Potential interactive effect of positive expectancy violation and sleep on memory consolidation in dogs.

In dogs, as in humans, both emotional and learning pretreatment affect subsequent behaviour and sleep. Although learning often occurs in an emotional-social context, the emotion-learning interplay in such context remain mainly unknown. Aims were to assess the effects of Controlling versus Permissive (emotional factors) training (learning factors) styles on dogs' behaviour, learning performance, and sleep. Family dogs (N = 24) participated in two command learning sessions employing the two training styles with each session followed by assessment of learning performance, a 2-h-long non-invasive sleep EEG measurement, and a retest of learning performance. Pre- to post-sleep improvement in learning performance was evident in dogs that received the Permissive training during the second learning session, indicating that dogs that experienced a more rewarding situation than expected (positive expectancy violation) during the second training session showed improved learning success after their afternoon sleep. These results possibly indicate an interactive effect of expectancy violation and sleep on enhancing learning.

Development of a human-analogue, 3-symptom domain Dog ADHD and Functionality Rating Scale (DAFRS).

The family dog, in its natural environment, exhibits neuropsychological deficits redolent of human psychiatric disorders, including behaviours that are similar to human attention-deficit/hyperactivity disorder (ADHD) symptoms. Based on standard questionnaire methods in humans, we aimed to develop and validate a detailed, psychometrically improved tool to assess owner views on relevant dog behaviours. We modified available questionnaires by adding items that allow for separate analysis of impulsivity, and items on functional impairment. We collected data from 1168 owners for different validation steps of the new questionnaire and, similarly to assessment of humans where teachers also evaluate as an expert control, we collected data from dog trainers. Exploratory and confirmatory factor analysis revealed 3 factors: inattention (IA), hyperactivity (H) and impulsivity (I), corresponding to all three human symptom dimensions in dogs. Test-retest analyses showed excellent agreement between measurements for all factors. Similarly to findings with humans, trainer-owner rating comparisons showed fair (IA) to moderate (H, I) agreement. As in humans, greater ADHD scores were associated with greater functional impairment scores. We suggest that in dogs, similarly to humans, parallel examination of (extreme) ADHD and functional impairment scores could help distinguish diagnosable individuals, after further validation of the questionnaire using a relevant behaviour test.

Dogs outperform cats both in their testability and relying on human pointing gestures: a comparative study.

The dog is a so far unique species to study interspecific communication and a promising evolutionary model for preverbal human communication. Recently cats were reported to show some similar skills to dogs. Here we directly compared both the testability and the success of companion dogs and cats in relying on human distal pointing gestures. Due to differences in their domestication, social and ecological background, and developmental processes, we expected better performance from dogs compared to cats. Using an object-choice task, cats made considerably fewer choices than dogs in the laboratory environment, and their tendency to make a choice declined during trials. They were slightly more testable at home, where their willingness to choose did not decrease over time. Dogs made more successful choices than cats, both at the group and individual level, irrespective of the type of the pointing gesture. Older cats were more successful. Despite the two species' rather similar role nowadays as human companions, our results support previous findings suggesting that, compared to the dog, the cat is a less ideal model to study some human communicative abilities in a laboratory environment.

Comment on "Human-directed attachment behaviour in wolves suggests standing ancestral variation for human-dog attachment bonds".

In their recent paper, Hansen Wheat et al. (Ecology and Evolution, 2022, 12, e9299) claimed that hand raised 23-week-old wolves showed the same attachment behaviour towards their handler in the Strange Situation Test (SST) (Determinants of infant behavior, 1969, 4, 111) as dogs. At first glance, their results seem to contradict previous findings that domestication caused a unique change in social-affiliative behaviours in dogs (Animal Behaviour, 2005, 70, 1367). We argue that no persuading evidence was presented to claim that "wolves can show attachment behaviours towards humans comparable to those of dogs". When dealing with a behaviour system (Child Development, 1977, 48, 1184), the subjects' behaviour must meet consistent criteria (Behavioural and Brain Science, 1978, 3, 417), and a few behavioural preferences should not be used to claim the presence of an attachment system, especially, if the experiment violates basic assumptions of the original test. We believe the intriguing scientific question is whether the dog-owner relationship is qualitatively different from what could be observed in the wolf-hand raiser relation. Assessing all available data, our answer is still yes; dogs are unique in this respect.

