021-83614-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7904949PMC
February 2021

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

Biol Rev Camb Philos Soc 2021 Jun 3;96(3):1021-1034. Epub 2021 Feb 3.

Department of Ethology, ELTE Eötvös Loránd University, Pázmány Péter sétány 1/C, Budapest, 1117, Hungary.

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.
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http://dx.doi.org/10.1111/brv.12688DOI Listing
June 2021

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

Sci Rep 2020 12 31;10(1):22461. Epub 2020 Dec 31.

Department of Ethology, ELTE Eötvös Loránd University, 1117, Budapest, Hungary.

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.
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http://dx.doi.org/10.1038/s41598-020-80417-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7775433PMC
December 2020

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

Front Psychol 2020 6;11:588916. Epub 2020 Nov 6.

Department of Ethology, ELTE Eötvös Loránd University, Budapest, Hungary.

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.
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http://dx.doi.org/10.3389/fpsyg.2020.588916DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7677580PMC
November 2020

Digital Endocasting in Comparative Canine Brain Morphology.

Front Vet Sci 2020 6;7:565315. Epub 2020 Oct 6.

Department of Ethology, Institute of Biology, ELTE Eötvös Loránd University, Budapest, Hungary.

Computed tomography (CT) is one of the most useful techniques for digitizing bone structures and making endocranial models from the neurocranium. The resulting digital endocasts reflect the morphology of the brain and the associated structures. Our first aim was to document the methodology behind creating detailed digital endocasts of canine skulls. We created digital endocasts of the skulls of 24 different dog breeds and 4 wild canids for visualization and teaching purposes. We used CT scanning with 0.323 mm × 0.322 mm × 0.6 mm resolution. The imaging data were segmented with 3D Slicer software and refined with Autodesk Meshmixer. Images were visualized in 3D Slicer and surface models were converted to 3D PDFs to provide easier interactive access, and 3D prints were also generated for visualization purposes. Our second aim was to analyze how skull length and width relate to the surface areas of the prepiriform rhinencephalic, prefrontal, and non-prefrontal cerebral convexity areas of the endocasts. The rhinencephalic area ratio decreased with a larger skull index. Our results open the possibility to analyze the relationship between the skull and brain morphology, and to link certain features to behavior, and cognition in dogs.
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http://dx.doi.org/10.3389/fvets.2020.565315DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7572857PMC
October 2020

Individual and group level personality change across the lifespan in dogs.

Sci Rep 2020 10 14;10(1):17276. Epub 2020 Oct 14.

Clever Dog Lab, Comparative Cognition, Messerli Research Institute, University of Veterinary Medicine, Vienna, Medical University of Vienna, and University of Vienna, Vienna, Austria.

In humans, age-related changes in personality occur in a non-random fashion with respect to their direction, timing, and magnitude. In dogs, there are still gaps in our knowledge about the detailed dynamics of age-related personality changes. We analysed the personality of 217 Border collies aged from 0.5 to 15 years both cross-sectionally and longitudinally using a test battery, to specify age periods when changes most prominently occur, assess the magnitude of changes, and analyse individual differences in personality change. We found that similar to humans, changes in personality occur unevenly during the dogs' life course, however, their dynamics seems to be specific for each trait. Activity-independence decreased mostly from puppyhood (0.5-1 years) to adolescence (> 1-2 years), then continued to decrease in a slowing rate. Novelty seeking did not change markedly until middle age (> 3-6 years), then showed a steady linear decrease. Problem orientation increased strongly until middle age then showed no marked changes in later age periods. We also revealed individual differences in personality change over time, and showed that a few individuals with potential age-related impairments significantly affected the general age trajectory of some traits. These results raise caution against the over-generalisation of global age trends in dogs.
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http://dx.doi.org/10.1038/s41598-020-74310-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7560605PMC
October 2020

Synergistic Benefits of Group Search in Rats.

Curr Biol 2020 Dec 24;30(23):4733-4738.e4. Epub 2020 Sep 24.

MTA-ELTE Statistical and Biological Physics Research Group, Hungarian Academy of Sciences, Pázmány P. stny. 1A, Budapest 1117, Hungary; Department of Biological Physics, Eötvös Loránd University, Pázmány P. stny. 1A, Budapest 1117, Hungary.

Locating unpredictable but essential resources is a task that all mobile animals have to perform in order to survive and reproduce. Research on search strategies has focused largely on independent individuals [1-3], but many organisms display collective behaviors, including during group search and foraging [4-6]. One classical experimental search task, informing studies of navigation, memory, and learning, is the location of a reward in a confined, complex maze setting [7, 8]. Rats (Rattus norvegicus) have been paradigmatic in psychological and biological studies [9, 10], but despite rats being highly social [11, 12], their group search behavior has not been investigated. Here, we explore the decision making of rats searching individually, or in groups, for a reward in a complex maze environment. Using automated video tracking, we find that rats exhibit-even when alone-a partially systematic search, leading to a continuous increase in their chance of finding the reward because of increased attraction to unexplored regions. When searching together, however, synergistic group advantages arise through integration of individual exploratory and social behavior. The superior search performances result from a strategy that represents a hierarchy of influential preferences in response to social and asocial cues. Furthermore, we present a computational model to compare the essential factors that influence how collective search operates and to validate that the collective search strategy increases the search efficiency of individuals in groups. This strategy can serve as direct inspiration for designing computational search algorithms and systems, such as autonomous robot groups, to explore areas inaccessible to humans. VIDEO ABSTRACT.
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http://dx.doi.org/10.1016/j.cub.2020.08.079DOI Listing
December 2020

The link between selection for function and human-directed play behaviour in dogs.

Biol Lett 2020 09 23;16(9):20200366. Epub 2020 Sep 23.

Institute of Ecology and Botany, Centre for Ecological Research, Vácrátót, Hungary.

Human-directed play behaviour is a distinct behavioural feature of domestic dogs. But the role that artificial selection for contemporary dog breeds has played for human-directed play behaviour remains elusive. Here, we investigate how human-directed play behaviour has evolved in relation to the selection for different functions, considering processes of shared ancestry and gene flow among the different breeds. We use the American Kennel Club (AKC) breed group categorization to reflect the major functional differences and combine this with observational data on human-directed play behaviour for over 132 breeds across 89 352 individuals from the Swedish Dog Mentality Assessment project. Our analyses demonstrate that ancestor dogs already showed intermediate levels of human-directed play behaviour, levels that are shared with several modern breed types. Herding and Sporting breeds display higher levels of human-directed play behaviour, statistically distinguishable from Non-sporting and Toy breeds. Our results suggest that human-directed play behaviour played a role in the early domestication of dogs and that subsequent artificial selection for function has been important for contemporary variation in a behavioural phenotype mediating the social bond with humans.
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http://dx.doi.org/10.1098/rsbl.2020.0366DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7532715PMC
September 2020

Longitudinal Volumetric Assessment of Ventricular Enlargement in Pet Dogs Trained for Functional Magnetic Resonance Imaging (fMRI) Studies.

Vet Sci 2020 Sep 4;7(3). Epub 2020 Sep 4.

Department of Ethology, Institute of Biology, ELTE Eötvös Loránd University, 1117 Budapest, Hungary.

Background: Recent studies suggest that clinically sound ventriculomegaly in dogs could be a preliminary form of the clinically significant hydrocephalus. We evaluated changes of ventricular volumes in awake functional magnetic resonance imaging (fMRI) trained dogs with indirectly assessed cognitive abilities over time (thus avoiding the use of anaesthetics, which can alter the pressure). Our research question was whether ventricular enlargement developing over time would have any detrimental effect on staying still while being scanned; which can be extrapolated to the ability to pay attention and to exert inhibition.