Event-related potentials indicate differential neural reactivity to species and valence information in vocal stimuli in sleeping dogs.

Dogs live in a complex social environment where they regularly interact with conspecific and heterospecific partners. Awake dogs are able to process a variety of information based on vocalisations emitted by dogs and humans. Whether dogs are also able to process such information while asleep, is unknown. In the current explorative study, we investigated in N = 13 family dogs, neural response to conspecific and human emotional vocalisations. Data were recorded while dogs were asleep, using a fully non-invasive event-related potential (ERP) paradigm. A species (between 250-450 and 600-800 ms after stimulus onset) and a species by valence interaction (between 550 to 650 ms after stimulus onset) effect was observed during drowsiness. A valence (750-850 ms after stimulus onset) and a species x valence interaction (between 200 to 300 ms and 450 to 650 ms after stimulus onset) effect was also observed during non-REM specific at the Cz electrode. Although further research is needed, these results not only suggest that dogs neurally differentiate between differently valenced con- and heterospecific vocalisations, but they also provide the first evidence of complex vocal processing during sleep in dogs. Assessment and detection of ERPs during sleep in dogs appear feasible.

Representation of rewards differing in their hedonic valence in the caudate nucleus correlates with the performance in a problem-solving task in dogs (Canis familiaris).

We have investigated dogs' (Canis familiaris) abilities in associating different sounds with appetitive stimuli of different incentive values. The association's establishment was first tested on family dogs (n = 20) in a problem-solving behavioural paradigm (experiment 1), then in a problem-solving behavioural paradigm as well as an fMRI study on specially trained family dogs (n = 20) (experiment 2). The aim was to show behavioural and parallel neural effects of the association formed between the two sounds and two different associated appetitive stimuli. The latency of solving the problem was considered an indicator of the motivational state. In our first experiment, where only behaviour was studied, we found that dogs were quicker in solving a problem upon hearing the sound associated with food higher in reward value, suggesting that they have successfully associated the sounds with the corresponding food value. In our second experiment, this behaviour difference was not significant. In the fMRI study, the cerebral response to the two sounds was compared both before and after the associative training. Two bilateral regions of interest were explored: the caudate nucleus and the amygdala. After the associative training, the response in the caudate nucleus was higher to the sound related to a higher reward value food than to the sound related to a lower reward value food, which difference was not present before the associative training. We found an increase in the amygdala response to both sounds after the training. In a whole-brain representational similarity analysis, we found that cerebral patterns in the caudate nucleus to the two sounds were different only after the training. Moreover, we found a positive correlation between the dissimilarity index in the caudate nucleus for activation responses to the two sounds and the difference in latencies (i.e. high reward value associated sound condition latency-low reward value associated sound condition latency) to solve the behavioural task: the bigger the difference between the conditions in latency to solve the task, the greater the difference in the neural representation of the two sounds was. In summary, family dogs' brain activation patterns reflected their expectations based on what they learned about the relationship between two sounds and their associated appetitive stimuli.

Dog brains are sensitive to infant- and dog-directed prosody.

When addressing preverbal infants and family dogs, people tend to use specific speech styles. While recent studies suggest acoustic parallels between infant- and dog-directed speech, it is unclear whether dogs, like infants, show enhanced neural sensitivity to prosodic aspects of speech directed to them. Using functional magnetic resonance imaging on awake unrestrained dogs we identify two non-primary auditory regions, one that involve the ventralmost part of the left caudal Sylvian gyrus and the temporal pole and the other at the transition of the left caudal and rostral Sylvian gyrus, which respond more to naturalistic dog- and/or infant-directed speech than to adult-directed speech, especially when speak by female speakers. This activity increase is driven by sensitivity to fundamental frequency mean and variance resulting in positive modulatory effects of these acoustic parameters in both aforementioned non-primary auditory regions. These findings show that the dog auditory cortex, similarly to that of human infants, is sensitive to the acoustic properties of speech directed to non-speaking partners. This increased neuronal responsiveness to exaggerated prosody may be one reason why dogs outperform other animals when processing speech.