Methods: Seven healthy dogs, 2-8 years old at the baseline scan and 4 years older at rescan, participated in a rigorous and gradual training for staying motionless (<2 mm) in the magnetic resonance (MR) scanner without any sedation during 6 minute-long structural MR sequences. On T1 structural images, volumetric analyses of the lateral ventricles were completed by software guided semi-automated tissue-type segmentations performed with FMRIB Software Library (FSL, Analysis Group, Oxford, UK).

Results And Conclusion: We report significant enlargement for both ventricles (left: 47.46 %, right: 46.07 %) over time while dogs retained high levels of attention and inhibition. The results suggest that even considerable ventricular enlargement arising during normal aging does not necessarily reflect observable pathological changes in behavior.
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http://dx.doi.org/10.3390/vetsci7030127DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7558420PMC
September 2020

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

Sci Rep 2020 09 7;10(1):14678. Epub 2020 Sep 7.

Department of Ethology, ELTE Eötvös Loránd University, Pázmány Péter sétány 1/C, Budapest, 1117, Hungary.

Dogs live in 45% of households, integrated into various human groups in various societies. This is certainly not true for wolves. We suggest that dogs' increased tractability (meant as individual dogs being easier to control, handle and direct by humans, in contrast to trainability defined as performance increase due to training) makes a crucial contribution to this fundamental difference. In this study, we assessed the development of tractability in hand-raised wolves and similarly raised dogs. We combined a variety of behavioural tests: fetching, calling, obeying a sit signal, hair brushing and walking in a muzzle. Wolf (N = 16) and dog (N = 11) pups were tested repeatedly, between the ages of 3-24 weeks. In addition to hand-raised wolves and dogs, we also tested mother-raised family dogs (N = 12) for fetching and calling. Our results show that despite intensive socialization, wolves remained less tractable than dogs, especially in contexts involving access to a resource. Dogs' tractability appeared to be less context dependent, as they followed human initiation of action in more contexts than wolves. We found no evidence that different rearing conditions (i.e. intensive socialization vs. mother rearing) would affect tractability in dogs. This suggests that during domestication dogs might have been selected for increased tractability, although based on the current data we cannot exclude that the differential speed of development of dogs and wolves or the earlier relocation of wolves to live as a group explains some of the differences we found.
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http://dx.doi.org/10.1038/s41598-020-71687-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7477132PMC
September 2020

Gut Microbiome Composition is Associated with Age and Memory Performance in Pet Dogs.

Animals (Basel) 2020 Aug 24;10(9). Epub 2020 Aug 24.

Department of Microbiology, ELTE Eötvös Loránd University, 1117 Budapest, Hungary.

Gut microbiota can crucially influence behavior and neurodevelopment. Dogs show unique similarities to humans in their physiology and may naturally develop dementia-like cognitive decline. We assessed 29 pet dogs' cognitive performance in a memory test and analyzed the bacterial 16S rRNA gene from fecal samples collected right after the behavioral tests. The major phyla identified in the dog microbiomes were Bacteroidetes, Firmicutes, and Fusobacteria, each represented by >20% of the total bacterial community. Fewer Fusobacteria were found in older dogs and better memory performance was associated with a lower proportion of Actinobacteria. Our preliminary findings support the existence of links between gut microbiota, age, and cognitive performance in pet dogs.
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http://dx.doi.org/10.3390/ani10091488DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7552338PMC
August 2020

Multilevel fMRI adaptation for spoken word processing in the awake dog brain.

Sci Rep 2020 08 3;10(1):11968. Epub 2020 Aug 3.

MTA-ELTE 'Lendület' Neuroethology of Communication Research Group, Hungarian Academy of Sciences - Eötvös Loránd University, Pázmány Péter sétány 1/C, 1117, Budapest, Hungary.