Factors Contributing to Successful Spontaneous Dog-Human Cooperation.

Dogs' ability to cooperate with humans is widely acknowledged, but the factors influencing their spontaneous cooperative tendencies are largely unknown. We investigated whether breed function, training experience, and owner-reported social motivation level contribute to spontaneous dog-owner cooperation. Family dogs (N = 100) of three breed groups (non-working dogs, cooperative/independent working breeds) with various training experiences were tested in an 'out-of-reach' task with their owners as their partners, who never directly asked for help during the test. We measured dogs' behaviour along three main components of successful cooperation: paying attention, understanding the problem, and willingness to cooperate. Breed groups had no significant effect on dogs' behaviour. No factor was associated with the behavioural variables related to not understanding the task. Dogs with high training levels and high social motivation showed more attention-related behaviours and were more likely to help the owner (training level and social motivation were not correlated with each other). Our results highlight the importance of training experience and social motivation in dogs' attentiveness and spontaneous cooperativity. This also points to the need for careful sample balancing and experimental procedures that do not rely on specific trained skills.

Central nodes of canine functional brain networks are concentrated in the cingulate gyrus.

Compared to the field of human fMRI, knowledge about functional networks in dogs is scarce. In this paper, we present the first anatomically-defined ROI (region of interest) based functional network map of the companion dog brain. We scanned 33 awake dogs in a "task-free condition". Our trained subjects, similarly to humans, remain willingly motionless during scanning. Our goal is to provide a reference map with a current best estimate for the organisation of the cerebral cortex as measured by functional connectivity. The findings extend a previous spatial ICA (independent component analysis) study (Szabo et al. in Sci Rep 9(1):1.25. https://doi.org/10.1038/s41598-019-51752-2 , 2019), with the current study including (1) more subjects and (2) improved scanning protocol to avoid asymmetric lateral distortions. In dogs, similarly to humans (Sacca et al. in J Neurosci Methods. https://doi.org/10.1016/j.jneumeth.2021.109084 , 2021), ageing resulted in increasing framewise displacement (i.e. head motion) in the scanner. Despite the inherently different approaches between model-free ICA and model-based ROI, the resulting functional networks show a remarkable similarity. However, in the present study, we did not detect a designated auditory network. Instead, we identified two highly connected, lateralised multi-region networks extending to non-homotropic regions (Sylvian L, Sylvian R), including the respective auditory regions, together with the associative and sensorimotor cortices and the insular cortex. The attention and control networks were not split into two fully separated, dedicated networks. Overall, in dogs, fronto-parietal networks and hubs were less dominant than in humans, with the cingulate gyrus playing a central role. The current manuscript provides the first attempt to map whole-brain functional networks in dogs via a model-based approach.

Spontaneous action matching in dog puppies, kittens and wolf pups.

We investigated the spontaneous tendency of dog puppies, kittens and wolf pups to match their behaviour to actions demonstrated by a human, in the absence of food reward. Based on dogs' inherent sociality and domestication history, we predicted that the tendency to match human actions is more pronounced in this species than in the other two. To test this, we exposed N = 42 dog puppies, N = 39 kittens and N = 8 wolf pups to ostensive human demonstrations of an object-related action. We found that dog puppies paid more attention to the demonstration than kittens and wolf pups. Dog puppies and wolf pups matched the demonstrated actions in more trials than kittens. Dog puppies also tended to reproduce the human demonstration that differed from the action they typically preformed in the absence of demonstration. These results support that dog puppies show a tendency to attend to humans and conform their behaviour to human demonstrations in the absence of extrinsic food rewards. This spontaneous tendency is also relevant for practical applications, by providing the basis to devise puppy-training methods that rely less on food rewards, and instead exploit puppies' natural predisposition for social learning.