Human brains process lexical meaning separately from emotional prosody of speech at higher levels of the processing hierarchy. Recently we demonstrated that dog brains can also dissociate lexical and emotional prosodic information in human spoken words. To better understand the neural dynamics of lexical processing in the dog brain, here we used an event-related design, optimized for fMRI adaptation analyses on multiple time scales. We investigated repetition effects in dogs' neural (BOLD) responses to lexically marked (praise) words and to lexically unmarked (neutral) words, in praising and neutral prosody. We identified temporally and anatomically distinct adaptation patterns. In a subcortical auditory region, we found both short- and long-term fMRI adaptation for emotional prosody, but not for lexical markedness. In multiple cortical auditory regions, we found long-term fMRI adaptation for lexically marked compared to unmarked words. This lexical adaptation showed right-hemisphere bias and was age-modulated in a near-primary auditory region and was independent of prosody in a secondary auditory region. Word representations in dogs' auditory cortex thus contain more than just the emotional prosody they are typically associated with. These findings demonstrate multilevel fMRI adaptation effects in the dog brain and are consistent with a hierarchical account of spoken word processing.
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http://dx.doi.org/10.1038/s41598-020-68821-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7398925PMC
August 2020

The molecular effect of a polymorphic microRNA binding site of Wolfram syndrome 1 gene in dogs.

BMC Genet 2020 07 28;21(1):82. Epub 2020 Jul 28.

Department of Medical Chemistry, Molecular Biology and Pathobiochemistry, Semmelweis University, Budapest, Hungary.

Background: Although the molecular function of wolframin remains unclear, the lack of this protein is known to cause stress in the endoplasmic reticulum. Some variants in the Wolfram Syndrome 1 gene (WFS1) were associated with various neuropsychiatric disorders in humans, such as aggressiveness, impulsivity and anxiety.

Results: Here we present an in silico study predicting a single nucleotide polymorphism (rs852850348) in the canine WFS1 gene which was verified by direct sequencing and was genotyped by a PCR-based technique. We found that the rs852850348 polymorphism is located in a putative microRNA (cfa-miR-8834a and cfa-miR-1838) binding site. Therefore, the molecular effect of allelic variants was studied in a luciferase reporter system that allowed assessing gene expression. We demonstrated that the variant reduced the activity of the reporter protein expression in an allele-specific manner. Additionally, we performed a behavioral experiment and investigated the association with this locus to different performance in this test. Association was found between food possessivity and the studied WFS1 gene polymorphism in the Border collie breed.

Conclusions: Based on our findings, the rs852850348 locus might contribute to the genetic risk of possessivity behavior of dogs in at least one breed and might influence the regulation of wolframin expression.
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http://dx.doi.org/10.1186/s12863-020-00879-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7390163PMC
July 2020

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

Animals (Basel) 2020 Jul 17;10(7). Epub 2020 Jul 17.

Department of Ethology, ELTE Eötvös Loránd University, 1117 Budapest, Hungary.

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.
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http://dx.doi.org/10.3390/ani10071222DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7401627PMC
July 2020

REM versus Non-REM sleep disturbance specifically affects inter-specific emotion processing in family dogs (Canis familiaris).

Sci Rep 2020 06 26;10(1):10492. Epub 2020 Jun 26.

Institute of Cognitive Neuroscience and Psychology, Research Centre for Natural Sciences, Budapest, Hungary.

Dogs have outstanding capabilities to read human emotional expressions, both vocal and facial. It has also been shown that positively versus negatively valenced dog-human social interactions substantially affect dogs' subsequent sleep. In the present study, we manipulated dogs' (N = 15, in a within subject design) sleep structure by specifically disrupting REM versus Non-REM sleep, while maintaining equal sleep efficiency (monitored via non-invasive polysomnography). We found that both the number of awakenings as well as relative Non-REM (but not relative REM) duration influenced dogs' viewing patterns in a task where sad and happy human faces were simultaneously projected with sad or happy human voice playbacks. In accordance with the emotion laterality hypothesis, the interaction between sound valence and Non-REM sleep duration was specific to images projected to the left (regardless of image-sound congruency). These results reveal the first evidence of a causal link between sleep structure and inter-specific emotion-processing in the family dog.
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http://dx.doi.org/10.1038/s41598-020-67092-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7319983PMC
June 2020

A Preliminary Study to Investigate the Genetic Background of Longevity Based on Whole-Genome Sequence Data of Two Methuselah Dogs.

Front Genet 2020 16;11:315. Epub 2020 Apr 16.

Department of Ethology, ELTE Eötvös Loránd University, Budapest, Hungary.

Aging is the largest risk factor in many diseases and mortality alike. As the elderly population is expected to increase at an accelerating rate in the future, these phenomena will pose a growing socio-economic burden on societies. To successfully cope with this challenge, a deeper understanding of aging is crucial. In many aspects, the companion dog is an increasingly popular model organism to study aging, with the promise of producing results that are more applicable to humans than the findings that come from the studies of classical model organisms. In this preliminary study we used the whole-genome sequence of two extremely old dogs - age: 22 and 27 years (or 90-135% more, than the average lifespan of dogs) - in order to make the first steps to understand the genetic background of extreme longevity in dogs. We identified more than ∼80 1000 novel SNPs in the two dogs (7500 of which overlapped between them) when compared to three publicly available canine SNP databases, which included SNP information from850 dogs. Most novel mutations (∼52000 SNPs) were identified at non-coding regions, while 4.6% of the remaining SNPs (n∼1600) were at exons, including 670 missense variants - 76 of which overlapped between the two animals - across 472 genes. Based on their gene ontologies, these genes were related - among others - to gene transcription/translation and its regulation, to immune response and the nervous system in general. We also detected 12 loss-of-function mutations, although their actual effect is unclear. Several genetic pathways were also identified, which pathways may be tempting candidates to be investigated in large sample sizes in order to confirm their relevance in extreme longevity in dogs (and possibly, in humans). We hypothesize a possible link between extreme longevity and the regulation of gene transcription/translation, which hypothesis should be further investigated in the future. This phenomenon could define an interesting direction for future research aiming to better understand longevity. The presented preliminary results highlight the utility of the companion dog in the study of the genetic background of longevity and aging.
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http://dx.doi.org/10.3389/fgene.2020.00315DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7176982PMC
April 2020

Comparison of Behavior and Genetic Structure in Populations of Family and Kenneled Beagles.

Front Vet Sci 2020 15;7:183. Epub 2020 Apr 15.

Department of Ethology, ELTE Eötvös Loránd University, Budapest, Hungary.

In dogs, the social and spatial restriction associated with living in a kennel environment could lead to chronic stress and the development of abnormal behaviors ("kennel-dog syndrome"). However, little is known about how kenneled dogs differ from their conspecifics living as pets in human families. In the current study, using a test battery exposing the dogs to novel stimuli, we compared the behavior of three groups of beagles: (1) kenneled dogs living in a restricted environment with limited human contact ( = 78), (2) family dogs living in human families as pets ( = 37), and (3) adopted dogs born in the kenneled population but raised in human families ( = 13). We found one factor comprising most of the test behaviors, labeled as Responsiveness. Family dogs and adopted dogs scored higher in Responsiveness than kenneled dogs. However, 23% of the kenneled dogs were comparable to family and adopted dogs based on a cluster analysis, indicating a similar (positive) reaction to novel stimuli, while 77% of the kenneled dogs were unresponsive (mostly immobile) in at least part of the test. To assess if the behavioral difference between the family and kenneled dogs could be due to genetic divergence of these two populations and/or to lower genetic diversity of the kenneled dogs, we analyzed their genetic structure using 11 microsatellite markers. We found no significant difference between the populations in their genetic diversity (i.e., heterozygosity, level of inbreeding), nor any evidence that the family and kenneled populations originated from different genetic pools. Thus, the behavior difference between the groups more likely reflects a G × E interaction, that is, the influence of specific genetic variants manifesting under specific environmental conditions (kennel life). Nevertheless, some kenneled individuals were (genetically) more resistant to social and environmental deprivation. Selecting for such animals could strongly improve the welfare of kenneled dog populations. Moreover, exploring the genetic background of their higher resilience could also help to better understand the genetics behind stress- and fear-related behaviors.
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http://dx.doi.org/10.3389/fvets.2020.00183DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7174610PMC
April 2020

Assistance and Therapy Dogs Are Better Problem Solvers Than Both Trained and Untrained Family Dogs.