Owner-rated hyperactivity/impulsivity is associated with sleep efficiency in family dogs: a non-invasive EEG study.

Subjective sleep disturbances are reported by humans with attention-deficit/hyperactivity disorder (ADHD). However, no consistent objective findings related to sleep disturbances led to the removal of sleep problems from ADHD diagnostic criteria. Dogs have been used as a model for human ADHD with questionnaires validated for this purpose. Also, their sleep physiology can be measured by non-invasive methods similarly to humans. In the current study, we recorded spontaneous sleep EEG in family dogs during a laboratory session. We analyzed the association of sleep macrostructure and deep sleep (NREM) slow-wave activity (SWA) with a validated owner-rated ADHD questionnaire, assessing inattention (IA), hyperactivity/impulsivity (H/I) and total (T) scores. Higher H/I and T were associated with lower sleep efficiency and longer time awake after initial drowsiness and NREM. IA showed no associations with sleep variables. Further, no association was found between ADHD scores and SWA. Our results are in line with human studies in which poor sleep quality reported by ADHD subjects is associated with some objective EEG macrostructural parameters. This suggests that natural variation in dogs' H/I is useful to gain a deeper insight of ADHD neural mechanisms.

Dog and human neural sensitivity to voicelikeness: A comparative fMRI study.

Voice-sensitivity in the auditory cortex of a range of mammals has been proposed to be determined primarily by tuning to conspecific auditory stimuli, but recent human findings indicate a role for a more general tuning to voicelikeness. Vocal emotional valence, a central characteristic of vocalisations, has been linked to the same basic acoustic parameters across species. Comparative neuroimaging revealed that during voice perception, such acoustic parameters modulate emotional valence-sensitivity in auditory cortical regions in both family dogs and humans. To explore the role of voicelikeness in auditory emotional valence-sensitivity across species, here we constructed artificial emotional sounds in two sound categories: voice-like vs. sine-wave sounds, parametrically modulating two main acoustic parameters, f0 and call length. We hypothesised that if mammalian auditory systems are characterised by a general tuning to voicelikeness, voice-like sounds will be processed preferentially, and acoustic parameters for voice-like sounds will be processed differently than for sine-wave sounds - both in dogs and humans. We found cortical areas in both species that responded stronger to voice-like than to sine-wave stimuli, while there were no regions responding stronger to sine-wave sounds in either species. Additionally, we found that in bilateral primary and emotional valence-sensitive auditory regions of both species, the processing of voice-like and sine-wave sounds are modulated by f0 in opposite ways. These results reveal functional similarities between evolutionarily distant mammals for processing voicelikeness and its effect on processing basic acoustic cues of vocal emotions.

Comparing Pears to Apples: Unlike Dogs, Cats Need Habituation before Lab Tests.

Research on the socio-cognitive skills of different species often benefit from comparative experiments, however, the ecology of the species and development of the individuals may differently determine how they react to the same test situation. In this study, our aims were twofold: to observe and compare the spontaneous behaviour of companion cats and dogs in the same novel environment, and to habituate them (if needed) to the novel environment in the presence of their owners and an unfamiliar experimenter. The behaviour of 62 family cats, 31 experienced (which had the opportunity to meet strangers and explore unfamiliar places) and 31 inexperienced cats, and 27 family dogs was compared in an unfamiliar room. The subjects' behaviour was coded during the first five minutes in the presence of two passive persons, their owners, and an unfamiliar experimenter. Then, based on a set of rules, first the owner, and then the experimenter tried to initiate interactions with the subjects and the subjects' willingness to interact was evaluated. To pass the habituation test, subjects were expected to play with the experimenter or accept food from them. All dogs passed the test on the first occasion, while almost 60% of the cats failed. The cats' experience did not play a significant role, in fact, younger cats passed more easily. We found marked differences between dogs and cats in all behavioural variables; compared to dogs, cats spent more time crouching and close to their box, while less time exploring or close to the owner. We did not find a difference in the cats' behaviour based on their experience. Our results support the hypothesis that unlike dogs, cats need extensive habituation in a novel environment. This could partially be explained by the difference in the ecology and/or domestication process of the species, although developmental effects cannot be excluded. Our findings have fundamental consequences not only for the considerations of the testability of cats and on the interpretation of their data collected in the laboratory, but in a more general sense on developing comparative experiments.