Front Vet Sci 2020 31;7:164. Epub 2020 Mar 31.

Department of Ethology, Institute of Biology, ELTE Eötvös Loránd University, Budapest, Hungary.

When faced with unsolvable or difficult situations dogs use different behavioral strategies. If they are motivated to obtain rewards, they either try to solve the problem on their own or tend to interact with a human partner. Based on the observation that in problem situations less successful and less perseverant dogs look more at the humans' face, some authors claim that the use of social strategies is detrimental to attempting an independent solution in dogs. Training may have an effect on dogs' problem-solving performance. We compared the behavior of (1) untrained, (2) trained for recreational purposes, and (3) working dogs: assistance and therapy dogs living in families ( = 90). During the task, dogs had to manipulate an apparatus with food pellets hidden inside. We measured the behaviors oriented toward the apparatus and behaviors directed at the owner/experimenter, and ran a principal component analysis. All measures loaded in one factor representing the use of the social strategy over a more problem-oriented strategy. Untrained dogs obtained the highest social strategy scores, followed by dogs trained for recreational purposes, and assistance and therapy dogs had the lowest scores. We conclude that assistance and therapy dogs' specific training and working experience (i.e., to actively help people) favors their independent and more successful problem-solving performance. General training (mainly obedience and agility in this study) also increases problem-oriented behavior.
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http://dx.doi.org/10.3389/fvets.2020.00164DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7145387PMC
March 2020

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

Sci Rep 2020 04 16;10(1):6505. Epub 2020 Apr 16.

Department of Ethology, Eötvös Loránd University, Budapest, Hungary.

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.
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http://dx.doi.org/10.1038/s41598-020-63573-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7162895PMC
April 2020

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

Front Behav Neurosci 2020 3;14:25. Epub 2020 Mar 3.

Department of Ethology, Eötvös Loránd Univesity, Budapest, Hungary.

Dogs are looking at and gaining information from human faces in a variety of contexts. Next to behavioral studies investigating the topic, recent fMRI studies reported face sensitive brain areas in dogs' temporal cortex. However, these studies used whole heads as stimuli which contain both internal (eyes, nose, mouth) and external facial features (hair, chin, face-outline). Behavioral studies reported that (1) recognition of human faces by dogs requires visibility of head contour and that (2) dogs are less successful in recognizing their owners from 2D pictures than from real human heads. In contrast, face perception in humans heavily depends on internal features and generalizes to 2D images. Whether putative face sensitive regions in dogs have comparable properties to those of humans has not been tested so far. In two fMRI experiments, we investigated (1) the location of putative face sensitive areas presenting only internal features of a real human face vs. a mono-colored control surface and (2) whether these regions show higher activity toward live human faces and/or static images of those faces compared to scrambled face images, all with the same outline. In Study 1 ( = 13) we found strong activity for faces in multiple regions, including the previously described temporo-parietal and occipital regions when the control was a mono-colored, homogeneous surface. These differences disappeared in Study 2 ( = 11) when we compared faces to scrambled faces, controlling for low-level visual cues. Our results do not support the assumption that dogs rely on a specialized brain region for processing internal facial characteristics, which is in line with the behavioral findings regarding dogs inability to recognize human faces based on these features.
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http://dx.doi.org/10.3389/fnbeh.2020.00025DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7063116PMC
March 2020

Cross-Sectional Age Differences in Canine Personality Traits; Influence of Breed, Sex, Previous Trauma, and Dog Obedience Tasks.

Front Vet Sci 2019 14;6:493. Epub 2020 Jan 14.

Department of Ethology, Eötvös Loránd University, Budapest, Hungary.

The dog has been suggested as a possible model for personality development over the lifespan, however, we know little about how aging may shape their personality or the magnitude of age-related changes. Previously we established that aging influences multiple dog demographics, which could also affect how personality traits change across different age periods. A demographic questionnaire and the Dog Personality Questionnaire were completed for a cross-sectional sample of 1,207 adult dogs living in Hungary (M = 7.71, SD = 4.12), split into six different age groups. Results revealed three of the five factors showed significant age effects. Activity/Excitability decreased with age, and whilst Responsiveness to training also decreased, only dogs older than 12 years differed significantly from the other groups. Aggressiveness toward animals showed a quadratic trajectory peaking in dogs aged 6-10 years. The greatest magnitude of age-related change was detected between late senior and geriatric ages, likely caused by compensatory behavioral changes to biological aging and owner attitudes to aging. When the models were re-run including the other explanatory variables, age group was no longer significant for the Responsiveness to training trait. The amount of time spent interacting/playing with the owner partially mediated the relationship between age and this trait, implying that interventions to increase play and training motivation may alleviate the negative effects of aging on dogs' trainability. Fifteen out of 28 explanatory variables were significantly associated with at least one of the five factors [weight, breed (pure/mixed breed), sex, off-leash activity, diet, previous trauma, age of dog when arrived in the household, play, dog training activities, number of known commands and dog obedience tasks]. Similarly to humans, dogs that had previously experienced trauma scored higher in fearfulness and aggression. A higher level of basic obedience was linked to some desirable dog personality traits (lower Fearfulness and Aggression, and higher Activity/Excitability and Responsiveness to training). Regardless of the direction of this relationship, obedience is an important aspect contributing to dog personality questionnaires and the dog-owner relationship. This study is unique in that it considered a wide variety of demographic variables which are influenced by aging.
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http://dx.doi.org/10.3389/fvets.2019.00493DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6971055PMC
January 2020

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

PLoS One 2020 3;15(1):e0227253. Epub 2020 Jan 3.

Department of Ethology, Eötvös Loránd University, Budapest, Hungary.

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.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0227253PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6941818PMC
May 2020

Age-related positivity effect on behavioural responses of dogs to human vocalisations.

Sci Rep 2019 12 27;9(1):20201. Epub 2019 Dec 27.

Department of Ethology, Eötvös Loránd University, Budapest, 1117, Hungary.

Age-related changes in the brain can alter how emotions are processed. In humans, valence specific changes in attention and memory were reported with increasing age, i.e. older people are less attentive toward and experience fewer negative emotions, while processing of positive emotions remains intact. Little is yet known about this "positivity effect" in non-human animals. We tested young (n = 21, 1-5 years) and old (n = 19, >10 years) family dogs with positive (laugh), negative (cry), and neutral (hiccup, cough) human vocalisations and investigated age-related differences in their behavioural reactions. Only dogs with intact hearing were analysed and the selected sound samples were balanced regarding mean and fundamental frequencies between valence categories. Compared to young dogs, old individuals reacted slower only to the negative sounds and there was no significant difference in the duration of the reactions between groups. The selective response of the aged dogs to the sound stimuli suggests that the results cannot be explained by general cognitive and/or perceptual decline. and supports the presence of an age-related positivity effect in dogs, too. Similarities in emotional processing between humans and dogs may imply analogous changes in subcortical emotional processing in the canine brain during ageing.
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http://dx.doi.org/10.1038/s41598-019-56636-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6934484PMC
December 2019

The role of common ancestry and gene flow in the evolution of human-directed play behaviour in dogs.

J Evol Biol 2020 03 4;33(3):318-328. Epub 2019 Dec 4.

Department of Zoology, Stockholm University, Stockholm, Sweden.