Exploring the advantages of using artificial agents to investigate animacy perception in cats and dogs.

Self-propelled motion cues elicit the perception of inanimate objects as animate. Studies usually rely on the looking behaviour of subjects towards stimuli displayed on a screen, but utilizing artificial unidentified moving objects (UMOs) provides a more natural, interactive context. Here, we investigated whether cats and dogs discriminate between UMOs showing animate vs inanimate motion, and how they react to the UMOs' interactive behaviour. Subjects first observed, in turn, the motion of an animate and an inanimate UMO, and then they could move freely for 2 min while both UMOs were present (two-way choice phase). In the following specific motion phase, the animate UMO showed one of three interactive behaviours: pushing a ball, a luring motion, or moving towards the subject (between-subject design). Then, subjects could move freely for 2 min again while the UMO was motionless. At the end, subjects were free to move in the room while the UMO was moving semi-randomly in the room. We found that dogs approached and touched the UMO(s) sooner and more frequently than cats, regardless of the context. In the two-way choice phase, dogs looked at the animate UMO more often, and both species touched the animate UMO more frequently. However, whether the UMO showed playing, luring or assertive behaviour did not influence subjects' behaviour. In summary, both species displayed distinctive behaviour towards the animate UMO, but in dogs, in addition to the physical contact this was also reflected by the looking behaviour. Overall, dogs were more keen to explore and interact with the UMO than cats, which might be due to the general increased stress of cats in novel environments. The findings indicate the importance of measuring multiple behaviours when assessing responses to animacy. The live demonstration using artificial agents provides a unique opportunity to study social perception in nonhuman species.

Chasing perception in domestic cats and dogs.

Chasing motion is often used to study the perception of inanimate objects as animate. When chasing interaction and independent motions between two agents are displayed simultaneously on a screen, we expect observers to quickly perceive and recognise the chasing pattern (because of its familiarity) and turn their attention to the independent motion (novelty effect). In case of isosceles triangles as moving figures, dogs and humans both display this behaviour, but dogs initially preferred to look at the chasing pattern whereas humans started to increase their gaze towards the independent motion earlier. Here, we compared whether family cats perceive moving inanimate objects as animate and whether their looking behaviour is similar to that of small family dogs. We displayed a chasing and independent motion side by side on a screen in two consecutive trials and assessed subjects' looking behaviour towards the motions. Similarly to previous studies, we found that dogs eventually looked longer at the independent motion, but cats preferred to look at the independent motion at the beginning of the video display and only later shifted their attention to the chasing motion. No difference was found in the frequency of gaze alternation of the two species. Thus, although cats discriminate between the chasing and independent motions, it is not clear whether this discrimination is controlled by animate motion cues. The difference may originate from their ecological situation and/or may be explained by specific perceptual mechanisms.

Non-invasive sleep EEG measurement in hand raised wolves.

Sleep research greatly benefits from comparative studies to understand the underlying physiological and environmental factors affecting the different features of sleep, also informing us about the possible evolutionary changes shaping them. Recently, the domestic dog became an exceedingly valuable model species in sleep studies, as the use of non-invasive polysomnography methodologies enables direct comparison with human sleep data. In this study, we applied the same polysomnography protocol to record the sleep of dog's closest wild relative, the wolf. We measured the sleep of seven captive (six young and one senior), extensively socialized wolves using a fully non-invasive sleep EEG methodology, originally developed for family dogs. We provide the first descriptive analysis of the sleep macrostructure and NREM spectral power density of wolves using a completely non-invasive methodology. For (non-statistical) comparison, we included the same sleep data of similarly aged dogs. Although our sample size was inadequate to perform statistical analyses, we suggest that it may form the basis of an international, multi-site collection of similar samples using our methodology, allowing for generalizable, unbiased conclusions. As we managed to register both macrostructural and spectral sleep data, our procedure appears to be suitable for collecting valid data in other species too, increasing the comparability of non-invasive sleep studies.

Evaluating ADHD Assessment for Dogs: A Replication Study.

The family dog, in its natural environment, exhibits neuropsychological deficits redolent of human psychiatric disorders, including behaviours similar to human Attention-Deficit/Hyperactivity Disorder (ADHD) symptoms. For dogs, Vas and colleagues developed a 13-item questionnaire to measure inattention and hyperactivity/impulsivity (Dog ARS; 2007). We re-assessed, in a large sample of dogs (N = 319), psychometric properties of the Dog ARS, to identify possible limitations as a basis for further development. We examined the cross-study stability of factor structure and 40-day temporal stability of item and subscale scores and compared owner-report with expert (dog trainer)-report (n = 86), paralleling human parent/teacher assessments. To identify ambiguous items, we administered a modified version (including "I don't know" options, N = 520) to a different sample. We could replicate the factor structure with evidence of good internal consistency and test-retest reliability of both subscales. Agreement between owner and trainer ratings was fair (inattention) and moderate (hyperactivity/impulsivity). Three ambiguous items were identified. Overall, we claim that the Dog ARS is a reliable tool to assess ADHD-like behaviour in dogs, but in its current form, it is not suitable to detect diagnosable individuals, as it does not comprise items assessing functional impairment, and also, the inclusion of owner-expert ratings in the evaluation process would be necessary.

Attachment towards the Owner Is Associated with Spontaneous Sleep EEG Parameters in Family Dogs.

Affective neuroscience studies have demonstrated the impact of social interactions on sleep quality. In humans, trait-like social behaviors, such as attachment, are related to sleep brain activity patterns. Our aim was to investigate associations between companion dogs' spontaneous brain activity during sleep (in the presence of the owner) and their relevant behavior in a task-free social context assessing their attachment towards the owner. In random order, each dog participated in a non-invasive sleep electroencephalogram (EEG) measurement and in the Strange Situation Test (SST) to assess their attachment behavior. We found that higher attachment scores were associated with more time spent in NREM sleep, lower NREM alpha power activity and lower NREM alpha-delta anticorrelation. Our results reveal that, when dogs sleep in a novel environment in the company of their owners, differences in their attachment are reflected in their sleep EEG characteristics. This could be best explained by the different degree that owners could be used as a safe haven in an unfamiliar environment and during the unusual procedure of the first EEG measurement.

Differences in dogs' event-related potentials in response to human and dog vocal stimuli; a non-invasive study.

Recent advances in the field of canine neuro-cognition allow for the non-invasive research of brain mechanisms in family dogs. Considering the striking similarities between dog's and human (infant)'s socio-cognition at the behavioural level, both similarities and differences in neural background can be of particular relevance. The current study investigates brain responses of n = 17 family dogs to human and conspecific emotional vocalizations using a fully non-invasive event-related potential (ERP) paradigm. We found that similarly to humans, dogs show a differential ERP response depending on the species of the caller, demonstrated by a more positive ERP response to human vocalizations compared to dog vocalizations in a time window between 250 and 650 ms after stimulus onset. A later time window between 800 and 900 ms also revealed a valence-sensitive ERP response in interaction with the species of the caller. Our results are, to our knowledge, the first ERP evidence to show the species sensitivity of vocal neural processing in dogs along with indications of valence sensitive processes in later post-stimulus time periods.