Among-population variance of phenotypic traits is of high relevance for understanding evolutionary mechanisms that operate in relatively short timescales, but various sources of nonindependence, such as common ancestry and gene flow, can hamper the interpretations. In this comparative analysis of 138 dog breeds, we demonstrate how such confounders can independently shape the evolution of a behavioural trait (human-directed play behaviour from the Dog Mentality Assessment project). We combined information on genetic relatedness and haplotype sharing to reflect common ancestry and gene flow, respectively, and entered these into a phylogenetic mixed model to partition the among-breed variance of human-directed play behaviour while also accounting for within-breed variance. We found that 75% of the among-breed variance was explained by overall genetic relatedness among breeds, whereas 15% could be attributed to haplotype sharing that arises from gene flow. Therefore, most of the differences in human-directed play behaviour among breeds have likely been caused by constraints of common ancestry as a likely consequence of past selection regimes. On the other hand, gene flow caused by crosses among breeds has played a minor, but not negligible role. Our study serves as an example of an analytical approach that can be applied to comparative situations where the effects of shared origin and gene flow require quantification and appropriate statistical control in a within-species/among-population framework. Altogether, our results suggest that the evolutionary history of dog breeds has left remarkable signatures on the among-breed variation of a behavioural phenotype.
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http://dx.doi.org/10.1111/jeb.13567DOI Listing
March 2020

Genetic Pathways of Aging and Their Relevance in the Dog as a Natural Model of Human Aging.

Front Genet 2019 18;10:948. Epub 2019 Oct 18.

Department of Ethology, Eötvös Loránd University, Budapest, Hungary.

Aging research has experienced a burst of scientific efforts in the last decades as the growing ratio of elderly people has begun to pose an increased burden on the healthcare and pension systems of developed countries. Although many breakthroughs have been reported in understanding the cellular mechanisms of aging, the intrinsic and extrinsic factors that contribute to senescence on higher biological levels are still barely understood. The dog, , has already served as a valuable model of human physiology and disease. The possible role the dog could play in aging research is still an open question, although utilization of dogs may hold great promises as they naturally develop age-related cognitive decline, with behavioral and histological characteristics very similar to those of humans. In this regard, family dogs may possess unmatched potentials as models for investigations on the complex interactions between environmental, behavioral, and genetic factors that determine the course of aging. In this review, we summarize the known genetic pathways in aging and their relevance in dogs, putting emphasis on the yet barely described nature of certain aging pathways in canines. Reasons for highlighting the dog as a future aging and gerontology model are also discussed, ranging from its unique evolutionary path shared with humans, its social skills, and the fact that family dogs live together with their owners, and are being exposed to the same environmental effects.
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http://dx.doi.org/10.3389/fgene.2019.00948DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6813227PMC
October 2019

Resting-state fMRI data of awake dogs (Canis familiaris) via group-level independent component analysis reveal multiple, spatially distributed resting-state networks.

Sci Rep 2019 10 24;9(1):15270. Epub 2019 Oct 24.

Eötvös Loránd University, Department of Ethology, Budapest, 1117, Hungary.

Resting-state networks are spatially distributed, functionally connected brain regions. Studying these networks gives us information about the large-scale functional organization of the brain and alternations in these networks are considered to play a role in a wide range of neurological conditions and aging. To describe resting-state networks in dogs, we measured 22 awake, unrestrained individuals of both sexes and carried out group-level spatial independent component analysis to explore whole-brain connectivity patterns. In this exploratory study, using resting-state functional magnetic resonance imaging (rs-fMRI), we found several such networks: a network involving prefrontal, anterior cingulate, posterior cingulate and hippocampal regions; sensorimotor (SMN), auditory (AUD), frontal (FRO), cerebellar (CER) and striatal networks. The network containing posterior cingulate regions, similarly to Primates, but unlike previous studies in dogs, showed antero-posterior connectedness with involvement of hippocampal and lateral temporal regions. The results give insight into the resting-state networks of awake animals from a taxon beyond rodents through a non-invasive method.
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http://dx.doi.org/10.1038/s41598-019-51752-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6813298PMC
October 2019

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

Sci Rep 2019 07 12;9(1):10092. Epub 2019 Jul 12.

Department of Ethology, Eötvös Loránd University, Budapest, Hungary.

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.
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http://dx.doi.org/10.1038/s41598-019-46434-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6626048PMC
July 2019